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GENERAL ASPECTS

c h a p t e r o n e

INTRODUCTION

3

PROLOGUE: THE ISSUES4

PLANTS AND DISEASE4

HISTORY OF PLANT PATHOLOGY AND EARLY SIGNIFICANT PLANT DISEASES8

LOSSES CAUSED BY PLANT DISEASES29

PLANT PATHOLOGY IN THE 20TH CENTURY46

PLANT PATHOLOGY TODAY AND FUTURE DIRECTIONS54

WORLDWIDE DEVELOPMENT OF PLANT PATHOLOGY AS A PROFESSION60

PLANT PATHOLOGY’S CONTRIBUTION TO CROPS AND SOCIETY65

BASIC PROCEDURES IN THE DIAGNOSIS OF PLANT DISEASES72

4 1. INTRODUCTION

PROLOGUE: THE ISSUES

Plant pathology is a science that studies plant diseasesand attempts to improve the chances for survival ofplants when they are faced with unfavorable envi-

ronmental conditions and parasitic microorganisms thatcause disease. As such, plant pathology is challenging,interesting, important, and worth studying in its ownright. It is also, however, a science that has a practicaland noble goal of protecting the food available forhumans and animals. Plant diseases, by their presence,prevent the cultivation and growth of food plants insome areas; or food plants may be cultivated and grownbut plant diseases may attack them, destroy parts or allof the plants, and reduce much of their produce, i.e.,food, before they can be harvested or consumed. In thepursuit of its goal, plant pathology is joined by the sci-ences of entomology and weed science.

It is conservatively estimated that diseases, insects,and weeds together annually interfere with the produc-tion of, or destroy, between 31 and 42% of all cropsproduced worldwide (Table 1-1). The losses are usuallylower in the more developed countries and higher in thedeveloping countries, i.e., countries that need food themost. It has been estimated that of the 36.5% averageof total losses, 14.1% are caused by diseases, 10.2% byinsects, and 12.2% by weeds.

Considering that 14.1% of the crops are lost to plantdiseases alone, the total annual worldwide crop lossfrom plant diseases is about $220 billion. To theseshould be added 6–12% losses of crops after harvest,which are particularly high in developing tropical coun-tries where training and resources such as refrigerationare generally lacking. Also, these losses do not includelosses caused by environmental factors such as freezes,droughts, air pollutants, nutrient deficiencies, and toxicities.

Although impressive, the aforementioned numbers donot tell the innumerable stories of large populations in many poor countries suffering from malnutrition,hunger, and starvation caused by plant diseases; or oflost income and lost jobs resulting from crops destroyedby plant diseases, forcing people to leave their farms and

villages to go to overcrowded cities in search of jobs thatwould help them survive.

Moreover, the need for measures to control plant dis-eases limits the amount of land available for cultivationeach year, limits the kinds of crops that can be grownin fields already contaminated with certain microorgan-isms, and annually necessitates the use of millions ofkilograms of pesticides for treating seeds, fumigatingsoils, spraying plants, or the postharvest treatment of fruits. Such control measures not only add to the costof food production, some of them, e.g., crop rotation,necessarily limit the amount of food that can be pro-duced, whereas others add toxic chemicals to the envi-ronment. It is therefore the duty and goal of plantpathology to balance all the factors involved so that the maximum amount of food can be produced with the fewest adverse side effects on the people and theenvironment.

PLANTS AND DISEASE

Plants make up the majority of the earth’s living envi-ronment as trees, grass, flowers, and so on. Directly orindirectly, plants also make up all the food on whichhumans and all animals depend. Even the meat, milk,and eggs that we and other carnivores eat come fromanimals that themselves depend on plants for their food.Plants are the only higher organisms that can convertthe energy of sunlight into stored, usable chemicalenergy in carbohydrates, proteins, and fats. All animals,including humans, depend on these plant substances forsurvival.

Plants, whether cultivated or wild, grow and producewell as long as the soil provides them with sufficientnutrients and moisture, sufficient light reaches theirleaves, and the temperature remains within a certain“normal” range. Plants, however, also get sick. Sickplants grow and produce poorly, they exhibit varioustypes of symptoms, and, often, parts of plants or wholeplants die. It is not known whether diseased plants feelpain or discomfort.

The agents that cause disease in plants are the sameor very similar to those causing disease in humans andanimals. They include pathogenic microorganisms, suchas viruses, bacteria, fungi, protozoa, and nematodes,and unfavorable environmental conditions, such as lackor excess of nutrients, moisture, and light, and the pres-ence of toxic chemicals in air or soil. Plants also sufferfrom competition with other, unwanted plants (weeds),and, of course, they are often damaged by attacks ofinsects. Plant damage caused by insects, humans, orother animals is not usually included in the study ofplant pathology.

TABLE 1-1Estimated Annual Crop Losses Worldwide

Attainable crop production (2002 prices) $1.5 trillionActual crop production (-36.5%) $950 billionProduction without crop protection $455 billionLosses prevented by crop protection $415 billionActual annual losses to world crop production $550 billionLosses caused by diseases only (14.1%) $220 billion

PLANTS AND DISEASE 5

Plant pathology is the study of the organisms and ofthe environmental factors that cause disease in plants;of the mechanisms by which these factors induce diseasein plants; and of the methods of preventing or control-ling disease and reducing the damage it causes. Plantpathology is for plants largely what medicine is forhumans and veterinary medicine is for animals. Eachdiscipline studies the causes, mechanisms, and controlof diseases affecting the organisms with which it deals,i.e., plants, humans, and animals, respectively.

Plant pathology is an integrative science and pro-fession that uses and combines the basic knowledge ofbotany, mycology, bacteriology, virology, nematology,plant anatomy, plant physiology, genetics, molecularbiology and genetic engineering, biochemistry, hor-ticulture, agronomy, tissue culture, soil science, forestry, chemistry, physics, meteorology, and manyother branches of science. Plant pathology profits fromadvances in any one of these sciences, and manyadvances in other sciences have been made in attemptsto solve plant pathological problems.

As a science, plant pathology tries to increase ourknowledge about plant diseases. At the same time, plantpathology tries to develop methods, equipment, andmaterials through which plant diseases can be avoidedor controlled. Uncontrolled plant diseases may result inless food and higher food prices or in food of poorquality. Diseased plant produce may sometimes be poi-sonous and unfit for consumption. Some plant diseasesmay wipe out entire plant species and many affect thebeauty and landscape of our environment. Controllingplant disease results in more food of better quality anda more aesthetically pleasing environment, but con-sumers must pay for costs of materials, equipment, andlabor used to control plant diseases and, sometimes, forother less evident costs such as contamination of theenvironment.

In the last 100 years, the control of plant diseases and other plant pests has depended increasingly on theextensive use of toxic chemicals (pesticides). Controllingplant diseases often necessitates the application of suchtoxic chemicals not only on plants and plant productsthat we consume, but also into the soil, where many path-ogenic microorganisms live and attack the plant roots.Many of these chemicals have been shown to be toxic tonontarget microorganisms and animals and may be toxicto humans. The short- and long-term costs of environ-mental contamination on human health and welfarecaused by our efforts to control plant diseases (and otherpests) are difficult to estimate. Much of modern researchin plant pathology aims at finding other environmentallyfriendly means of controlling plant diseases. The mostpromising approaches in-clude conventional breedingand genetic engineering of disease-resistant plants, appli-

cation of disease-suppressing cultural practices, RNA-and gene-silencing techniques, of plant defense-promoting, nontoxic substances, and, to some extent, useof biological agents antagonistic to the microorganismsthat cause plant disease.

The challenges for plant pathology are to reduce foodlosses while improving food quality and, at the sametime, safeguarding our environment. As the world population continues to increase while arable land andmost other natural resources continue to decrease, andas our environment becomes further congested andstressed, the need for controlling plant diseases effec-tively and safely will become one of the most basicnecessities for feeding the hungry billions of our increas-ingly overpopulated world.

The Concept of Disease in Plants

Because it is not known whether plants feel pain or dis-comfort and because, in any case, plants do not speakor otherwise communicate with us, it is difficult to pin-point exactly when a plant is diseased. It is accepted thata plant is healthy, or normal, when it can carry out itsphysiological functions to the best of its genetic poten-tial. The meristematic (cambium) cells of a healthy plantdivide and differentiate as needed, and different types of specialized cells absorb water and nutrients from the soil; translocate these to all plant parts; carry onphotosynthesis, translocate, metabolize, or store thephotosynthetic products; and produce seed or otherreproductive organs for survival and multiplication.When the ability of the cells of a plant or plant part tocarry out one or more of these essential functions isinterfered with by either a pathogenic organism or anadverse environmental factor, the activities of the cellsare disrupted, altered, or inhibited, the cells malfunctionor die, and the plant becomes diseased. At first, theaffliction is localized to one or a few cells and is invisi-ble. Soon, however, the reaction becomes more wide-spread and affected plant parts develop changes visibleto the naked eye. These visible changes are the symp-toms of the disease. The visible or otherwise measura-ble adverse changes in a plant, produced in reaction toinfection by an organism or to an unfavorable environ-mental factor, are a measure of the amount of disease in the plant. Disease in plants, then, can be defined asthe series of invisible and visible responses of plant cellsand tissues to a pathogenic organism or environmentalfactor that result in adverse changes in the form, func-tion, or integrity of the plant and may lead to partialimpairment or death of plant parts or of the entire plant.

The kinds of cells and tissues that become affecteddetermine the type of physiological function that will be

6 1. INTRODUCTION

disrupted first (Fig. 1-1). For example, infection of rootsmay cause roots to rot and make them unable to absorbwater and nutrients from the soil; infection of xylemvessels, as happens in vascular wilts and in somecankers, interferes with the translocation of water andminerals to the crown of the plant; infection of thefoliage, as happens in leaf spots, blights, rusts, mildews,mosaics, and so on, interferes with photosynthesis; in-fection of phloem cells in the veins of leaves and in the

bark of stems and shoots, as happens in cankers and in diseases caused by viruses, mollicutes, and protozoa,interferes with the downward translocation of photo-synthetic products; and infection of flowers and fruitsinterferes with reproduction. Although infected cells inmost diseases are weakened or die, in some diseases,e.g., in crown gall, infected cells are induced to dividemuch faster (hyperplasia) or to enlarge a great deal more (hypertrophy) than normal cells and to produce

FIGURE 1-1 Schematic representation of the basic functions in a plant (left) and of the kinds ofinterference with these functions (right) caused by some common types of plant diseases.

T

y

PLANTS AND DISEASE 7

abnormal amorphous overgrowths (tumors) or abnor-mal organs.

Pathogenic microorganisms, i.e., the transmissiblebiotic (= living) agents that can cause disease and aregenerally referred to as pathogens, usually cause disease in plants by disturbing the metabolism of plant cellsthrough enzymes, toxins, growth regulators, and othersubstances they secrete and by absorbing foodstuffsfrom the host cells for their own use. Some pathogensmay also cause disease by growing and multiplying inthe xylem or phloem vessels of plants, thereby blockingthe upward transportation of water or the downwardmovement of sugars, respectively, through these tissues.Environmental factors cause disease in plants whenabiotic factors, such as temperature, moisture, mineralnutrients, and pollutants, occur at levels above or belowa certain range tolerated by the plants.

Types of Plant Diseases

Tens of thousands of diseases affect cultivated and wildplants. On average, each kind of crop plant can beaffected by a hundred or more plant diseases. Somepathogens affect only one variety of a plant. Otherpathogens affect several dozen or even hundreds ofspecies of plants. Plant diseases are sometimes groupedaccording to the symptoms they cause (root rots, wilts,leaf spots, blights, rusts, smuts), to the plant organ theyaffect (root diseases, stem diseases, foliage diseases), orto the types of plants affected (field crop diseases, veg-etable diseases, turf diseases, etc.). One useful criterionfor grouping diseases is the type of pathogen that causesthe disease (see Figs. 1-2 and 1-3). The advantage of such a grouping is that it indicates the cause of the disease, which immediately suggests the probable

FIGURE 1-2 Schematic diagram of the shapes and sizes of certain plant pathogensin relation to a plant cell. Bacteria, mollicutes, and protozoa are not found in nucle-ated living plant cells.

8 1. INTRODUCTION

development and spread of the disease and also possi-ble control measures. On this basis, plant diseases in thistext are classified as follows:

I. Infectious, or biotic, plant diseases1. Diseases caused by fungi (Figs. 1-4A and 1-4B)2. Diseases caused by prokaryotes (bacteria and

mollicutes) (Figs. 1-4C and 1-4D)3. Diseases caused by parasitic higher plants (Fig.

1-5A) and green algae4. Diseases caused by viruses and viroids (Fig.

1-5B)5. Diseases caused by nematodes (Fig. 1-5C)6. Diseases caused by protozoa (Fig. 1-5D)

II. Noninfectious, or abiotic, plant diseases (Fig. 10-1)1. Diseases caused by too low or too high a

temperature2. Diseases caused by lack or excess of soil

moisture3. Diseases caused by lack or excess of light4. Diseases caused by lack of oxygen5. Diseases caused by air pollution6. Diseases caused by nutrient deficiencies7. Diseases caused by mineral toxicities8. Diseases caused by soil acidity or alkalinity

(pH)

9. Diseases caused by toxicity of pesticides10. Diseases caused by improper cultural practices

HISTORY OF PLANT PATHOLOGY AND EARLYSIGNIFICANT PLANT DISEASES

Introduction

Even when humans lived as hunters or nomads and theirfood consisted only of meat or leaves, fruit, and seeds,which they picked wherever they could find them, plantdiseases took their toll on hunted animals and onhumans. Plant diseases caused leaves and shoots tomildew and blight, and fruit and seeds to rot, therebyforcing humans to keep looking until they could findenough healthy fruit or food plants of some kind tosatisfy their hunger. As humans settled down and be-came farmers, they began growing one or a few kindsof food plants in small plots of land and depended onthese plants for their survival throughout the year. It isprobable that every year, and in some years more thanin others, part of the crop was lost to diseases. In suchyears food supplies were insufficient and hunger wascommon. In years when wet weather favored the devel-opment of plant diseases, most or all of the crop was

Fungi

PlasmodiumSpore

Morphology

Morphology

Adults Egg Juvenile Protozoa (flagellates)

Dodder Witchweed Dwarf mistletoe Broomrapes

Viroids

Multiplication Spiroplasma

Colony Spores

Bacteria

Mollicutes

Parasitichigherplants

Viruses

Nematodes

Types of mycelium

Morphology and flagellation Fission Streptomyces

FIGURE 1-3 Morphology and ways of multiplication of some of the groups of plant pathogens.

HISTORY OF PLANT PATHOLOGY AND EARLY S IGNIF ICANT PLANT DISEASES 9

destroyed and famines resulted, causing immense suf-fering and probably the death of many humans andanimals from starvation. It is not surprising, therefore,that plant diseases are mentioned in some of the oldest

books available (Homer, c. 1000 b.c., Old Testament, c. 750 b.c.) and were feared as much as human diseasesand war.

FIGURE 1-4 Three types of pathogenic microorganisms that cause plant diseases. (A) Fungus growing out of apiece of infected plant tissue placed in the center of a culture plate containing nutrient medium. (B) Mycelium andspores of a plant pathogenic fungus (Botrytis sp.) (600¥). (C) Bacteria at a stoma of a plant leaf (2500¥). (D) Phyto-plasmas in a phloem cell of a plant (5000¥). [Photographs courtesy of (B) M. F. Brown and H. G. Brotzman, (C) L.Mansvelt, I. M. M. Roos, and M. J. Hattingh, and (D) J. W. Worley.]

BOX 1 Plant diseases as the wrath of gods — theophrastus

The climate and soil of countries aroundthe eastern Mediterranean Sea, fromwhere many of the first records of antiq-uity came to us, allow the growth andcultivation of many plants. The mostimportant crop plants for the survival of

people and of domesticated animalswere seed-producing cereals, especiallywheat, barley, rye, and oats; andlegumes, especially beans, fava beans,chickpeas, and lentils. Fruit trees such asapple, citrus, olives, peaches, and figs, as

well as grapes, melons, and squash, werealso cultivated. All of these crop plantssuffered losses annually due to drought,insects, diseases, and weeds. Becausemost families grew their own crops anddepended on their produce for survival

continued

10 1. INTRODUCTION

FIGURE 1-5 The other four types of pathogens that cause plant disease. (A) Thread-like parasitic higher plantdodder (Cuscuta sp.) parasitizing pepper seedlings. (B) Tobacco ringspot virus isolated from infected tobacco plants(200,000¥). (C) Plant parasitic nematodes (Ditylenchus sp.) isolated from infected onion bulbs (80¥). (D) Protozoa(Phytomonas spp.) in a phloem cell of an oil palm root (4000¥) [Photographs courtesy of (A) G. W. Simone, (C) N.Greco, supplied courtesy R. Inserra, and (D) W. de Sousa].

until the next crop was produced the following year, losses of any amount of crops, regardless of cause, createdserious hunger and survival problems forthem. Occurrences of mildews (Fig. 1-6,see also pages 448–452), blasts (Figs. 1-7 A, 1-7B, 1-8A and 1-8B, see also pages582–591), and blights on cereals (Figs.1-9 A and 1-9B, see also pages 562–571)and legumes (Figs. 1-10A and 1-10B) arementioned in numerous passages ofbooks of the Old Testament (about 750

b.c.) of the Bible. Blasts, probably thesmut diseases, destroyed some or allkernels in a head by replacing them withfungal spores. Blights, probably rusts,weakened the plants and used up thenutrients and water that would fill thekernels, leaving the kernels shriveled andempty (Fig. 1-9B).

Mention of plant diseases is foundagain in the writings of the Greekphilosopher Democritus, who, around470 b.c., noted plant blights and

described a way to control them. It wasnot, however, until another Greekphilosopher, Theophrastus (Fig. 1-11, c.300 b.c.) made plants and, to a muchsmaller extent, plant diseases the objectof a systematic study. Theophrastus wasa pupil of Aristotle and later became hissuccessor in the school. Among others,Theophrastus wrote two books onplants. One, called “The Nature ofPlants,” included chapters on the mor-phology and anatomy of plants and

A


A B

C D

FIGURE 1-6 Powdery mildew symptoms on (A) leaves of young wheat plant, (B) cluster of grape berries, (C) lilacleaf, and (D) azalea plant. [Photographs courtesy of (A) G. Munkvold, Iowa State University, (B) E. Hellman, TexasA&M University, and (C and D) S. Nameth, Ohio State University.]

descriptions of wild and cultivatedwoody plants, perennial herbaceousplants, wild and cultivated vegetableplants, the cereals, which also includedlegumes, and medicinal plants and theirsaps. The other book, called “Reasons ofVegetable Growth,” included chapterson plant propagation from seeds and bygrafting, the environmental changes andtheir effect on plants, cultural practicesand their effect on plants, the origin andpropagation of cereals, unnatural influ-ences, including diseases and death of

plants, and about the odor and the tasteof plants. For these works, Theophras-tus has been considered the “father ofbotany.”

The contributions of Theophrastus tothe knowledge about plant diseases arequite limited and influenced by thebeliefs of his times. He observed thatplant diseases were much more commonand severe in lowlands than on hillsidesand that some diseases, e.g., rusts, weremuch more common and severe oncereals than on legumes. In many of the

early references, plant diseases were con-sidered to be a curse and a punishmentof the people by God for wrongs andsins they had committed. This impliedthat plant diseases could be avoided ifthe people would abstain from sin.Nobody, of course, thought that farmersin the lowlands sinned more than thoseon the hillsides, yet Theophrastus andhis contemporaries, being unable toexplain plant diseases, believed that Godcontrolled the weather that “broughtabout” the disease. They believed that

continued

12 1. INTRODUCTION

BA

FIGURE 1-7 Loose smut (blast) of (A) barley and (B) wheat caused by the fungus Ustilago sp. [Photographs cour-tesy of (A) P. Thomas and (B) I. Evans, WCPD.]

A B

FIGURE 1-8 Cover smut or bunt (blast) of wheat caused by the fungus Tilletia. (A) Plant on the left is healthy;plant on the right shows infected, smaller, rounded, black wheat kernels in glumes spread out. (B) Healthy (lightcolored) and covered smut-infected (dark colored) kernels of wheat. [Photographs courtesy of (A) WCCPD and (B) P. Lipps, Ohio State University.]


A B

FIGURE 1-9 (A) Wheat stems and leaves infected heavily with stem rust of wheat caused by the fungus Pucciniatritici. (B) Wheat kernels from rust-infected plants on the left are thin and almost empty of nutrients compared tokernels on the right from a healthy wheat plant, which are plump, full of starch and other nutrients. [Photographscourtesy of (A) CIMMYT and (B) USDA, Cereal Dis. Lab., St. Paul, MN.]

A B

FIGURE 1-10 Close-up of bean rust caused by the fungus Uromyces appendiculatus. (A) Rust spots on the upperand lower sides of bean leaves. (B) Rust-infected bean plants in the field showing many leaves killed by the rust andfallen off. [Photographs courtesy of (A) R. G. Platford, WCPD, and (B) J. R. Steadman, University of Nebraska.]

continued

14 1. INTRODUCTION

Efforts to control plant diseases were similarly ham-pered by the lack of information on the causes of diseaseand by the belief that diseases were manifestations ofthe wrath of God. Nevertheless, some ancient writers,e.g., Homer (c. 1000 b.c.), mention the therapeuticproperties of sulfur on plant diseases, and Democritus(c. 470 b.c.) recommended controlling plant blights bysprinkling plants with the olive grounds left after extrac-tion of the olive oil. Most ancient reports, however, dealtwith festivals and sacrifices to thank, please, or appeasea god and to keep the god from sending the dreadedrusts, mildews, blasts, or other crop scourges. Very littleinformation on controlling plant diseases was writtenanywhere for almost 2000 years.

During the two millennia of fatalism, a few impor-tant observations were made on the causes and controlof plant diseases, but they were not believed by theircontemporaries and were completely ignored by the gen-erations that followed. It was not until about a.d. 1200that a higher plant, the mistletoe, was proposed as a par-asite that obtains its food from the host plant, which itmakes sick. It was also noted that the host plant can becured by pruning out the part carrying the mistletoe.Nobody, however, followed up on this important observation.

FIGURE 1-11 Theophrastus, the“father of botany.”

plant diseases were a manifestation ofthe wrath of God and, therefore, thatavoidance or control of the diseasedepended on people doing things thatwould please that same superpower. Inthe fourth century b.c.; the Romans suf-fered so much from hunger caused bythe repeated destruction of cereal cropsby rusts and other diseases that theycreated a separate god, whom they

named Robigus. To please Robigus, theRomans offered prayers and sacrifices inthe belief that he would protect themfrom the dreaded rusts. The Romanseven established a special holiday forRobigus, the Robigalia, during whichthey sacrificed red dogs, foxes, and cowsin an attempt to please and pacifyRobigus so he would not send the ruststo destroy their crops.

BOX 2 Mistletoe recognized as the first plant pathogen

Mistletoes are plants that live as para-sites on branches of trees (see pages 715)but, for various reasons, they havecaught the fancy of people in variouscultures and have made a name forthemselves way beyond their real properties.

Although mistletoe is the first plantpathogen to be recognized as such andthe first pathogen for which a culturalcontrol (by pruning affected branches)was recommended, both by AlbertusMagnus (Fig. 1-12A) around 1200 a.d.,a great deal more has been fantasized,

said, written, and practiced about it thanits importance as a pathogen would indi-cate. Mistletoe, to be sure, both thecommon or leafy mistletoe (Viscum inEurope and elsewhere, Phoradendron inNorth America), which infects manydeciduous trees (Figs. 1-12B and 1-12C)and especially the dwarf mistletoes(Arceuthobium), which infects conifers,cause considerable damage to trees theyinfect. In many cases, the evergreenmistletoe plants can be seen clearly afternormal leaf fall in the autumn and makeup as much as half of the top of the

deciduous tree they infect. They gener-ally damage trees by making their trunksand branches swell where they areinfected and then break there duringwindstorms, thereby reducing thesurface of the tree and reducing thequality of timber.

Mistletoes, of course, are evergreenparasitic plants that sink their “roots,”usually called sinkers or haustoria, intobranches of trees. Through the sinkersthey absorb all the water and mineralnutrients and most of the organic sub-stances they need from the plant. True


A

B

C

FIGURE 1-12 (A) Albertus Magnus, who recognized the mistletoe as a plant parasite. (B) Tufts of individual mistle-toe plants growing on branches of an oak tree in winter. (C) Close-up of a mistletoe plant whose main stems aregrowing out of the trunk of an oak tree.

mistletoes, however, have well-devel-oped leaves and chlorophyll and carryon photosynthesis and manufacture atleast some of the sugars and otherorganic substances they need. Mistletoeplants produce separate male and femaleflowers and berry-like fruits containinga single seed. The seeds are coated witha sticky substance and are either forciblyexpelled and stick to branches of nearbytrees or are eaten by birds but gothrough their digestive tract and stick tobranches on which birds drop them.

The striking visibility of true mistle-toes on deciduous trees, and their abilityto remain green while their host leavesfall for the winter, excited the imagina-tion of people since the times of theancient Greeks and inspired many mythsand traditions involving the mistletoe

plant through the centuries. The plantitself was thought to possess mysticalpowers and became associated withmany folklore customs in many coun-tries. It was thought to bestow life andprotect against poison, to act as anaphrodisiac, and to bestow fertility.Mistletoe sprigs placed over house andstable doors or hung from ceilings werebelieved to ward off witches and evilspirits. The Romans decorated theirtemples and houses in midwinter withmistletoe to please the gods to whom itwas sacred. In Nordic mythology, themistletoe was sacred to Frigga, thegoddess of love, but was used by Loki,the goddess of evil, as an arrow andkilled Frigga’s son, the god of thesummer sun. Frigga managed to reviveher son under the mistletoe tree and, in

her joy, she kissed everyone who wasunder the mistletoe tree. But, for itsmisdeed to her son, she condemned themistletoe to, be in the future, a parasiteand to have no power to cause misfor-tune, sorrow, or death. She decreedinstead that anyone standing under amistletoe tree was due not only protec-tion from any harm, but also a kiss, atoken of peace and love. So, in Scandinavia, mistletoe was thought of asa plant of peace: under the mistletoe,enemies could agree on a truce orfeuding spouses could kiss and make up.In England, a ball of mistletoe was dec-orated with ribbons and ornaments andwas hung up at Christmas. If a younglady was standing under the ball, shecould not refuse to be kissed or she couldnot expect to get married the following

continued

16 1. INTRODUCTION

Biology and Plant Pathology in Early Renaissance

People continued to suffer from hunger and malnutri-tion due partially at least to diseases destroying theircrops and their fruit. They, however, continued to con-sider plant diseases as the work and wish of their Godand, therefore, an event that could neither be under-stood nor avoided. In the mid-1600s, however, a groupof French farmers noted that wheat rust was alwaysmore severe on wheat near barberry bushes than awayfrom them (Fig. 1-13). The farmers thought that the rustwas produced by the barberry plants from which itmoved to wheat. They, therefore, asked the French gov-ernment to pass the first plant disease regulatory legis-lation that would force towns to cut and destroy thebarberry bushes to protect the wheat crop.

In 1670, the French physician Thoullier observed thatergotism or Holy Fire, a serious and often deadly diseaseof humans in northcentral Europe (see pages 39 and559), did not spread from one person to another butseemed to be associated with the consumption of ergot-contaminated grains. At about the same time, RobertHooke, in England, invented the double-lensed (com-pound) microscope with which he examined thin slicesof cork and called its units “cells.” Soon after, theDutchman Antonius van Leeuwenhoek (Fig. 1-14A)improved significantly the lenses and the structure of the

microscope and began to examine not only the anatomyof plants, but also the body of filamentous fungi andalgae, protozoa, sperm cells, blood cells, and even bac-teria. All of these microorganisms, of course, were con-sidered to be produced by whatever organism (animal

FIGURE 1-13 A bush of barberry (Berberis vulgaris) growing atthe edge of a wheat field and helping close the dioecious disease cycleof wheat stem rust disease. The fungus, Puccinia graminis, overwin-ters on barberry on which it produces spores that infect wheat plantsnear the barberry (see photo) from which then spores of the fungusspread to more wheat plants. (Photograph courtesy of USDA CerealDis. Lab., St. Paul, MN.)

year. A couple in love that kiss under themistletoe is equivalent to promising tomarry and a prediction of long life andhappiness together. Nowadays, in manyparts of Europe and America, a person

standing under a ball or even a sprig ofmistletoe at Christmastime is inviting tobe kissed by members of the oppositegender as a sign of friendship and good-will. There are, actually, more myths and

customs associated with mistletoe. Whowould think that a minor parasitichigher plant would excite the imagina-tion of so many others and have so manystories about it.

BOX 3 Plant diseases as the result of spontaneous generation

Following Theophrastus, other than theproposal by Magnus that the mistletoewas a parasite, there was little usefulknowledge that was added about plantsor about plant diseases for about 2000years, although there are reports offamines in several parts of the world.Especially bad were outbreaks in north-central Europe of ergotism, a disease ofhumans and animals caused from eatinggrains contaminated with parts of thefungus that causes the ergot disease ofcereals (see pages 501–504). People con-tinued to associate plant diseases withsin and the wrath of God and thereforewere fatalistic about the occurrence of

plant diseases, the repeated losses offood, and the hunger and famines thatfollowed. References to the ravages ofplant diseases appeared in the writingsof several contemporary historians, butlittle was added to the knowledge aboutthe causes and control of plant diseases.People everywhere believed that plantdiseases, as well as human and animaldiseases, just happened spontaneously.Whatever was observed on diseasedplants or on diseased plant produce wasconsidered to be the product or theresult of the disease rather than the causeof it. After the invention of the com-pound microscope in the mid-1600s,

which enabled scientists to see many ofthe previously invisible microorganisms,scientists, as well as laypeople, becameeven stronger believers in the sponta-neous generation of diseases and of themicroorganisms associated with dis-eased or decaying plant, human, oranimal tissues. That is, they came tobelieve that the mildews, rusts, decay, orother symptoms observed on diseasedplants, and any microorganisms foundon or in diseased plant parts, were thenatural products of diseases that justhappened rather than being the causeand effect of the diseases.


or plant) or medium they happened to be found in andwere not thought of as independent, autonomous organ-isms. In 1735, the Swedish philosopher–botanist Carl von Linne’ (Fig. 1-14B) published his main work“Systema Naturae,” by which he established the diag-nosis of plant species and the binomial nomenclature ofplants. Linne’s species, however, were rigid and weresupposed to have remained unchanged since creation. Itwas not until more than a century later, in 1859, thatthe Englishman Charles Darwin (Fig. 1-14C) publishedhis book “The Origin of Species by Means of NaturalSelection” and showed that species of all organisms,plants and animals, evolve over time and adapt tochanges in their environment for survival.

The discovery and availability of the microscope,however, sparked significant interest in microscopicfungi and, subsequently, their possible association withplant diseases. In 1729, the Italian botanist Pier AntonioMicheli described many new genera of fungi and illus-trated their reproductive structures. He also noted thatwhen placed on freshly cut slices of melon, these struc-tures grew and produced the same kind of fungus thathad produced them. He proposed, therefore, that fungiarise from their own spores rather than spontaneously,but because the “spontaneous generation” theory was so imbedded in people’s minds, nobody believedMicheli’s evidence. Similarly, in 1743, the English scientist Needham observed nematodes inside small,

FIGURE 1-14 (A) Antonius van Leeuwenhoek. (B) Carl von Linne’. (C) Charles Darwin.

BA

C

18 1. INTRODUCTION

abnormally rounded wheat kernels but he, too, failed to show or suggest that they were the cause of theproblem.

In 1755, the Frenchman Tillet, working with smuttedwheat, showed that he could increase the number ofwheat plants developing covered smut (Figs. 1-8A and1-8B) by dusting wheat kernels before planting withsmut dust, i.e., with smut spores (Fig. 1-15). He alsonoted that he could reduce the number of smutted wheatplants produced by treating the smut-treated kernels

with copper sulfate. Tillet, too, however, did not inter-pret his experiments properly and, instead of conclud-ing that wheat smut is an infectious plant disease, hebelieved that it was a poisonous substance contained inthe smut dust, rather than the living spores and funguscoming from them, that caused the disease. More than50 years later, in 1807, Prevost, another Frenchman,repeated both the inoculation experiments and those inwhich the seeds were treated with copper sulfate, asdone by Tillet, and he obtained the same results. In addi-tion, Prevost observed smut spores from untreated andtreated wheat seed under the microscope and noticedthat those from untreated seed germinated and grewwhereas those from treated seed failed to germinate. He,therefore, concluded correctly that it was the smutspores that caused the smut disease in wheat and thatthe reduced number of smutted wheat plants derivedfrom copper sulfate-treated seed was due to the inhibi-tion of germination of smut spores by the copper sulfate.Prevost’s conclusions, however, were not accepted by theFrench Academy of Sciences because its scientists andother scientists throughout Europe still believed thatmicroorganisms and their spores formed through spon-taneous generation and were the result rather than thecause of disease. In 1855, a nematode was observed ingalls of cucumber roots, but again they were thought tohave appeared there spontaneously. These beliefs con-tinued to be held and expounded by scientists until theearly 1860s, when, in 1861–1863, Anton deBary (Fig.1-16A) proved that potato late blight was caused by afungus and Louis Pasteur (Fig. 1-16B) proved that microorganisms were produced from preexistingmicroorganisms and that most infectious diseases werecaused by germs. The latter established the “germ theoryof disease,” which changed the way of thinking of sci-entists and led to tremendous progress. Significant

FIGURE 1-15 Teliospores of the fungus Tilletia, the cause of thecovered smut or bunt of wheat. (Photograph courtesy of M.Babadoost, University of Illinois.)

A B C

FIGURE 1-16 (A) Anton deBary. (B) Louis Pasteur. (C) Robert Koch.


impetus to this progress was added by Robert Petri, who developed artificial nutrient media for culturing the microorganisms (Petri dishes), and by Robert Koch (Fig. 1-16C), who established that for proving that a

certain microorganism was the cause of a particularinfectious disease, certain necessary steps (Koch’s postulates) must be carried out and certain conditionsmust be satisfied.

BOX 4 Potato blight and the irish famine: a deadly mix of ignorance and politics

In about 1800, the potato, which wasintroduced in Europe from South andCentral America around 1570 a.d., wasa well-established crop in Ireland. Afterstrong objections against adopting itbecause (1) it was new and not men-tioned in the Bible, (2) it was producedin the ground and, therefore, wasunclean, and (3) because parts of it werepoisonous, the potato was neverthelessadopted and its cultivation spreadrapidly. Adoption of potato cultivationcame as a result of it producing muchmore edible food per unit of land thangrain crops, mostly wheat and rye,grown until then. It was adopted alsobecause the ground protected it from thepests and diseases that destroyed above-ground crops and from destruction bythe soldiers sent by absentee Englishlandlords to collect overdue land rents.

At that time, most Irish farmers wereextremely poor, owned no land, andlived in small windowless, one-roomhuts. The farmers rented land fromabsentee English landlords who lived inEngland, and planted grain and othercrops. The yields were poor and, in anycase, large portions of them had to beused for paying the exorbitant rent so asto avoid eviction. The Irish farmers alsokept small plots of land, usually as smallas a quarter of an acre and basically sur-vived the winter with the food they pro-duced on that land. Potato productionwas greatly favored by the cool, wetclimate of Ireland, and the farmersbegan growing and eating potatoes tothe exclusion of other crops and food-stuffs. Irish farmers, therefore, becamedependent on potatoes for their suste-nance and survival. Lacking properwarehouses, the farmers stored theirpotato tubers for the winter in shallowditches in the ground. Periodically, theywould open up part of the ditch andremove as many potatoes as theythought they would need for the nextfew weeks.

The potatoes grew well for manyyears, free of any serious problems. Inthe early 1840s, potato crops began tofail to varying extents in several areas ofEurope and Ireland. Most of thegrowing season of 1845 in Ireland wasquite favorable for the growth of potatoplants and for the formation of tubers.Everything looked as though therewould be an excellent yield of potatoeseverywhere that year. Then, the weatherover northern Europe and Irelandbecame cloudy, wetter, and cooler andstayed that way for several weeks (Fig.1-17A). The potato crop, which untilthen looked so promising, began toshow blighted leaves and shoots (Fig. 1-17B), and whole potato plants becameblighted and died. In just a few weeks,the potato fields in northern Europe andin Ireland became masses of blighted androtting vegetation (Fig. 1-17C). Thefarmers were surprised and worried,especially when they noticed that manyof the potatoes still in the ground wererotten and others had rotting areas ontheir surface (Fig. 1-17D). They didwhat they could to dig up the healthy-looking potatoes from the affected fieldsand put them in the ditches to hold themthrough the winter.

The farmer’s worry became horrorwhen later in the fall and winter theybegan opening the ditches and lookingfor the potatoes they had put in them atharvest. Alas, instead of potatoes theyfound only masses of rotting tubers (Figs.1-17D and 1-17E), totally unfit for con-sumption by humans or animals. Thedependence of Irish farmers on potatoesalone meant that they had nothing elseto eat — and neither did any of theirneighbors. Hunger (Fig. 1-17F) wasquickly followed by starvation, whichresulted in the death of many Irish. Thefamine was exacerbated by the politicalsituation between England and Ireland.The British refused to intervene and helpthe starving Irish with food for several

months after the blight destroyed thepotatoes. Eventually, by February of thenext year (1846), food, in the form ofcorn from the United States, began to beimported and made available to thestarving poor who paid for it by workingon various government constructionprojects. Unfortunately, the weather in1846 was again cool and wet, favoringthe potato blight, which again spreadinto and destroyed the potato plants andtubers. Hunger, dysentery, and typhusspread among the farmers again, andmore of the survivors emigrated to NorthAmerica. It is estimated that one and ahalf million Irish died from hunger, andabout as many left Ireland, emigratingmostly to the United States of America.

The cause of the destruction of thepotato plants and of the rotting of thepotato tubers was, of course, unknownand a mystery to all. The farmers andother simple folk believed it to have beenbrought about by “the little people,” bythe devil himself whom they tried toexorcise and chase away by sprinklingholy water in the fields, by locomotivestraveling the countryside at devilishspeeds of up to 20 miles per hour anddischarging electricity harmful to cropsthey went by, or to have been sent byGod as punishment for some unspecifiedsin they had committed. The more edu-cated doctors and clergy were so con-vinced of the truth of the theory ofspontaneous generation that even whenthey saw the mildewy fungus growth onaffected leaves and on some stems andtubers, they thought that this growthwas produced by the dying plant as aresult of the rotting rather than the causeof the death and rotting of the plant.

Some of the educated people,however, began to have second thoughtsabout the situation. Dr. J. Lindley, a pro-fessor of botany in London, proposedincorrectly that the plants, during therains, overabsorbed water through theirroots and because they could not get rid

continued

20 1. INTRODUCTION

End of June

A

Mid-July

Mid-August

Mid-September

Mid-October

B

FIGURE 1-17 The late blight of potato and the Irish famine. (A) Itinerary of the advance of the potato blightbetween June, when the blight was first detected in Belgium, and the end of October 1845, by which time it spreadfrom Italy to Ireland and from Spain to the Scandinavian countries. (B) A young lesion on a potato leaf covered withsporangiophores and sporangiospores of the fungus (oomycete). (C) A potato plant killed completely by the blight(right) next to a healthy-looking resistant plant (left). (D) External and internal appearance of potato tubers infectedwith the late blight disease. The oomycete is still found near the surface. (E) Advanced invasion and rotting of potatotuber infected with late blight. (F) A period drawing of a family digging for potatoes to avoid starvation during theIrish famine. [Photographs courtesy of (A) W. E. Fry, Cornell University, (B) D. P. Weingartner, University of Florida,(C and D) Cornell University, (E) USDA, and (F) Illustrated London News, 1849.]

of the excess water, their tissues becameswollen and rotted. The Reverend Dr.Miles Berkeley, however, noticed thatthe mold covering potato plants about torot was a fungus (oomycete) similar butnot identical to a fungus he observed ona sick onion. The fungus on potato,however, was identical to a fungusrecovered from sick potato plants innorthern Europe. Berkeley concludedthat this fungus was the cause of thepotato blight, but when he proposed itin a letter to a newspaper, it was con-sidered as an incredible and bizarretheory unsupported by facts. The puzzleof what caused blight of potato contin-ued unanswered for 16 years after the1845 destruction of potatoes by theblight. Finally, in 1861, Anton deBary(Fig. 1-16A) did a simple experimentthat proved that the potato blight was

caused by a fungus. DeBary simplyplanted two sets of healthy potatoes, oneof which he dusted with spores of thefungus collected from blighted potatoplants. When the tubers germinated andbegan to produce potato plants, thehealthy tubers produced healthy plants,whereas the healthy tubers dusted withthe spores of the fungus produced plantsthat became blighted and died. Nomatter how many times deBary repeatedthe experiment, only tubers treated withthe fungus became infected and pro-duced plants that became infected.Therefore, the fungus, which, we knownow, is an oomycete was named Phy-tophthora infestans (“infectious plantdestroyer” from phyto = plant, phthora= destruction, infestans = infectious),was the cause of the potato blight.DeBary also showed that the fungus did

not just reappear from nowhere the fol-lowing growing season but instead sur-vived the winter in partially infectedpotato tubers in the field or storage. Inthe spring, the fungus infected youngplants coming from these partially rottentubers, produced new spores on theseplants, and the spores then spread toother cultivated potato plants that wereinfected and killed. With this experimentdeBary actually disproved the theory ofspontaneous generation, which statedthat microorganisms are produced spon-taneously by dying and dead plants andanimals, and ushered in the germ theoryof disease. The honor for this proof,however, is reserved for Louis Pasteur,who proved the theories while workingwith bacteria at about the same time,1861–1863, that deBary published hiswork with the potato blight fungus.


The Expanding Role of Fungi as Causes of Plant Disease

Following the observation by French farmers around the mid-1600s and, independently, by Connecticutfarmers in the early 1700s that wheat rust was worsenear barberry bushes, the farmers came to believe thatbarberry fathered the rust, which then moved to wheat.The request by farmers for legislation to force towns to eradicate barberries and in that way to protect thewheat plants from rust followed. At about the sametime, spores of the rust fungus were observed with the compound microscope for the first time in England(Hooke, 1667). In Italy, Micheli 60 years later (1729)described many new genera of fungi, illustrated theirreproductive structures, and noted that when he placedthem on freshly cut slices of melon, these fungal struc-

tures generally reproduced the same kind of fungus that produced them. He proposed that fungi arose from their own spores rather than spontaneously, butnobody believed him. New information about plantpathogenic fungi continued to be developed, but mostof it was not accepted by the scientists of the time for along time.

As mentioned previously, in 1755, Tillet in Franceshowed that wheat smut is a contagious plant disease,but even he believed that it was a poisonous substancecontained in the smut dust, rather than a living microor-ganism, that caused the disease. In 1807, Prevost, alsoin France, repeated and expanded Tillet’s experimentsand appeared to have demonstrated conclusively thatwheat smut was caused by a fungus. His conclusions,however, were not accepted because the scientists wereblinded by the belief that microorganisms and their

FIGURE 1-17 (Continued)

E F

DC

22 1. INTRODUCTION

spores were the result rather than the cause of disease.These beliefs continued to be shared and expounded byscientists for at least another 50 years.

The devastating epidemics of late blight of potato innorthern Europe, particularly Ireland, in the 1840s notonly dramatized the effect of plant diseases on humansuffering and survival, but also greatly stimulated inter-est in their causes and control. In 1861, deBary finallyestablished experimentally beyond criticism that a fun-gus (Ph. infestans) was the cause of the plant diseaseknown as late blight of potato, a disease that closelyresembles the downy mildews.

It is, perhaps, worth noting here that it was duringthose years (1860–1863) that Louis Pasteur proposed,and finally provided irrefutable evidence, that microor-ganisms arise only from preexisting microorganisms and that fermentation is a biological phenomenon, notjust a chemical one. Pasteur’s conclusions, however,were not generally accepted for many years afterward.Nevertheless, the proof for involvement of microorgan-isms (germs) in fermentation and disease signaled thebeginning of the end of the theory of spontaneous gen-eration and provided the basis for the germ theory ofdisease.

Although fungi had already been the object of studyby many scientists, proof that they were causing diseasein plants greatly increased interest in them. DeBary

himself also carried out studies of the smut and rustfungi, of the fungi causing downy mildews, and of thefungus Sclerotinia, which induces rotting of vegetables.The German Kühn in the 1870s and later contributedsignificantly to the studies of infection and developmentof smut in wheat plants and promoted the developmentand application of control measures, particularly seedtreatment for cereals. Kühn also wrote the first book onplant pathology, “Diseases of Cultivated Crops, TheirCauses and Their Control,” in which he recognized thatplant diseases are caused by an unfavorable environ-ment but can also be caused by parasitic organisms suchas insects, fungi, and parasitic plants.

During the years of Pasteur and Koch, several scien-tists also made significant contributions to plant pathol-ogy and to biology and medicine. After establishingbeyond criticism in 1861 that the potato blight wascaused by a fungus, DeBary went on to show con-clusively that smut and rust fungi were also the causes and not the results of their respective plant dis-eases. Moreover, he showed that some rust diseasesrequire two alternate host plants (see Fig. 1-13) to com-plete their life cycle, e.g., the fungus causing the stem rustof wheat requires wheat and barberry. DeBary alsoshowed (1886) that some fungi induce rotting of veg-etables (Fig. 1-18) by secreting substances (enzymes) thatdiffuse into plant tissues in advance of the pathogen.

A

C

B

FIGURE 1-18 Infection and advanced internal rotting of summer squash (A) by the fungus Choanephora, of peachfruit (B) by the fungus Rhizopus sp., and (C) of kiwi fruit by the fungus Botrytis cinerea. In all cases, fruit rot is aresult of, primarily, pectinolytic enzymes secreted by the fungi and advancing ahead of the mycelium. A small amountof the fungi can be seen on the surface of the fruits. (C) Courtesy of T. Michailides, University of California.


The Discovery of Other Causes of Infectious Diseases

Although Leeuwenhoek first saw microbes with themicroscope he invented in 1674, little progress wasmade toward the concept of microbes as the cause ofdisease for almost another 200 years. In 1776, Jennerintroduced vaccination against the virus-induced small-pox, an extremely infectious and severe disease that usedto kill 10 to 20% of those infected, but could only spec-ulate as to its cause and how it worked. In 1861,however, deBary showed that the potato blight wascaused by a fungus while Pasteur formulated the germtheory of fermentation. In 1864, Pasteur invented pas-teurization and, in 1880, made the first vaccine againstthe chicken cholera. In the meantime, in 1876, Koch

identified the anthrax bacillus, Bacillus anthracis, as thefirst bacterium to cause disease in animals and humans.In addition, in 1887, Koch formulated his rules ofdisease diagnosis that became known as “Koch’s postu-lates.” These rules became the standard procedure forproving that a disease is caused by a bacterium or anyother kind of pathogen.

Nematodes

The first report of nematodes associated with a plantdisease was made in England by Needham in 1743. Heobserved nematodes (Fig. 1-19A) within small, abnor-mally rounded wheat kernels (wheat galls; Fig. 1-19B);however, he did not show or suggest that they were thecause of the disease. It was not until 1855 that a second

D

A

C

B

FIGURE 1-19 (A) A typical nematode. (B) Wheat seed galls, each filled with as many as 30,000 nema-todes. (C) M. Woronin. (D) Clubroot of cabbage caused by the protozoon Plasmodiophora brassicae.[Photographs courtesy of (A and B) USDA Nematology Laboratory, Beltsville, Maryland, and (D) C. M.Ocamp, Oregon State University.]

24 1. INTRODUCTION

nematode, the root knot nematode, was observed incucumber root galls. In the next 4 years two other plantparasitic nematodes, the bulb and stem nematode andthe sugarbeet cyst nematode, were reported frominfected plant parts. Several more nematodes parasitiz-ing plants were described in the early part of the 20thcentury by Cobb, who made numerous significant con-tributions to plant nematology.

Protozoan Myxomycetes

In 1878, Woronin (Fig. 1-19C), in Russia, was the firstto show that a plant disease, the clubroot disease ofcabbage (Fig. 1-19D), was caused by a fungus that hasbeen shown to be a protozoan plasmodiophoromycete.These are fungus-like, single-celled microorganisms thatlack a cell wall and, as a result, produce an amoeba-like body called a plasmodium and zoospores. Thesemicroorganisms used to be thought of as lower fungi but

are now considered members of a different kingdom, thekingdom protozoa.

Bacteria

Soon after Koch showed that bacteria cause disease inanimals and humans, Burrill in Illinois showed, in 1878,that bacteria (Fig. 1-20A) caused the fire blight disease(Fig. 1-20B) of pear and apple. Following Burrill’s discovery, several other plant diseases were shown, particularly by Erwin Smith (Fig. 1-20C) of the U.S.Department of Agriculture (USDA), to be caused by bac-teria. In the early 1890s, Smith was the first to showthat crown gall disease (Fig. 1-20D), which he consid-ered similar to cancerous tumors of humans andanimals, was caused by bacteria. Studies of how thisbacterium, known as Agrobacterium tumefaciens,caused tumors in plants led to the discovery, almost acentury later, that whenever the bacterium infects plants

A B

C D

FIGURE 1-20 (A) The fire blight bacterium Erwinia amylovora. (B) Fire blight on apple trees. (C) Erwin F. Smith.(D) Crown gall, caused by the bacterium Agrobacterium tumefaciens. [Photographs courtesy of (A) Oregon State University, and (B) K. Mohan and (D) R. L. Forster, University of Idaho.]


it transfers part of its DNA to the plant and that theDNA is expressed by the plant as if it were plant DNA(see also pages 624–625). The discovery that the bac-terium acts as a natural genetic engineer of plants led tothe development of this bacterium so that it could beloaded with, and then transfer to plants, DNA segmentscoding for desirable characteristics, which formed thebasis of biotechnology, especially of plants. As withfungal plant pathogens, however, acceptance of bacteriaas causes of disease in plants was slow. For example, aslate as 1899, Alfred Fischer, a prominent Germanbotanist, rejected the results of Smith and others whoclaimed to have seen bacteria in plant cells.

Viruses

At about the same time that more diseases of plants wereshown to be caused by bacteria, the Dutchman AdolphMayer (Fig. 1-21A), in 1886, injected juice obtainedfrom tobacco plant leaves showing various patterns of greenish yellow mosaic (Fig. 1-21B) into healthytobacco plants and the latter then developed similarmosaic patterns. Because no fungus was present on theplant or in filtered juice, Mayer concluded that thedisease was probably caused by bacteria. In 1892,however, Ivanowski showed that whatever caused thetobacco mosaic disease could pass through a filter thatretains bacteria, so he concluded that the disease wascaused by a toxin secreted by bacteria or, perhaps, byunusually small bacteria that passed through the poresof the filter. In 1898, Beijerinck, by repeating some of these experiments, finally concluded that the to-bacco mosaic disease was caused not by a microor-ganism, but by a “contagious living fluid’ ” that hecalled a virus.

No one had any idea, however, what a virus was andwhat it looked like for another 40 years. The true nature,size, and shape of the virus (Fig. 1-21C) remainedunknown for several more decades. In 1935, Stanleyadded ammonium sulfate to tobacco juice extracted frominfected tobacco leaves and obtained as a sediment in theflask a crystalline protein that, when rubbed on tobacco,caused the tobacco mosaic disease. This led him to con-clude that the virus was an autocatalytic protein thatcould multiply within living cells. Although his resultsand conclusions were later proved incorrect, for his dis-covery Stanley received a Nobel Prize in Chemistry. In1936, Bawden and colleagues demonstrated that thecrystalline preparations of the virus actually consisted ofnot only protein, but also a small amount of ribonucleicacid (RNA). The first virus (tobacco mosaic virus) parti-cles were seen with the electron microscope in 1939 byKausche and colleagues. Finally, in 1956, Gierrer andSchramm showed that the protein could be removed fromthe virus and that the ribonucleic acid carried all thegenetic information that enabled it to cause infection andto reproduce the complete virus. It was shown subse-quently that although the nucleic acid of most virusesinfecting plants is single-stranded RNA, some viruseshave double-stranded RNA, some double-strandedDNA, and some single-stranded DNA.

The search for the cause of the many thousands ofplant diseases led to the discovery of at least three morekinds of pathogens and it is likely that others remain tobe discovered.

Protozoa

Flagellate trypanosomatid protozoa were observed inthe latex-bearing cells of laticiferous plants of the family

FIGURE 1-21 (A) Adolph Mayer. (B) Tobacco leaf showing symptoms of tobacco mosaic. (C) Particles of tobaccomosaic virus.

A B C

26 1. INTRODUCTION

Euphorbiaceae by Lafont in 1909. Such protozoa,however, were thought to parasitize the plant latexwithout causing disease on the host plant. In 1931,Stahel found flagellates infecting the phloem of coffeetrees, causing abnormal phloem formation and wiltingof the trees. In 1963, Vermeulen presented convincingevidence of the pathogenicity of flagellates to coffeetrees, and in 1976 flagellates were reported to be asso-ciated with several diseases of coconut and oil palm treesin South America and in Africa. In recent years, ofcourse, the Myxomycota and the Plasmodiophoromy-cota, which were previously thought to be fungi, havebeen transferred to the kingdom protozoa.

Mollicutes (Phytoplasmas)

For nearly 70 years after viruses were discovered, manyplant diseases were described that showed symptoms ofgeneral yellowing or reddening of the plant or of shootsproliferating and forming structures that resembledwitches’ brooms. These diseases were thought to becaused by viruses, but no viruses could be found in suchplants. In 1967, Doi and colleagues in Japan observedmollicutes, i.e., wall-less mycoplasma-like bodies in thephloem of plants exhibiting yellows and witches’ broomsymptoms. That same year the same group showed thatthe mycoplasma-like bodies and symptoms disappearedtemporarily when the plants were treated with tetracy-cline antibiotics. Since then, mycoplasma-like organisms(MLOs) that infect plants have been reclassified as phy-toplasmas, and some of them that have helical bodiesand can be found in other environments besides plantsare known as spiroplasmas.

Viroids

In 1971, studies of the potato spindle tuber diseaseshowed that it was caused by a small, naked, single-

stranded, circular molecule of infectious RNA, whichwas called a viroid (see later). Viroids have been foundto be the cause of several dozen plant diseases. Viroidsseem to be the smallest infectious nucleic acid molecules.Although more than 40 viroids have been found toinfect plants, no viroids have been found that infectanimals or humans.

Apparently, however, an even smaller type of infec-tious agent, called a prion, exists (see later). Prionsapparently consist only of a small (~55,000Da) protein,which is encoded by a chromosomal gene of the host.Prions have been shown to cause the scrapie disease ofsheep, “mad cow” disease, and at least three slow-devel-oping degenerative diseases of humans. So far, no prionshave been found to infect plants, but there is no obviousreason why they should not.

Serious Plant Diseases of Unknown Etiology

Although pathogens as large and complex as fungi andnematodes or as tiny and simple as viroids and prionshave been discovered, there are many severe diseases ofplants, particularly of trees, for which we still do notknow their real cause, despite years of searching andresearch. Some of them, such as peach short life in the southeastern United States, waldsterben, or forestdecline in central Europe and various forest tree declinesin the northeastern and northwestern United States, maybe caused by more than one pathogen or by combina-tions of pathogens and adverse environment. Others,such as citrus blight in Florida and South America, spearrot in oil palm in Suriname and Brazil, and mango mal-formation in India and other mango-growing countries,seem to have a biotic agent as the primary cause, butthe activity of the agent seems to be strongly affected byenvironmental factors such as soil or temperature.Despite more than 100 years of research on some plantdiseases, the causes of these diseases remain unknown.

BOX 5 Koch’s postulates

Robert Koch (1843–1910) (Fig. 1-16C)was a medical doctor and a bacteriolo-gist. He was the first to show, in 1876,that anthrax, a disease of sheep andother animals, including humans, wascaused by a bacterium that he calledBacillus anthracis. He subsequently dis-covered, in 1882, that tuberculosis and,in 1883, that cholera are each caused bya different bacterium, which led to thegeneral conclusion that each disease is

caused by a specific microbe. Theseexperiments confirmed for the first timethe germ theory of disease proposedearlier by Louis Pasteur.

Before Koch’s experiments, and whileKoch himself was carrying out the workon the diseases mentioned earlier, therewas confusion and uncertainty about theoccurrence and the cause of each disease.Much of the time when bacteria or fungiwere isolated from diseased or dead

human, animal, or plant tissues, the isolated bacteria or fungi were subse-quently shown to be saprophytes, i.e.,they coexisted with the microorganismthat caused the disease but could not bythemselves cause the disease for whichthey were being considered. Based on hisexperiences, in 1887, Koch set out thefour steps or criteria that must be satis-fied before a microorganism isolatedfrom a diseased human, animal, or plant


can be considered as the cause of thedisease. These four steps, rules, or crite-ria are known as “Koch’s postulates.”

1. The suspected causal agent (bac-terium or other microorganism)must be present in every diseasedorganism (e.g., a plant) examined.

2. The suspected causal agent (bac-terium, etc.) must be isolated fromthe diseased host organism (plant)and grown in pure culture.

3. When a pure culture of the sus-pected causal agent is inoculatedinto a healthy susceptible host(plant), the host must reproducethe specific disease.

4. The same causal agent must berecovered again from the experi-mentally inoculated and infectedhost, i.e., the recovered agent musthave the same characteristics as theorganism in step 2.

Koch’s rules are possible to imple-ment, although not always easy to carryout, with such pathogens as fungi, bac-

teria, parasitic higher plants, nematodes,most viruses and viroids, and the spiro-plasmas. These organisms can be iso-lated and cultured, or can be purified,and they can then be introduced into theplant to see if they cause the disease.With the other pathogens, however, suchas some viruses, phytoplasmas, fastidi-ous phloem-inhabiting bacteria, proto-zoa, and even some plant pathogenicfungi that are obligate parasites of plants(such as the powdery mildew, downymildew, and rust fungi), culture orpurification of the pathogen is not yetpossible and the pathogen often cannotbe reintroduced into the plant to re-produce the disease. Thus, with thesepathogens, Koch’s rules cannot becarried out, and their acceptance as theactual pathogens of the diseases withwhich they are associated is more or lesstentative. In most cases, however, the cir-cumstantial evidence is overwhelming,and it is assumed that further improve-ment of techniques of isolation, culture,and inoculation of pathogens willsomeday prove that today’s assumptions

are justified. However, in the absence ofthe proof demanded by Koch’s rules andas a result of insufficient information, allplant diseases caused by phytoplasmas(e.g., aster yellows) and fastidious vas-cular bacteria (e.g., Pierce’s disease ofgrape) were for years thought to becaused by viruses.

Despite the difficulties of carrying outKoch’s postulates with some causalagents, they have been and continue tobe applied, sometimes with certain modifications, in all cases of disease. They have had and continue to have atremendous effect in deciding and inconvincing others that a particularmicroorganism is the cause of a specificdisease. By attempting to carry outKoch’s postulates in all newly discovereddiseases, a great deal of work withpotential saprophytes has been avoided,while, at the same time, doubt and crit-icism are reduced to a minimum whileconfidence in and use of the identifica-tion increase greatly and quickly.

BOX 6 Viruses, Viroids, and Prions

Although they have been with us forever,we know relatively little about howthese pathogen operate. There are manycommon characteristics among virusesand viroids. The relationship of prionsto others is only in their small size butthey are contrasted to the other two inthat they do not depend on any kind ofnucleic acid (RNA or DNA). Virusescause numerous severe diseases in alltypes of organisms, have been studiedthe longest, and we know the mostabout them. Viroids cause more than 40diseases in plants, some of them lethal.Prions seem to affect only humans andanimals in which they cause degenera-tive diseases of the brain, such as therecently much publicized “mad cowdisease.”

Viruses are submicroscopic spherical,rod-shaped, or filamentous entities(organisms) (Figs. 1-22A–1-22C) thatconsist of only one type of nucleic acid

(DNA or RNA). The nucleic acid is sur-rounded by a coat consisting of one ormore kinds of protein molecules. Virusesinfect and multiply inside the cells ofhumans, animals, plants, or other organ-isms and usually cause disease.

Viroids were discovered by Diener(Fig. 1-22D) and colleagues in 1971while they were studying the potatospindle tuber disease (Fig. 1-22E).Viroids are the smallest infectious agentsthat multiply autonomously in plantcells; they consist only of small, circularRNA molecules (Fig. 1-22F) that are toosmall to code for even one small proteinand therefore lack a protein coat.Viroids infect plant cells and are repli-cated in their nucleus, using the sub-stances and enzymes of plant cells.Viroids infect only plants and in manyof them they usually cause disease.Viroids have not yet been detected in anyother kind of organism besides plants.

Prions were proposed for the first timein 1972 by Prusiner (Fig. 1-22G) who,for that and subsequent work, receivedthe Nobel Prize in Physiology or Medi-cine in 1997. Prions are at first normalsmall protein molecules produced innerve and other cells of the brain. Prionsbecome pathogenic, i.e., they cannotcarry out their normal functions and,instead, have adverse effects on the brainand cause disease. This occurs whenprions are forced by conditions in thebrain to change shape (Fig. 1-22H). Thechange in shape signals the onset ofinfection. Prions are not associated withany nucleic acid. Abnormal prionsappear to increase in number and tocause the appearance of amyloid fibrilsand plaques, as well as the appearanceof small cavities (Fig. 1-22I) in the brainof diseased animals and humans. Prionshave not been observed in plants orother organisms.

continued

28 1. INTRODUCTION

E F

BA

C

D

FIGURE 1-22 (A–C) Relative shapes and sizes of plant viruses: spherical, rod shaped, and flexuous. (D) T. O.Diener. (E) Potatoes infected with potato spindle tuber viroid. (F) Circular and linear particles of the coconut cadang-cadang viroid. (G) Stanley Prusiner. (H) Schematic presentation of a normal protein and of a deformed inactive one,i.e., a prion. (I) Plaques in the brain of an animal affected by a prion. [Photographs courtesy of (E) H. D. Thurston,Cornell University, (F) J. W. Randles, University of Adelaide, Australia, and (H and I) S. Prusiner, University of California.]

LOSSES CAUSED BY PLANT DISEASES 29

LOSSES CAUSED BY PLANT DISEASES

Plant diseases are of paramount importance to humansbecause they damage plants and plant products onwhich humans depend for food, clothing, furniture, theenvironment, and, in many cases, housing. For millionsof people all over the world who still depend on theirown plant produce for survival, plant diseases can makethe difference between a comfortable life and a lifehaunted by hunger or even death from starvation. Deathfrom starvation of one and a quarter million Irish peoplein 1845 and much of the hunger of the underfed mil-lions living in the developing countries today are exam-ples of the consequences of plant diseases. For countrieswhere food is plentiful, plant diseases are significant pri-marily because they cause economic losses to growers.Plant diseases, however, also result in increased prices of products to consumers; they sometimes cause directand severe pathological effects on humans and animalsthat eat diseased plant products; they destroy the beauty of the environment by damaging plants aroundhomes, along streets, in parks, and in forests; and, in trying to control the diseases, people release billionsof pounds of toxic pesticides that pollute the water andthe environment.

Plant Diseases Reduce the Quantity and Qualityof Plant Produce

The kinds and amounts of losses caused by plant dis-eases vary with the plant or plant product, the pathogen,the locality, the environment, the control measures prac-ticed, and combinations of these factors. The quantityof loss may range from slight to 100%. Plants or plantproducts may be reduced in quantity by disease in thefield, as indeed is the case with most plant diseases, orby disease during storage, as is the case of the rots ofstored fruits, vegetables, grains, and fibers. Sometimes,destruction by the disease of some plants or fruits iscompensated by greater growth and yield of the remain-ing plants or fruits as a result of reduced competition.Frequently, severe losses may be incurred by reductionin the quality of plant products. For instance, whereasspots, scabs, blemishes, and blotches on fruit, vegeta-bles, or ornamental plants may have little effect on thequantity produced, the inferior quality of the productmay reduce the market value so much that productionis unprofitable or a total loss. For example, with applesinfected with apple scab, even as little as 5% diseasemay cut the price in half; with others, e.g., potatoesinfected with potato scab, there may be no effect onprice in a market with slight scarcity, but there may bea considerable price reduction in years of even minorgluts of produce.

G H I


30 1. INTRODUCTION

A B

FIGURE 1-23 Powdery mildew of grape on (A) leaves and (B) grape cluster. White mycelium may coverall green parts, which become dry and brown. (Photographs courtesy of M. A. Ellis, Ohio State University.)

BOX 7 White, dry, and downy vineyards — bordeaux to the rescue!

During the second half of the 1800s, thesaying that bad things come in threesfound perfect application in the Euro-pean and particularly the French grapeand wine industry. In the 1840s, a con-dition known to exist on grapes inAmerica but never before observed inEurope appeared first in England andsoon after in France: young grape leaveswould be covered with spots of whitepowder (Fig. 1-23A). Later, as the leafgrew in size and age, the white spotswould spread and cover most of the leaf.The white mildewy stuff would also geton the berries, which would becomedirty gray, wither, and sometimes crack.The condition was called powderymildew and was later shown to be causedby the fungus Uncinula necator. Often,parts of the leaf would turn brown toblack and die, while the berries wouldremain small, discolored (Fig. 1-23B),and unfit for wine production or to beeaten fresh. By 1854, French wine pro-duction was reduced by 80% due to thenew disease. New grapevines were fran-tically imported from many countries in

the hope that some of them wouldsurvive the powdery mildew. Fortu-nately, at the same time, it was noticedin England that when a mixture of pow-dered lime and sulfur was dusted on thevines, it significantly protected the leavesand the berries from powdery mildew.This practice became somewhat acceptedin France and losses from powderymildew were reduced significantly.

The early scramble for and importa-tion of foreign vines, however, broughtwith it a second calamity to the Frenchand European grape and wine industrythat was much more disastrous thanpowdery mildew. In the early 1860s,young leaves on French vines woulddevelop several small galls on the under-side (Fig. 1-24A), but then, a few weekslater, all the leaves would turn yellowishto red in early spring and summer andsubsequently would wither and fall off(Fig. 1-24B) in July or August. Affectedvines produced little or no fruit and thefollowing year they died. The dead, dryleaves gave to the condition the name“phylloxera” (=“dryleaf” from the

Greek phyllo = leaf, and xera = dry). Itwas later noted that phylloxera wasassociated with aphids, some of whichfed on the young leaves and inducedgalls, while many more were foundfeeding on the roots of grapevines. Theaphids not only induced galls on thesmall roots, they also multiplied quicklyand sucked the nutrients out of theroots, killing the roots and, by denyingthe plant water, caused the leaves to dis-color, wither, and fall off. The phyllox-era condition was spreading slowly but,in vineyards into which it spread, it haddevastating results.

It was determined that phylloxeraaphids had probably been brought infrom the United States with vinesimported for resistance to the powderymildew problem. The phylloxera aphids,however, did not seem to attack or causeserious damage on American grapevines.So, a new wave of importation of Amer-ican vines began. These vines were usedas rootstocks on which the Europeanvarieties were grafted. The degree ofresistance of some of the rootstocks to


A B

FIGURE 1-24 Phylloxera on grape caused by the grape root aphid. (A) Patch of grapevines showing dry foliageor defoliation due to infection of their roots by the phylloxera aphid. (B) Phylloxera aphids (Dactylosphaira vitifolia)feeding on and eventually killing the rootlets of grapevines, thereby causing drying and death of the plants. (Pho-tographs: Queensland Dept. Natural Resources.)

the phylloxera aphids was excellent (Fig.1-24B) and so the French and otherEuropean vineyards could be restoredsignificantly over time.

Unfortunately, however, a thirdcalamity hit the European vineyardswhile they were just beginning to feelthat they had figured out how to escapethe destructiveness of phylloxera. In1878, grape leaves in some French vine-yards began to show whitish downyspots on their undersides (Fig. 1-25A),while the upper sides of such leaves cor-responding to the underside downyspots became yellow at first and thenturned brownish black and died. Thiscondition became known as downymildew and was shown to be caused bythe fungus Plasmopara viticola. As thenumber and size of the spots increased,most or all of the leaf was affected, died,and fell off the vine. Young shoots werealso affected, as were young grape clus-ters, becoming covered with the whitedowny growth (Fig. 1-25B). Later, theyturned brown and eventually shriveled.Berries infected later in the seasonremained hard compared to healthy

ones, exhibited a light green to reddishmottle, and eventually dropped.

The downy mildew spread rapidlywithin vineyards and from one vineyardto another. It reduced grape yields andquality greatly and killed the youngvines in many vineyards. Downy mildewwas especially severe and spread themost in cool, rainy weather. Within 5years of its appearance in France itspread to all the vineyards of thatcountry and into those of adjacent coun-tries. The grape producers in these countries became panicky again. Manyscientists showed concern for the pro-blem and interest in finding a solutionfor it. Some of them used different sub-stances, which they added to the soil ordusted on the vines, trying to protectthem from downy mildew. For severalyears nothing worked. Then one day, theFrench botany professor Pierre AlexisMillardet (Fig. 1-25C), while walkingamong the vineyards, noticed that insome of them, the vines of a few rowsalong the dirt road had a bluish film ontheir leaves. What was most noteworthywas that these vines seemed to still have

all their leaves healthy, whereas vines inrows that did not have the bluish film,the leaves, young twigs, and berry clus-ters were affected severely by downymildew (Fig. 1-25D). The owner of thevineyard told him that the bluish filmwas actually bluestone (copper sulfate),mixed with some hydrated lime to betterstick on the leaves. The mixture wassprayed on the vines to create theimpression that it was poisonous and inthat way to keep passersby from goinginto his vineyard and taking his grapes.With that information in hand, Mil-lardet went back to his laboratory wherehe mixed copper sulfate and hydratedlime in various proportions and triedthem on downy mildew-affected vines.Finally, in 1885, he found the best com-bination for the control of downymildew. This solution (8-8-100) becameknown as Bordeaux mixture andushered in the era of control of plant dis-eases with fungicides. Bordeaux mixtureproved to be an excellent fungicide andbactericide and for more than a centurywas the fungicide used the mostthroughout the world.

continued

Plant Diseases May Limit the Kinds of Plants andIndustries in an Area

Plant diseases may limit the kinds of plants that can grow in a large geographic area. For example, the

American chestnut was annihilated in North America asa timber tree by the chestnut blight disease, and theAmerican elm is being eliminated as a shade tree byDutch elm disease.

32 1. INTRODUCTION

A B

C D

FIGURE 1-25 Downy mildew of grape. Early symptoms on (A) grape leaf and (B) grape cluster. (C) P. Millardet.(D) At left, grapevines exposed to downy mildew but treated with Bordeaux mixture still retain most of their foliage,whereas, at right, unprotected grapes lost almost all of their foliage as a result of downy mildew. [Photographs cour-tesy of (A) J. Travis and J. Rytter, Pennsylvania State University, (B) University of Georgia, Extension, and (D) G. Ash,Charles Sturt University, Australia.]

BOX 8 Familiar trees in the landscape: going, going, gone

In the 19th century, two plant diseases,powdery and downy mildews of grape,and an insect pest of grapes, the phyl-loxera aphid, each of which alone could

have destroyed the European vineyards,spread from North America intoEurope. The rediscovery of the use ofsulfur against powdery mildew, the dis-

covery of Bordeaux mixture againstdowny mildew, and the discovery ofrootstocks resistant to phylloxera savedthe European grape industry in each


continued

case. In the 20th century, Europereturned the favor to North America bygiving North America two plant dis-eases, chestnut blight and Dutch elmdisease, each of which killed billions oftrees, bringing their respective hostspecies to the brink of extinction. Unfor-tunately, no good control of these dis-eases exists even to date, and more of theremaining, at least elm trees, continue tobe killed. Another disease, lethal yellow-ing of coconut palms, has spreadthrough several of the Caribbean islandsand adjacent countries, the states ofFlorida and Texas, west Africa, andelsewhere. Lethal yellowing has de-stroyed the majority of coconut palms inthese areas and, like chestnut blight andthe Dutch elm disease, it is still impossi-

ble or very difficult to control and con-tinues to kill and threaten the remainingtrees with extinction.

Chestnut Blight

There was a time not too long ago thatin a broad band of land of the UnitedStates, several hundred miles in widthand extending from the bottom of thestates of Georgia and Mississippi to thetop of Maine and Michigan and intoOntario, Canada (Fig. 1-26A), that themost common trees in the forests werethe majestic American chestnuts (Fig. 1-26B). They provided timber and chest-nuts, the latter serving as a source offood for humans and for wildlife, whilethe trees served as a habitat for wildlife.

Both timber and chestnuts provided asource of income for the local people.The trees had been there apparentlyforever and looked like they would alsolast forever.

Then something seemingly minor hap-pened. In 1904, the leaves of a fewbranches of large chestnut trees and afew young trees in the New York zoobegan to turn brown and die. Beforeanyone could figure out what was hap-pening, many more young trees andbranches of older ones died, giving thetrees a blighted appearance. From there,chestnut blight spread rapidly througheastern North America so that by the1920s the blight could be found in theentire natural range of the Americanchestnut tree. By now, scientists in

0 100

kmA

200

B

C

FIGURE 1-26 Chestnut blight. (A) Natural range of American chestnut before the chestnut blight fungus epidemicof 1904–1944. (B) Stand of young, pole-sized chestnut trees devastated by chestnut blight. (C) Chestnut blight cankeron trunk of young chestnut tree causing the death of the tree. [Photographs courtesy of (B) W. L. MacDonald, WestVirginia University, and (C) R. L. Anderson, U.S. Forest Service.]

34 1. INTRODUCTION

A

BC

FIGURE 1-27 Dutch elm disease. (A) Early symptoms of elm tree showing wilting, curling, and browning of leavesof branch infected with the Dutch elm disease fungus. (B) Advanced symptoms of wilt, defoliation, and death of largebranches of tree affected with the disease. (C) Dead elm trees along a road, all killed by Dutch elm disease. [Pho-tographs courtesy of (A) R. J. Stipes, Virginia Tech University, (B) R. L. Anderson, U.S. Forest Service, and (C), E. L.Barnard, Florida Forest Service.]

general, and plant pathologists in par-ticular, were quite adept at identifyingmost causes of plant disease, and chest-nut blight was quite easy to diagnose. Itwas soon shown that chestnut blight iscaused by a fungus, Cryphonectria par-asitica. The fungus attacks and kills thebark of branches and of young trees,causing a canker (Fig. 1-26C) thatexpands along and around the stem,girdling stems at that point and causingthe leaves above the canker to wilt anddie. Unfortunately, the fungus producesspores that are carried to other branchesand trees by wind-blown rain, by insects,and by birds. By the late 1920s, aboutthree and a half billion American chest-nut trees had become infected. Infectedtrees and branches would producesprouts from areas below the canker andthe sprouts would grow without becom-

ing infected until they were 2 to 4 inchesin diameter. At some point, and beforethey produced any fruit, the funguswould attack and kill them too. Thatway, although the huge original chestnuttrees kept producing new sprouts yearafter year for many years, their killing bythe ever-present fungus finally exhaustedthe trees and they finally died to theirroots. Hardly any trees escaped, makingchestnuts the first tree to approachextinction in modern times because of aplant disease caused by a fungus.

Dutch Elm Disease

The American elm grows to be a big,gracefully shaped and beautiful vase-liketree that exists naturally mixed withother hardwoods throughout easternNorth American forests and extending

into the Great Plains. The elm was soonadopted by early homeowners and townsettlers in North America and beautifiedmany a street by being planted in rowson both sides of the street. Then, in1930, a few elm trees in Cleveland,Ohio, began to show wilting, yellowing,and then browning of the leaves of somebranches (Fig. 1-27A). The wilted,brown leaves later fell off and the branchappeared defoliated and dead. Morebranches showed similar symptoms laterthat year or the following year, and theentire elm tree usually died (Fig. 1-27B)within 1 or a few years. Trees withsimilar symptoms were soon observed insome east coast states. The diseasebecame known as Dutch elm diseasebecause, although it had been reportedfrom France in 1917, it was the firstreport from Holland in 1921 that


received all the publicity. The Dutch elmdisease spread rapidly in North America,crossing the Mississippi River by 1956and reaching the Pacific coast states by1973. In its path, the disease has killedthe vast majority of yard, park, andstreet trees (Fig. 1-27C), although quitea few trees in their natural forest habitatare still free of the disease.

Dutch elm disease is caused by thefungus Ophiostoma ulmi. The fungus iscarried to healthy elm trees by two elmbark beetles that lay their eggs in weak-ened or dead elm trees or logs, oftenthose killed by the Dutch elm disease.The eggs hatch and produce larvae thatform tunnels, and if the tree or logs areinfected with the disease, the fungusgrows into and produces spores in thetunnels. The adult beetles then emergecovered with spores of the fungus andlook for vigorous young elm branches tofeed on. While they are feeding andcausing hardly any damage to the elmtrees, they deposit spores of the fungusin the feeding wound. The spores germi-nate and produce mycelium and morespores, both of which spread and multi-ply in the xylem vessels of the tree andcause the vessels to become clogged.

Water and minerals cannot move fromthe root to the shoots and leaves beyondthe point of clogging. The shoots andleaves subsequently wilt and die and,eventually, the entire tree dies.

Lethal Yellowing of CoconutPalms

Lethal yellowing-like symptoms ondying palm trees had been included inbrief reports from the Cayman Islands,Cuba, and Jamaica even during the 19thcentury. In 1955, coconut palm trees inthe Key West islands of Florida werenoticed to drop their coconuts prema-turely. Then, the next inflorescence hadblackened tips and set no fruit. Soon,first the lower, older leaves and then thenext younger leaves turned yellow andthen brown and died. Finally, all theleaves and the vegetative bud died (Fig.1-28A) and the entire top of the tree felloff, leaving the tall palm trunk lookinglike a telephone pole (Fig. 1-28B). Thelethal yellowing disease was first foundin mainland Florida in 1971 and killed15,000 coconut palm trees by1973,40,000 by 1974, and, by 1975, 75% of

the coconut palm trees in Dade Countywere dead or dying from the disease.Tremendous losses of palm treesoccurred in many other countries. Forexample, in Jamaica, of six million treescounted in 1961, 90% had been killedby lethal yellowing by 1981. Thousandsof hectares of palm trees were killed inMexico and also in Tanzania, more thana million coconut palm trees were killedin Ghana within 30 years, and morethan 60,000, about 50% of the palmtrees in Togo, were killed by lethal yel-lowing by 1964.

The lethal yellowing disease is causedby a phytoplasma, which is a kind ofbacterium that lacks a cell wall. Thephytoplasma lives and multiplies in thephloem sieve elements of palm trees andcauses the lethal yellowing symptoms byclogging some of the sieve tubes andinterfering with the transportation oforganic foodstuffs out of the leaves andalso by producing biologically activesubstances that are toxic and cause theyellowing and death of the leaves, inflo-rescence, and vegetative bud of coconuttrees. The phytoplasma is spread fromdiseased to healthy trees by a small planthopper. The plant hopper sucks up juice

continued

BA

FIGURE 1-28 Lethal yellowing of coconut palm trees. (A) Coconut palms at different stages of the disease, withthe disease advancing from the lower fronds upward until the apical bud is killed. (B) Telephone pole-like trunks ofcoconut palms left after trees were killed by the lethal yellows phytoplasma. (Photographs courtesy of University ofFlorida.)

36 1. INTRODUCTION

from the phloem of palm trees and, if thetree is infected with the mycoplasma, theplant hopper sucks up some phytoplas-mas also. When the plant hopper landsand feeds on a healthy palm tree, ittransmits some of the phytoplasmas itcarries into the phloem sieve elements.Once in the phloem cells, the phytoplas-mas multiply and move throughoutmuch of the phloem of the tree and causethe tree to develop the symptoms oflethal yellowing and to die.

Oak Wilts and Sudden Death

Oaks have been killed for decades byoak wilt (see page 532) caused by thefungus Ceratocystis fagacearum, but itsspread and development are slower thanthe Dutch elm disease of elm. At thesame time, the oak population is largerand distributed more widely comparedto elm. Recently, different species ofPhytophthora have been attacking andkilling oak trees in California, Oregon,Europe, and elsewhere (see pages 418).The progression of these epidemics ishard to predict, but the loss of thousandsof oak trees is certain.

Butternut Canker

Butternut trees are native to easternNorth American forests and their woodhas been used for furniture and forcarving. In 1967, butternut trees in Iowawere observed to have multiple cankerson branches and stems and to subse-quently die from the disease. Soon after-ward, the disease was found to occurwidely in the forests of the southeasterncoastal region and was shown to becaused by the imperfect fungus Sirococ-cus clavigignenti-juglandacearum. Con-trary to chestnut trees killed by chestnutblight, in butternut trees, the cankerfungus infects both young and old treesthrough wounds. Because butternuttrees do not sprout after their stem iskilled, they are lost entirely. The diseasehas spread so rapidly that the US Forest

Service estimated that about 80% of thebutternut trees in the southeast had beenkilled by the mid-1990s. The remainingsurvivors were mostly along the banks ofstreams and rivers, but most of themwere also heavily infected and were notreproducing.

Cypress Canker

Cypress trees (Cupressus semper-virens) and other species grow inMediterranean climates, including Cali-fornia, the Mediterranean, and Persia.For more than three millennia they havebeen valued as ornamentals for their tall,statuesque, columnar shape, as well asfor their wood, which is resistant towoodworms, rots, and decays. Cypresstrees are extremely long lived, some ofthem possibly living for more than 2000years. Many of the world’s centers ofcivilization, such as the Acropolis ofAthens, Olympia, Delphi, Florence, andothers, and many of the paintings overthe centuries derive much of their classicbeauty from the real or painted cypresstrees in them.

The first cypress canker outbreak wasdescribed in California in the mid-1920s, but the disease apparently existedthere for more than 10 years before that.The disease then spread inland acrossthe United States and into SouthAmerica and, apparently, was trans-ported from there across the oceans intothe Mediterranean countries, NewZealand, and South Africa so that bynow it is believed to be present in mostparts of the world where cypress treesgrow. Cypress canker or cypress blight iscaused by three species of the fungusSeiridium, particularly S. cardinale. Thefungus produces spores (conidia) thatinfect twigs and small branches throughwounds and causes cankers that kill thetwigs and branches. Resin flows out ofthe cracks of cankers while the foliage ofinfected twigs and branches turns yel-lowish to red at first, becoming reddishbrown as the twigs die. A noticeabledieback of twigs, branches, and tree tops

becomes visible at a distance. Heavilyinfected trees die. Large numbers andlarge percentages of cypress trees havebeen killed by the cypress canker fungusin the last few decades. Spread of thedisease among the remaining trees con-tinues, possibly at an accelerated rate. Asmany as one million cypress trees havebeen killed in central Italy, whichincludes Florence, with some grovesshowing more than 45% tree mortalityfrom cypress canker infections. In someof the Greek islands and in parts of themainland, 70 to 98% of the cypress treeshave been killed by this disease.

The Xylella Outbreak

The European grape, Vitis vinifera,which provides all high-quality table andwine grapes throughout the world,cannot be grown in the southeasternUnited States because it is devastated bythe indigenous xylem-inhabiting bac-terium Xylella fastidiosa, the cause ofPierce’s disease of grape. The disease hadbeen reported in California in the 1880s,but lack of appropriate vectors, appro-priate alternate hosts, and timing ofunfavorable weather conditions kept thedisease under control. As a result, grapesin California and Texas were free of thatenemy but, in 1990, the disease wasfound in Texas where it has spreadwidely among the vineyards and hascaused heavy losses. In 1998, one of itsplanthopper vectors and the bacteriumcausing Pierce’s disease were found invineyards of southern California, threat-ening not only the grape industry, butalso many of the ornamental crops ofCalifornia. Xylella bacteria wereexpected to do well in the Californiaclimate, but the absence of an effectivevector of the bacteria provided protec-tion and comfort to its agriculturalindustry. Now that the bacteria and oneof their vectors have been broughttogether in that state, the Californiagrape industry, and possibly its orna-mentals, will probably never be the sameagain.


Plant diseases may also determine the kinds of agri-cultural industries and the level of employment in anarea by affecting the amount and kind of produce avail-able for local canning or processing. However, plant diseases are also responsible for the creation of newindustries that develop chemicals, machinery, andmethods to control plant diseases; the annual expendi-tures to this end amount to billions of dollars in theUnited States alone.

Plant Diseases May Make Plants Poisonous toHumans and Animals

Some diseases, such as ergot of rye and wheat, makeplant products unfit for human or animal consumptionby contaminating them with poisonous fruiting struc-tures (Fig. 1-29).

BOX 9 Ergot, ergotism, and LSD: a bad combination

For centuries, if not for millennia, peopleand domestic animals from northernSpain to Russia, and probably else-where, suffered periodically from avariety of symptoms ranging from red-dening and blistering of the skin to aburning sensation, to excruciating painin the lower abdomen, muscle spasms,trembling, shaking, and convulsions,hallucinations and permanent insanity,gangrene and loss of fingers and limbs,and, occasionally, death. As a result ofthe initial burning sensation afflictedpersons felt, the disease became knownas “devil’s curse,” “fire,” or “holy fire.”In 1093, following a series of years ofsevere outbreaks of the disease, a reli-gious order was formed in southernFrance to help those suffering from thedisease. Because the patron saint of theorder was Saint Anthony, the diseasebecame known as “St. Anthony’s fire.”The disease varied in severity and occur-rence from year to year and appeared toaffect poor people more often than thewell-to-do.

The disease seems to have existedsince ancient times. It was described inChina as early as 1100 b.c., in Assyriain 600 b.c., and was reported to severelyaffect the troops of Julius Caesar in oneof his campaigns in France. Actually,France has experienced several seriousepidemics of “holy fire,” including thewell-documented ones of 857, of 994(which is said to have killed between

20,000 and 50,000 people), and of1093. It is speculated that the Salemwitchcraft trials in Salem, Massachu-setts, in 1692, may indeed be the resultof the “holy fire” disease caused by theconsumption of ergot-contaminatedflour. In 1722, 20,000 soldiers of thearmy of Peter the Great of Russia diedfrom consuming bread made fromseverely infected wheat. Outbreaks of “holy fire” occurred even during the 20th century. For example, in1926–1927 in Russia, as many as10,000 people were affected by thedisease, more than 200 cases werereported in 1927 in England, and morethan 200 people were affected in 1951in Provence, France, 32 of them becom-ing insane and 4 dying, all from eatingbread made from ergot-contaminatedwheat flour.

St. Anthony’s fire is known today asergotism and is the result of people andanimals consuming grain coming fromcultivated cereals and wild grassesinfected with one of several ergot-producing fungi. Ergot (from the French“argot,” which means a spur) is thefruiting structure produced by Clavicepspurpurea and related fungi in place ofthe seed of the plant (Figs. 1-29A–1-29D) and contaminates the grain afterharvest. Ergot is also the name of thedisease of cereals and grasses caused bythis and related fungi. Ergot, the plantdisease, can reduce grain yields signifi-

cantly, as each ergot replaces completelythe kernel that it infects. Most of thedamage to the crop, however, is becauseit makes the rest of the crop unfit forhuman or animal consumption unlessthe ergots are removed.

Ergots contain a number of potentalkaloids and other biologically activecompounds that affect primarily thebrain and the circulatory system. Thebest known of the ergot alkaloids islysergic acid diethylamide, the infamousLSD (Fig. 1-29E) that was widely usedas a hallucinogen by the hippie cultureof the 1960s. Depending on the weather,the host plant (wheat, rye, barley, etc.)and the species of the ergot-formingfungus, the amount of ergot in the fieldand in the harvested grain may vary, asdoes the frequency and severity of thesymptoms of ergotism (Figs. 1-29F and1-29G). Rye, which is often consumedby animals and poor people, is the mostfrequent host of ergot, whereas wheat,preferred by the rich, is the least frequenthost of ergot. The property of ergotalkaloids to constrict blood vessels andcause gangrene in humans and animalsthat consumed food contaminated withergot sclerotia was put to good use bydoctors and midwifes who used groundergots at the wound to stop excessivebleeding occurring at childbirth and atsevere accidents.

continued

38 1. INTRODUCTION

A

C D

B

FIGURE 1-29 Ergot of cereals. Ergot sclerotia replacing the kernels in the heads of (A) rye, (B) barley, and (C) wheat. (D) Ergot sclerotia from barley mixed with healthy barley kernels. (E) The chemical formula of LSD found in ergot sclerotia. (F) Calf legs showing hemorrhage causedby consumption of feed containing ergot sclerotia. (G) A sketch of several people, some of whom hadbecome maimed as a result of eating bread containing ground ergot sclerotia. [Photographs courtesyof (A–C) I. R. Evans, WCCPD, (D) G. Munkvold, Iowa State University, (F) Department of Veteri-nary Science, NDSU, and (G), Breugel, 16th Century, Art History Museum, Vienna.]



GE F

BOX 10 Mycotoxins and mycotoxicoses

Many grains (Figs. 1-30A–1-30D) andsometimes other seeds and also plantproducts such as bread (Fig. 1-30E), hay,purees, and rotting fruit (Fig. 1-30F) areoften infected or contaminated with oneor more fungi that produce toxic com-pounds known as mycotoxins. Animalsor humans consuming such productsmay develop severe diseases of internalorgans, the nervous system, and the cir-culatory system and may die. Also, manypasture grasses are infected with certainendophytic fungi that grow internally inthe plant (Fig. 1-30G) and, althoughthey do not seem to seriously damage thegrass plants, they produce toxic com-pounds that cause severe diseases in thewild and domestic animals that eat theplants. Similarly, toxic and sometimeslethal to animals are some grasses whoseseeds are infected with bacteria carriedthere by a nematode; these bacteria areoften themselves infected with a virus(bacteriophage) that induces the bacteriato produce compounds very toxic toanimals.

Ergotism is an example of a mycotox-icosis caused by food and feed madeextremely unhealthy by mycotoxins pro-duced by the fungus Claviceps purpurea.Ergotism causes very direct and dra-matic symptoms and has been knownfor many centuries, if not millennia.There have been, however, innumerable

other cases in which people or animalsbecame chronically or acutely ill byeating food or feed that contained unsus-pected toxic substances. The existenceand identity of the toxic substances hadremained unknown, the sources of suchunsafe food and feed had been littlenoticed, and the ailments affectinghumans and animals remained unex-plained. It was not until the 1960s thata severe disease of young turkey birdswas shown to be caused by moldy feedand called attention to the importance ofmycotoxins in the health of people andanimals.

Mycotoxins are toxic fungal metabo-lites that are released by relatively fewbut universally present fungi growing ongrains, legumes, and nuts. Such produce,especially when harvested while stillcontaining a high percentage of moistureor if it is damaged and stored at rela-tively high humidity, becomes moldy,i.e., it supports the growth of myco-toxin-producing fungi. Such moldyproduce is likely to carry high concen-trations of mycotoxins. Several of themycotoxins are proven carcinogens, maydisrupt the immune system, and mayretard the growth of animals or humansthat consume them. Even very smallamounts of mycotoxins bring about thedetrimental effect of mycotoxins on theimmune system and metabolism of

humans and animals, thereby posing acontinuous health hazard. At higherconcentration, which occur often onmoldy produce, mycotoxins causevisible clinical symptoms (mycotoxi-coses) in both humans and animals inthe form of nervous agitation, dermaland subcutaneous lesions, impairedgrowth, damage to kidneys and liver,cancer, and others symptoms. Myco-toxins and mycotoxicoses are describedin greater detail on page 559–560.

Although the last recorded outbreakof gangrenous ergotism occurred inEthiopia in 1978, it was not until 1960that the first general interest in myco-toxicoses was shown when the so-called“turkey X disease” appeared in farmanimals in England. It was eventuallyshown that the disease was caused byfeed contaminated with aflatoxins, andwhen these were shown to cause cancerin the liver of humans and animals, inter-est in mycotoxins skyrocketed. Aflatox-ins are extremely toxic, appear in themilk of animals consuming contami-nated feed, attack primarily the liver, andare mutagenic, teratogenic, and carcino-genic. In the last several decades, severaloutbreaks of aflatoxicosis have occurredin tropical countries where many adultsin rural populations often consumemoldy corn. Blood examinations inadults and children living in some tropi-

continued

40 1. INTRODUCTION

A

B

C

D

E

F

G

FIGURE 1-30 Mycotoxin-containing plant products infected with mycotoxin-producing fungi. (A) Portion of earof corn infected with Aspergillus. (B) Damaged corn kernels infected heavily with mycotoxin-producing Gibberellafungi. Wheat (C) and rye (D) kernels from fields infected heavily with the wheat scab-causing Fusarium spp. (E) Breadinfected with Aspergillus, Penicillium, and other fungi. (F) Orange fruit infected with Penicillium. (G) Fluorescentmycelium of an endophytic fungus in a grass plant in which it produces mycotoxins. [Photographs courtesy of (A) P.Lipps, Ohio State University, (B) R. W. Stack, North Dakota State University, (C and D) WCCPD, and (G) A. DeLucca,USDA.]


cal areas and showing various symptomsof varying intensity have revealed thepresence of aflatoxins in them, with sig-nificant seasonal variations.

In addition to aflatoxins produced bythe two aforementioned species ofAspergillus, several other equally toxicmycotoxins, e.g., ochratoxins, are pro-duced by these and by other species ofAspergillus, by Penicillium, and by otherfungi. Ochratoxins occur in cereals,coffee, bread, and in many preservedfoods of animal origin. About 20,000people in the northern Balkans seem tobe suffering from diseases caused bychronic exposure to ochratoxin. Poison-ing from moldy sugar cane is caused bya mycotoxin produced by species ofArthrinium, and in one rural area inChina it affected more than 800 personswho had ingested moldy sugar cane.Aspergillus and Penicillium are ex-tremely common in nature and arealmost always present to some extent inany feed and in most foods. Aflatoxinsare the most common mycotoxins, buteven more potent mycotoxins, e.g.,patulin, roquefortin C, and others, arealso produced by species and strains ofPenicillium.

A number of potent mycotoxins, thetrichothecins, are produced by severalspecies of Fusarium and, to a lesserextent, by species of Trichoderma, Tri-

chothecium, Myrothecium, and Stachy-botrys. The most common trichothecinis deoxynivalenol, also known as vomi-toxin. Another type of mycotoxin, zear-alenone, is produced by somewhatdifferent species of Fusarium (F. gramin-earum). Vomitoxin and zearalenoneoften occur together, especially in scabbywheat and in corn infected with Gib-berella ear rot, but they have also beenfound in moldy rice, cottonseed, flour,barley, malt, beer, and other foods. Inaddition to humans, vomitoxin andzearalenone affect cattle, swine, chickensand other birds, cats, dogs, and fish.Individuals fed contaminated food orfeed over a period respond by vomiting,refusal to eat, suppression of theirimmune system, diarrhea, loss of weight,and low milk production in the case of cows. A still different group of myco-toxins, called fumonisins, are producedby Fusarium verticillioides (F. monili-forme, F. proliferatum) and relatedspecies, primarily in corn and corn-based products. Fumonisins affect all ormost of the animals affected by the otherFusarium toxins but they also affect andare particularly toxic to horses. Inhorses, low concentrations of fumon-isins cause liquefaction of the brain,resulting in the “blind staggers” and“crazy horse disease” in which horsesdisplay blindness, head butting and

pressing, constant circling and being agi-tated, and finally die. In swine, fumon-isin attacks the heart and the respiratorysystem, in which it causes swellings, andit also causes lesions in the liver and pan-creas. In humans, fumonisins have beenlinked to cancer. In the last 10 years, out-breaks of fumonisins in feed or foodhave been reported in several states fromArizona to Virginia and from South Car-olina to the upper Midwest and in some Canadian provinces.

In most of the cases just mentioned,most of the damage is caused by themycotoxins in food or feed consumed byhumans and animals. However, forpeople and animals spending consider-able time surrounded by moldy food orfeed, there is the added danger ofdirectly breathing spores of these fungi.It is not clear how detrimental to theirhealth this is, but humans and animals,especially horses, exposed to spores ofStachybotrys chartarum develop irrita-tion of the mouth, throat and nose,shock, skin necrosis, decrease in leuko-cytes, hemorrhage, nervous disorder,and death. Stachybotrys grows on strawand feed and on moist surfaces on wallsand in air-conditioning ducts and is con-sidered one of the most important causesof the “sick building syndrome.”

Plant Diseases May Cause Financial Losses

In addition to direct losses in yield and quality, finan-cial losses from plant diseases can arise in many ways.Farmers may have to plant varieties or species of plantsthat are resistant to disease but are less productive, morecostly, or commercially less profitable than other vari-eties. They may have to spray or otherwise control adisease, thus incurring expenses for chemicals, machin-ery, storage space, and labor. Shippers may have toprovide refrigerated warehouses and transportationvehicles, thereby increasing expenses. Plant diseases maylimit the time during which products can be kept freshand healthy, thus forcing growers to sell during a shortperiod of time when products are abundant and pricesare low. Healthy and diseased plant products may needto be separated from one another to avoid spreading ofthe disease, thus increasing handling costs.

The cost of controlling plant diseases, as well as lostproductivity, is a loss attributable to diseases. Some

plant diseases can be controlled almost entirely by oneor another method, thus resulting in financial losses only to the amount of the cost of the control. Some-times, however, this cost may be almost as high as, oreven higher than, the return expected from the crop, as in the case of certain diseases of small grains. Forother diseases, no effective control measures are yetknown, and only a combination of cultural practicesand the use of somewhat resistant varieties makes it pos-sible to raise a crop. For most plant diseases, however,as long as we still have chemical pesticides, practicalcontrols are available, although some losses may beincurred, despite the control measures taken. In these cases, the benefits from the control applied aregenerally much greater than the combined direct lossesfrom the disease and the indirect losses due to expensesfor control.

Despite the variety of types and sizes of financiallosses that may be caused by plant diseases, well-informed farmers who use the best combinations of

42 1. INTRODUCTION

available resistant varieties and proper cultural, biolog-ical, and chemical control practices not only manage toproduce a good crop in years of severe disease out-

breaks, but may also obtain much greater economic benefits from increased prices after other farmers suffersevere crop losses.

BOX 11 The insect-pathogen connection: multifafaceted and important

Insects and similar organisms, such asmites and nematodes, are involved inti-mately and commonly in the facilitation,initiation, and development of manybiotic and abiotic plant diseases. Someinsects, e.g., gall-forming aphids andsome mites, cause disease-like conditionsin plants on which they feed. The impor-tance of insect involvement in the devel-opment of pathogen-induced plantdisease is so great that it can hardly beexaggerated. For some reason, however,it does not receive sufficient coverage intextbooks and in courses of plantpathology. Insects become involved indisease development in plants primarilythrough the following four types ofaction. (1) Insects visit infected plantorgans oozing bacteria or fungal sporesor plants covered with fungal spores,become smeared with bacteria or spores,and, quite passively, transfer them toother plants where they might causedisease. (2) They cause wounds on plantorgans (leaves, fruit, shoots, branches,stems, roots) on which they feed ordeposit their eggs and these allowpathogens, primarily fungi and bacteria,to enter the plant. (3) By feeding onplants, especially perennial ones, insectsweaken them and make them more vul-nerable to attack by some pathogenicfungi. (4) Insects act as vectors of certainpathogens, including a few fungi andbacteria, many viruses, and all phyto-plasmas and protozoa. Insects carrythese pathogens from diseased to healthyplants where they initiate new disease.These pathogens depend totally oninsects for transmission, i.e., in theabsence of the insect vectors there is nospread of the pathogen and no new dis-eased plants.

The first type of incidental transfer ofbacteria or fungal spores to other plantsor organs where they might causedisease probably involves many types ofcrawling, walking, or flying insects, suchas flies (Figs. 1-31A and 1-31B). Someinsects walk through or feed on flower

nectar, as, for example, do bees (Fig. 1-31C)) in pear blossoms infected withthe fireblight (Fig. 1-31D) bacterium, oron sugars released in infected areas, suchas cankers, on stems, or spots orpowdery and downy mildews on leaves,or on spots on fruit still on the tree orafter harvest. Such insects may includedifferent types of fruit flies, aphids,leafhoppers, beetles, ants, and manyothers.

Numerous insects feed and causefeeding wounds on various plant organs,e.g., fruits and roots, and several insectscause wounds when they deposit theireggs into such organs. Fungal and, some-times, bacterial pathogens, such as thesoft rot bacterium of potatoes and manyother fleshy organs, are facilitatedgreatly in entering these organs throughthe wounds made by the insects. Forexample, the plum curculio beetle (Fig.1-31E) creates wounds on fruit (Fig.1-31F) during ovipositing. The increasednumber of entry points for the fungusmade on the fruit by insects makes itpossible for fungi such as those causingbrown rot of pome and stone fruits to bemuch more damaging in orchards whereinsect control is poor.

When insects feed on roots, leaves, orshoots of plants, especially perennialones, the plants not only are wounded innumerous places and allow plant patho-genic fungi and bacteria to enter throughthe wounds and cause disease, they arealso weakened greatly, especially in theirability to mobilize their defenses againstpathogens and to protect themselvesfrom becoming diseased. This situationis commonly observed on trees whoseroots have been damaged by insects or have been defoliated by insects. Insuch trees, cankers or root rots, causedby fungi that are normally weakpathogens, develop much more rapidlyand cause severe damage or may evenkill the entire tree, something that wouldnot have happened in the absence of thedamage.

The fourth way in which insects influ-ence the development of disease in plantsis by forming close associations withcertain pathogens. In such specificinsect/pathogen associations, transmis-sion and spread of certain pathogensfrom diseased to healthy plants dependalmost entirely on the availability andinvolvement of one or a few specificinsect vectors. For example, the corn fleabeetle (Fig. 1-32A) is the main vector ofthe bacteria causing bacterial wilt ofcorn (Fig. 1-32B), whereas the stripedand spotted cucumber beetles (Fig. 1-32C) are the main vectors of the cucur-bit wilt bacteria (Fig. 1-32D). Similarly,without the vectoring ability of twospecies of elm bark beetles (Fig. 1-32E), Dutch elm disease (Fig. 1-32F), whichis caused by a fungus, would not possi-bly occur. Certain insects have alsoformed symbiotic associations withphloem-inhabiting bacteria such as thecitrus greening disease bacteria; withspecific xylem-inhabiting bacteria, e.g.,the planthoppers that transmit the bac-terium that causes Pierce’s disease ofgrapevines; with the xylem-inhabitingnematode causing pine wilt; and withphloem-inhabiting plant pathogenic pro-tozoa causing wilt diseases in coffee andpalm trees.

The association of certain insects withspecific pathogens, however, has reachedits greatest frequency with the plantpathogenic phloem-inhabiting phyto-plasmas that cause the yellows, prolifer-ation, and decline diseases of numerousplants (e.g., aster yellows, apple prolif-eration, coconut palm lethal yellowing),and also with many of the phloem-inhabiting plant viruses. Phytoplasmasare transmitted by the closely relatedleafhoppers, plant hoppers, and psyllidinsects.

Plant viruses, however, are transmit-ted by one or a few species belonging tothe following groups of insects: aphids(Fig. 1-33A) transmit a large number ofviruses, such as potato virus Y (Fig. 1-

THE INSECT—PATHOGEN CONNECTION: MULTIFACETED AND IMPORTANT 43

A

B

C D

E F

FIGURE 1-31 Examples of insects helping spread plant diseases. Common flies (A) help spread fruit diseases suchas brown rot of cherries (B). Bees (C) help spread diseases, such as fire blight of apple and pear (D). Curculio weevil(E) makes holes when ovipositing on fruit (F) that allow fruit-rotting fungi to enter the fruit. [Photographs courtesyof (A and C) University of Florida, (B) J. W. Pscheidt, Oregon State University, (D) T. Van Der Zwet, and (E and F)Clemson University.]

33B); leafhoppers and planthoppers(Fig. 1-33C) vector numerous viruses,such as the rice grassy stunt virus (Fig. 1-33D) (as well as phytoplasmas,spiroplasmas, and xylem and phloem-inhabiting bacteria); and whiteflies (Fig.1-33E) vector geminiviruses, such astomato yellow leaf curl virus (Fig. 1-

33F). Other specific virus vectors includecertain thrips, beetles, and mealybugs.The mechanisms of transmission ofviruses by their insect vectors vary con-siderably. Although all phytoplasmasand most viruses transmitted by leafhop-pers are taken up by the insect vector,circulated internally in its body, and

multiply in some of its organs beforethey are injected into the phloem of newhosts, in many of the viruses, especiallythose transmitted by aphids, the virus iscarried on or in the stylet of the vectorand through it is deposited in phloem orparenchyma cells of the new host plant.

continued

44 1. INTRODUCTION

A

C

E F

D

B

FIGURE 1-32 Examples of insects serving as specific vectors of many important bacterial and fungal diseases. Thecorn flea beetle (A) is the vector of Stewart’s wilt of corn (B). The striped cucumber beetle (C) is one of two vectorsof bacterial wilt off cucurbits (D). The elm bark beetle (E) is one of two vectors of Dutch elm disease (F). [Photographscourtesy of (A) G. Munkvold and (B) M. Carlton, both Iowa State University, (C and D) Clemson University, (E) U.S.Forest Service, and (F) Minnesota Department of Natural Resource Archives.]

THE INSECT—PATHOGEN CONNECTION: MULTIFACETED AND IMPORTANT 45

AB

CD

E F

FIGURE 1-33 Examples of insects serving as specific vectors of viruses. Aphids (A) are the most important spe-cific vector of numerous plant viruses such as potato virus Y (B). Leafhoppers and related planthoppers (C) are spe-cific vectors for many viruses, such as grassy stunt virus (D) and also for phytoplasmas and xylem- and phloem-limitedfastidious bacteria. Whiteflies (E) are the specific vectors of many devastating viruses, such as the tomato yellow leafcurl geminivirus (F). [Photographs courtesy of (A, B, E, and F) University of Florida and (C and D) H. Hibino.]

PLANT PATHOLOGY IN THE 20TH CENTURY

Early Developments

The Descriptive Phase

As agriculturists, botanists, naturalists, and other scien-tists, such as physicians, became aware of and familiarwith the existence of plant disease and with some of thecauses of plant disease, reports began to be published in

scientific, popular, and semipopular journals describingnumerous plant diseases on a variety of agricultural andornamental plants. The availability of improved magni-fying lenses and of microscopes made possible the detec-tion and description of many fungi, nematodes, and,later, bacteria associated with diseased plants. Develop-ment and introduction of techniques for growingmicroorganisms (fungi and bacteria) in pure culture byBrefeld, Koch, Petri, and others (1875–1912) con-tributed greatly to plant pathology. In 1887, Koch’s

46 1. INTRODUCTION

“postulates,” which must be satisfied before a particu-lar microorganism isolated from a diseased plant can beaccepted as the cause of the disease and not be an unre-lated contaminant, had a profound effect on plantpathology. Similarly, improvements in compound micro-scopes and in plant tissue-staining techniques allowedhistopathological and cytological studies of infectedplants that revealed the location of the pathogens(mostly fungi, nematodes, and bacteria) in relation tothe infected plant cells and tissues. After 1940, the electron microscope made it possible to visualize anddescribe most viruses and, after 1970, helped detect anddescribe the mollicutes and viroids.

During the descriptive phase of plant pathology,many observations were also made and reported con-cerning the biology of the microorganisms involved.Most reports dealt with the types of spores produced byfungal pathogens, the means of spread of pathogens, thelocation of their survival during winter, the kinds of hostplants infected, and so on. Quite often, such observa-tions were correlated with the prevailing environmentalconditions, such as rain and temperature, and with differences in disease severity among the various hosts.Different types of control practices, mostly cultural butalso some chemical ones, were tried for various diseases.The discovery that sprays with Bordeaux mixture couldcontrol the downy mildew of grape encouraged experi-mentation with this and some other compounds for thecontrol of many diseases on almost all crops.

The Experimental Phase

As the importance of plant diseases and of plant pathol-ogy as a new discipline and new profession began to berecognized in the late 1800s, scientists began to be hiredas plant pathologists and to be added to the variousUSDA and state agricultural experiment stations. Thesescientists began to experiment in all areas of plantpathology. Although new diseases and pathogens con-tinued to be discovered and described, plant patholo-gists began to ask questions and to design experimentsto answer them about how pathogens enter their hostplants, multiply, and spread within the plant; the mech-anisms of host plant cell death and breakdown;pathogen sporulation; spore dispersal, overwintering,oversummering, and germination; vector involvement;and the effect of environment on disease development,among others. They also began noticing and studyingvariability among plant species and varieties in disease expression and loss. As knowledge accumulated,experimentation also grew rapidly on ways to controlplant diseases and to avoid or reduce the losses from them.

The Etiological Phase

The etiological phase of plant pathology involved obser-vations and experiments aimed at proving the causes(etiology) of specific plant diseases. Although the etio-logical phase began with the proof of pathogenicity ofthe late blight fungus on potatoes and of the rust andsmut fungi of cereals, etiological studies were facilitatedand accelerated greatly by the development of tech-niques for the pure culture of fungi and bacteria and bythe necessity to satisfy Koch’s postulates for everydisease. Numerous reports in the late 1890s and in thefirst third of the 20th century dealt with descriptions of the symptoms of thousands of mostly fungal plantdiseases on all types of hosts, of efforts to isolate andculture the suspected pathogens, and of subsequentexperiments to prove the pathogenicity of the isolated,suspected pathogens. Many of these reports oftenincluded information on the losses estimated to becaused by the disease and on experiments about waysthat could control the disease.

The etiological phase resumed, continued, and accel-erated as new types of pathogens, such as viruses, phytoplasmas, fastidious bacteria, protozoa, andviroids, were discovered. Although the methodologieshad to be adapted to the size and properties of each typeof pathogen, the goal and the result remained the deter-mination of the etiology of the disease. The etiologicalphase often depended on, and benefited from, improve-ments in methodology and instrumentation, such as theelectron microscope, special nutrient media, density gra-dient centrifugation, electrophoresis, the development ofserological techniques, the polymerase chain reaction(PCR), and the development of DNA probes and othernucleic acid tests and tools.

The Search for Control of Plant Diseases

As mentioned earlier, in addition to prayers and sacri-fices to gods, some minor but realistic recommenda-tions for control of plant diseases were reported in thewritings of the ancient Greeks Homer (1000 b.c.),Democritus (470 b.c.), and Theophrastus (300 b.c.). Itwas not until the mid-1600s, however, that a species orvariety was reported to be more resistant to a diseasethan another related species or variety, although it isassumed that, despite the absence of written reports,growers, knowingly or unknowingly, have been foreverusing a selection of resistant plants as a control of plantdiseases. This is likely to have occurred not only becauseseeds from resistant and therefore healthier plantslooked bigger and better than those from infected sus-ceptible plants, but also because in severe disease out-

PLANT PATHOLOGY IN THE 20TH CENTURY 47

breaks, resistant plants were the only ones survivingand, therefore, their seeds were the only ones availablefor planting.

The earliest use of chemicals for the control of plantdiseases probably began in the late 1600s when somefarmers in southern England planted wheat seed thathad been salvaged from a ship wreck; they noticed that far fewer wheat plants produced from such seedwere infected with smut (bunt) than wheat plants pro-duced from other seed. This led some farmers to treatwheat seed with brine (sodium chloride solution) tocontrol bunt. In the mid-1700s, copper sulfate was sub-stituted for sodium chloride, and bunt control improvedsignificantly. This treatment is still used in the poorerparts of the world, although in many countries cop-per sulfate has been replaced by other, more effectivefungicides.

Diseases of fruit and ornamental trees were some-times too obvious to ignore and although their causewas unknown, several cures, many of them worthless,were proposed. As mentioned earlier, it was notedaround a.d. 1200 that a tree can be cured from mistle-toe infections if the branch carrying the mistletoe ispruned out. In the mid-1700s, recommendations for thecontrol of cankers included excisions of the canker andthe application of grafting wax on the cut area.However, some “scientists” incorrectly recommendedthe use of vinegar to prevent canker on trees or the use of worthless mixtures of cow dung, lime rubbishfrom old buildings, wood ashes, and river sand to curediseases, defects, and injuries of plants. In the early1800s, lime sulfur and aqueous suspensions of sulfurwere recommended for the control of mildew of fruittrees.

The Main Areas of Progress

Chemical Control of Plant Diseases

The introduction from America into Europe of thefungus causing the aggressive downy mildew disease ofgrape in the late 1870s stimulated a search by severalinvestigators, especially in France, for chemicals thatcould control the disease. In 1885, Millardet noticedthat vines sprayed with a bluish-white mixture of coppersulfate and lime retained their leaves, whereas the leavesof untreated vines were killed by the disease. After tryingseveral combinations, Millardet concluded in that sameyear that a mixture of copper sulfate and hydrated limecould effectively control the downy mildew of grape.This mixture, which became known as Bordeauxmixture, was soon shown to be equally effective against

the late blight of potato, other downy mildews, andmany other leaf spots and blights of many differentplants. For more than 100 years, Bordeaux mixture wasused more than any other fungicide against a widevariety of plant diseases in all parts of the world, andeven today it is one of the most widely used fungicidesworldwide. The discovery of Bordeaux mixture provedthat plant diseases can be controlled chemically andgave great encouragement and stimulus to the study ofthe nature and control of plant diseases.

In 1913, organic mercury compounds were intro-duced as seed treatments, and such treatments wereroutine until the 1960s when all mercury-containingpesticides were banned because of their toxicity. In themeantime, in 1928, Alexander Fleming (Fig. 1-34) dis-covered the antibiotic penicillin. This was effectiveagainst bacteria causing diseases of humans and animalsbut was not particularly effective against bacterial dis-eases of plants. Besides, the demand for use against bac-terial diseases of humans and animals was so great andthe antibiotic was so expensive that its use against bac-terial diseases of plants was considered unlikely for atleast the next 20 years. Penicillin, however, opened anew area for research in the control of plant diseases. Inthe meantime, in 1934, the first dithiocarbamate fungi-cide (thiram) was discovered, which led to the develop-ment of a series of effective and widely used fungicides,including ferbam, zineb, and maneb. Many other impor-tant protective fungicides followed. In 1965, the firstsystemic fungicide, carboxin, was discovered, and it wassoon followed by the introduction of several other sys-temic fungicides, such as benomyl.

Antibiotics, primarily streptomycin, were first used tocontrol bacterial plant diseases in 1950. Soon after, theantibiotic cycloheximide was shown to be effectiveagainst several plant pathogenic fungi. In 1967, tetra-

FIGURE 1-34 Alexander Fleming.

48 1. INTRODUCTION

cycline antibiotics were shown to control plant diseasescaused by mollicutes; a few years later, tetracycline wasshown to control plant diseases caused by fastidiousbacteria that live in the xylem of their host plants.

Appearance of Pathogen Races Resistant toBactericides and Fungicides

In 1954, it was noticed that a few strains of bacteriacausing disease in plants were resistant to certain antibi-otics, and, in 1963, strains of fungal plant pathogenswere found that were resistant to certain protectivefungicides. It was in the 1970s, however, when the useof systemic fungicides became widespread, that new isolates/strains of numerous fungal plant pathogensappeared that were resistant to a fungicide that had pre-viously been effective. The appearance of pathogen racesresistant to chemicals prompted the development of newstrategies in controlling plant diseases with fungicidesand bactericides. Such strategies included the use of mix-tures of fungicides, alternating compounds in successivesprays, and spraying with a systemic compound in theearly stages of the disease and with a broad-spectrumcompound in the later stages of the disease.

Public Concern about Chemical Pesticides

It had long been common knowledge that chemicalpesticides are toxic poisons. The word pesticide itselfmeans “pest killer.” Pests, of course, include bacteria,fungi, insects, weeds, rodents, and other living thingsthat affect humans, animals, or plants adversely.Depending on the kind of pest against which they are effective, pesticides are known as bactericides, fungicides, nematicides, insecticides, herbicides, and soon.

The public assumed at first that pesticides were toxiconly against the kinds of pests at which they were aimed.Scientists and users alike felt certain that animals andhumans were not affected by pesticides unless they werefed large amounts of pesticides accidentally or inten-tionally. For a long time, therefore, pesticides wereapplied liberally on fields, fruits, vegetables, stagnantwaters, and even directly on animals and humans tocontrol insects and diseases affecting them. Hundreds ofpesticides were produced annually, and many of thenewer pesticides were much more toxic than the earlierones, i.e., they could kill or seriously injure microbes,pests, higher animals, and humans at a much lower con-centration and faster than earlier pesticides. Some of thepesticides broke down into nontoxic or much less toxiccompounds soon after they were applied and wereexposed to air, sun, and moisture. Others, however, suchas DDT and the chlorinated hydrocarbons, consisted of

persistent molecules that resisted breakdown andremained toxic for many years or indefinitely.

A few voices of concern about using pesticides werebeginning to be heard in the 1950s, but the obvious ben-efits from controlling insects and diseases in plants,animals, and humans were so overwhelming and theassurances of pesticide safety by scientists and pesticideindustries so effective that few such concerns reachedthe wider public. Rachel Carson’s (Fig. 1-35) book“Silent Spring,” published in 1962, however, vividlydescribed the dangers of polluting the environment withpoisonous chemicals and documented several cases ofbird and fish deaths to be the results of pesticides beingaccumulated and concentrated through the food chain.Carson’s book generated a great deal of controversy butalso a much greater awareness of the possible adverseeffects of pesticides. Many scientists at first were quiteskeptical and unconvinced of Carson’s arguments. Littleby little, however, many of them agreed to do researchon the issue of safety of pesticides and began testinginsects, earthworms, birds, fish, plants, animals, waterstreams, lakes, and even soil and underground waterreservoirs for pesticides. To the surprise of many scien-tists, pesticides, particularly the persistent types, werefound in many of these bodies, sometimes in fairly highconcentrations. By that time (mid-1960s), air pollutionby automobiles and factories, water and ground pollu-tion with industrial wastes (chemicals, nuclear reactorbyproducts), and so on were also becoming issues ofconcern to the public. The “Environmental Movement”was solidifying, and concerns about environmental pol-lution of all types began to gain momentum.

FIGURE 1-35 Rachel Carson.


By the mid-1960s, all pesticides containing mercurywere banned by the U.S. government, and soon after-ward DDT and chlorinated hydrocarbons were alsobanned. Laws were passed that prohibited the use ofpesticides causing cancer in laboratory animals or muta-tions in microorganisms. All existing pesticides weresubjected to a new, stricter review, and those found tobe carcinogenic or mutagenic were banned and removedfrom the market. The uses of many pesticides that con-tinued to be allowed were further reduced as to the crop,dosage, timing, and number of applications, while theinterval between last application and harvest wasincreased. Since the mid-1980s, approximately 85–90%of the pesticides or pesticide uses previously availablefor plant disease control have been banned by the U.S.government or discontinued by the manufacturers, andit is likely that several of the remaining ones will bebanned or withdrawn in the near future. In the mean-time, the requirements for less toxic, more specific pes-ticides have increased, as have the costs of bringing apesticide to the market. The costs of potential litigationfor injury from pesticides have also increased greatly.Much stricter rules have been imposed on pesticideapplicators, pesticide applications, and handlers ofproducts treated with pesticides, with each restrictionmaking it safer, but more expensive, to apply pesticides.The current or anticipated lack of a supply of effectivepesticides has increased the effort to develop alternativecontrols. Different controls may be provided by usingantagonistic microorganisms (biological control),improving old cultural practices, and developing newones. Particularly desirable are new control methodsthat incorporate disease resistance into crop varieties,either by conventional breeding or through genetic engi-neering technologies, and using nontoxic compoundsthat activate the natural defenses of plants.

Alternative Controls for Plant Diseases

Concern over the potential toxicity of pesticides andover the continuing loss of appropriate, effective pesti-cides available for plant disease control has continuedto increase since the 1970s. This has led to the reexam-ination and improvement of many old practices and tothe development of some new cultural practices for usein controlling plant diseases. Proper cultural practicesinclude removal of plant debris and infected plant parts,use of seed free of pathogens, crop rotation with plantspecies that are immune to the kinds of pathogens thataffect the other rotation crops, soil fallow, reduced orno tillage, destruction of weeds, fertilization with appro-priate amounts and forms of fertilizer, appropriate irri-gation, adjusting the time and rate of sowing and dateof harvest, and minimizing the influx of pathogen

vectors into crops through border plants. The modifi-cation of cultural practices, use of resistant varieties, andmonitoring of the appearance and development of plantdisease epidemics that allow for a reduced use of pesti-cides have become the basis of “integrated manage-ment” of plant diseases.

It was reported early in the 20th century that somesoils, through the microorganisms they harbor orthrough other means, suppress the development ofcertain diseases caused by soilborne pathogens. AfterFleming reported in 1928 that certain fungi, such asPenicillium, inhibit the growth of other fungi and bac-teria, plant pathologists began searching for nonpatho-genic microorganisms that could be applied to plantsbefore or after infection with a pathogen and that wouldantagonize the pathogen and keep it from infecting theplant. Numerous nonpathogenic microorganisms,mostly fungi and bacteria, have been found that antag-onize various plant pathogenic fungi, bacteria, andnematodes, and some of them have been shown toprotect the host plant from infection by the pathogen.In the early 1930s, it was shown that infection of a plant with a mild strain of a virus prevented or delayed infection of the plant by a severe strain of thesame virus (“cross protection”). It has been shown morerecently that even some plant pathogenic fungi and bacteria can be controlled by pretreatment of the plantwith an avirulent or hypovirulent strain of the samespecies.

Biological control of plant diseases with antagonisticmicroorganisms is practiced to a rather limited extent.The first such control was obtained in 1963 andinvolved inoculation of the surface of stumps of freshlycut pines with spores of a nonpathogenic fungus (Phleviopsis gigantea) that protected them from infec-tion by the fungus (Heterobasidion annosum) thatcauses root and butt rot of pines. In 1972, control ofthe crown gall bacterium was obtained by preinoculat-ing seeds or roots of transplants of stone fruit trees witha related but nonpathogenic bacterium, and control ofthe tobacco mosaic virus in tomato fields was obtainedby preinoculating tomato seedlings with a nonpatho-genic strain of the virus produced by mutating the virusartificially. Experimentally, biological control can beobtained against many plant pathogenic fungi and bac-teria infecting foliage or roots in the field or fruits instorage, and also against some nematodes, but fieldapplications are still mostly ineffective. The control ofviral diseases by cross protection is used in the tristezadisease of citrus and in some other virus diseases. A newand promising type of biological control of viral dis-eases, discovered in the late 1980s, uses the introductionof one or several appropriate viral genes into host plantsthrough genetic engineering and expression of these

50 1. INTRODUCTION

genes by the host. These genes then prevent or delayinfection of the plant by the virus.

Another recent, very exciting and promising means ofplant disease control is through the use of pathogenicmicroorganisms or chemical compounds that cause tinynecrotic lesions in the treated plant and, by so doing,activate the defenses of the whole plant against subse-quent infections by pathogens of the same or differenttypes. This has been called systemic acquired (orinduced or activated) resistance. In the early 1990s, nontoxic chemical compounds called plant defense activators were synthesized that, when applied to plants, activate the systemic defenses of plants againstpathogens without causing necrotic lesions. The firstsuch compound, named Actigard, was market testedwith considerable success in 1996.

Interest in the Mechanisms by Which Pathogens Cause Disease

Once it became apparent that fungi and other micro-organisms were the causes rather than the results ofplant disease, efforts began to understand the mecha-nisms by which microorganisms cause disease. In 1886,deBary, working with the Sclerotinia rot disease ofcarrots (Fig. 1-36) and other vegetables, noted that hostcells were killed in advance of the invading hyphae ofthe fungus and that juice from rotted tissue could breakdown healthy host tissue, whereas boiled juice fromrotted tissue had no effect on healthy tissue. DeBaryconcluded that the pathogen produces enzymes andtoxins that degrade and kill plant cells from which thefungus can then obtain its nutrients. In 1905, cytolytic

enzymes were reported by L. R. Jones to be involved inseveral soft rot diseases of vegetables caused by bacte-ria. In 1915, it was reported that the pectic enzymes pro-duced by fungi (Fig. 1-37A) play a significant role intheir ability to cause disease on plants, but it was notuntil the 1940s that cellulases were implicated in plantdisease development.

After deBary, many attempted to show that mostplant diseases, particularly vascular wilts and leaf spots,were caused by toxins secreted by the pathogens, butthose claims could not be confirmed. A 1925 suggestionthat the bacterium Pseudomonas tabaci, the cause of thewildfire disease of tobacco, produces a toxin that isresponsible for the bacteria-free chlorotic zone (“halo”)(Fig. 1-37B) surrounding the bacteria-containingnecrotic leaf spots was confirmed in 1934. The wildfiretoxin was the first toxin to be isolated in pure form inthe early 1950s. In 1947, a species of the fungusHelminthosporium (Bipolaris), which attacked andcaused blight only on oats of the variety Victoria and itsderivatives, was shown to produce a toxin named vic-torin. This toxin could induce the symptoms of thedisease only on the varieties susceptible to the fungus.Many other bacterial and fungal toxins were subse-quently detected and identified. The toxins exhibitedseveral distinctive mechanisms of action, each affectingspecific sites on mitochondria, chloroplasts, plasmamembranes, specific enzymes, or specific cells such asguard cells. In addition, several detailed biochemicalstudies were carried out to elucidate the mechanisms bywhich toxins affect or kill plant cells or by which cellsof resistant plants avoid or inactivate them.

Early observations that in many diseases the affectedplants showed stunting, whereas in others they showedexcessive growth, tumors, and other growth abnormal-ities (Fig. 1-37C), led many investigators to suspectimbalances of levels of growth regulators in diseasedplants. In 1926, E. Kurosawa showed that the excessivegrowth of rice seedlings (Fig. 1-37D) infected with thefungus Gibberella could also be produced by treatinghealthy seedlings with sterile culture filtrates of thefungus. In 1939, the growth regulator produced by thefungus was identified and named gibberellin. By the late1950s, numerous plant pathogenic fungi and bacteriawere shown to produce the plant hormone indoleaceticacid (IAA). In the mid-1960s, a cytokinin was shown tobe produced by the bacterium that causes the fasciation(leafy gall) disease of peas and other plants, and thesymptoms of the disease could also be reproduced bytreating the plants with kinetin, which is an animal-derived cytokinin. In the late 1970s and in the 1980s,detailed studies were made of the mechanisms of diseaseinduction in the Agrobacterium tumefaciens-inducedcrown gall disease of many plants.FIGURE 1-36 Sclerotinia white mold of carrots.


These studies showed that the bacterium introducesinto plant cells a specific part of transforming DNA (T-DNA) of its transformation-inducing plasmid (Tiplasmid). This DNA becomes incorporated into and istranscribed by the plant cell. The T-DNA contains

several genes, one of which codes for IAA and one fora cytokinin. When these genes are expressed by the plantcell, the growth regulators they produce lead to uncon-trolled enlargement and division of affected plant cells.Depending on the relative concentration of the two

A

C D

B

FIGURE 1-37 Chemical weapons used by pathogens in causing disease. (A) Apple infected withgray mold and showing the action of the pectinolytic enzymes ahead of the fungal pathogen. (B) Haloaround lesions on tomato leaf show the presence of toxin produced by the bacterial pathogen. (C) Formation of crown gall as a result of excessive amounts of growth regulators produced by thecrown gall bacterial pathogen. (D) Excessive growth of rice seedlings is the result of excessive pro-duction of gibberellin growth regulators by the fungal pathogen. [Photographs courtesy of (B) R. J.McGovern, (C) University of Florida and (D) R. K. Webster, University of California.]

52 1. INTRODUCTION

growth regulators, the infection may result in the pro-duction of unorganized galls (tumors), partially organ-ized teratomas, or hairy roots.

From the mid-1950s until about 1980, a great manystudies were carried out on the effect of infection on therespiration of host cells and on the possible role ofaltered respiration in plant defenses, and resistance, toinfection. Similarly, numerous studies were carried outon the types of host cell enzymes that may be activatedon infection, the types and amounts of metabolites (sub-stances) accumulating following infection, and, particu-larly, the types and amounts of phenolic compounds andphenol-oxidizing enzymes produced following infection.These studies provided a great deal of information onmany of the biochemical reactions that go on in plantcells following infection but did not entirely explain themechanisms by which plants defend themselves againstpathogens.

From the early 1970s onward, many studies havebeen devoted to the elucidation of the numerous meta-bolic changes associated with the hypersensitiveresponse, i.e., the localized defense reaction of a resist-ant plant to a pathogen. In the hypersensitive response,numerous enzymes, known as plant pathogenesis-related (PR) proteins, are activated. Some of the PR pro-teins induce the synthesis of ethylene, which is a planthormone able to induce many stress responses; someinduce the production of oxidative enzymes and pro-teins involved in cell wall modification and strengthen-ing against pathogen invasion; some synthesizeantimicrobial compounds such as phytoalexins; andsome are enzymes that attack and dissolve componentsof the cell wall of the pathogen or are proteinaseinhibitors that neutralize specific enzymes of thepathogen. Information on such proteins is, potentially,of great practical significance for possible use to genet-ically engineer plants, which, upon infection, willproduce sufficient amounts of appropriate pathogenesis-related proteins that will result in protecting the plantsfrom becoming diseased.

The Concept of Genetic Inheritance of Resistance and Pathogenicity

In 1894, Eriksson showed that the cereal rust fungusPuccinia graminis consists of different biological racesthat cannot be distinguished morphologically but differin their pathogenicity to their cereal host; for example,some of them being able to attack wheat, but not theother cereals, such as oats and rye.

In 1902, H. M. Ward recognized the necrotic defensereaction, which E. C. Stakman later (1915), studying itin the cereal rusts, called the “hypersensitive response.”

In 1964, Z. Klement and colleagues recognized that thehypersensitive response also operates against bacterialplant pathogens. In 1972, a similar necrotic or hyper-sensitive response was described in animals and wascalled apoptosis (= falling out); this research showed theexistence of many common features in the defense reac-tions of plants and animals.

In 1905, Biffen reported that the resistance of twowheat varieties and their progeny to a rust fungus wasinherited in a Mendelian fashion. In 1909, Orton,working with the Fusarium wilts of cotton, watermelon,and cowpea, distinguished among disease resistance,disease escape, and disease endurance (tolerance). In1911, Barrus showed that there is genetic variabilitywithin a pathogen species; i.e., different pathogen racesare restricted to certain varieties of a host species. Soonafter, Stakman and colleagues (1914) established thatmorphologically indistinguishable races of a pathogenwithin a pathogen species differ in their ability to attackcertain varieties. The pathogen races can be distin-guished by their ability to infect different varietieswithin a set of host differential varieties (Fig. 1-38).Their work helped explain why a variety that was resist-ant in one geographic area was susceptible in another,

FIGURE 1-38 Differential reaction of leaves of wheat varieties toa race of wheat rust. This test is used to monitor the appearance ofnew rust races. (Photograph courtesy of USDA.)


why resistance changed from year to year, and whyresistant varieties suddenly became susceptible. In allcases the change was due to the presence or appearanceof a different physiological race of the pathogen.

The genetics of disease resistance and susceptibilityremained obscure until 1946 when Flor (Fig. 1-39A),working with the rust disease of flax, showed that foreach gene for resistance in the host there was a corre-sponding gene for avirulence in the pathogen and foreach gene for virulence in the pathogen there was a gene for susceptibility in the host plant (a gene-for-generelationship).

In 1963, Vanderplank (Fig. 1-39B) suggested thatthere are two kinds of resistance: one, known as verti-cal resistance, is controlled by a few “major” resistancegenes and is strong but is effective only against one ora few specific races of the pathogen, and the other,known as horizontal resistance, is determined by many“minor” resistance genes and is weaker but is effectiveagainst all races of a pathogen species. It has been pro-posed that each major or minor gene for resistance represents one or several steps in a series of biochemi-cal reactions and that it usually operates in conjunctionwith several other genes. Together, these genes enablethe plant to produce certain types of plant cell sub-stances and structures that interfere with, or inhibit, thegrowth, multiplication, or survival of the attackingpathogen, and in that way they inhibit, or stop, thedevelopment of disease. Some of the plant defense struc-tures and substances exist before the plant comes intocontact with the pathogen, but the most effectivedefense structures and substances are produced inresponse to attack by the pathogen.

In 1946, E. Gaümann proposed that in manyhost–pathogen combinations plants remain resistantthrough hypersensitivity; i.e., the attacked cells are sosensitive to the pathogen that they and some adjacentcells die immediately and in that way they isolate orcause the death of the pathogen. In the early 1960s, it

was proposed that, in some cases, disease resistance isbrought about by phytoalexins, i.e., antimicrobial plantsubstances that either are absent or are present at non-detectable levels in healthy plants, but accumulate tohigh levels in response to attack by a pathogen.

The genetic inheritance of pathogenicity in pathogenshas been shown to parallel, and to mirror, that of resist-ance in plants, as mentioned previously. Some pathogengenes for virulence and even more genes for avirulencehave been isolated, and the sequences as well as theproducts (enzymes, toxins, inhibitors, growth regula-tors) of several of these genes are also known.

Epidemiology of Plant Disease Comes of Age

Epidemiological observations, i.e., observations con-cerning the increase of disease within plant populationsand how such increases relate to environmental factors,were recorded with many plant diseases as the latterbegan to be reported. Little effort was made, however,to correlate and utilize such information in controllingplant diseases. From studies of the apple scab disease,Mills in 1944 developed a table listing the duration ofrain required at each temperature for apple buds, leaves,and fruit to become infected by the ever-present applescab fungus. He and others then could use this infor-mation to predict whether infection would take placeand whether, therefore, control measures (fungicides)should be applied.

It was in 1963, however, that Vanderplank (Fig. 1-39B), through the book “Plant Diseases: Epidemics andControl,” established epidemiology as an important and interesting field of plant pathology. In his book,Vanderplank discussed the principles and variables inplant disease epidemics, stated the difference in thedevelopment and control of monocyclic and polycyclicpathogens, and described the general structure and pat-terns of epidemics. A few years later, modeling of plantdiseases was introduced, which, through analysis ofinformation on the host, the pathogen, and their inter-actions, collected at various points in time and undervarying environmental conditions, could predict thecourse of an epidemic. In 1969, the first computer simulation program of plant disease epidemics was pub-lished for the fungal-induced early blight disease oftomato and potato. The simulation program was devel-oped by modeling each stage of the life cycle of thepathogen as a function of various environmental condi-tions designed to stimulate the pathogen. Since the mid-1970s, disease modeling and computer simulation ofepidemics have been developed for many diseases and, together with newly developed disease-monitoringinstrumentations, have been used in plant disease-

A B

FIGURE 1-39 (A) H. H. Flor. (B) J. E. Vanderplank.

54 1. INTRODUCTION

forecasting systems. Disease forecasting has become animportant component of integrated pest management(IPM) and has helped reduce the amounts of pesticidesapplied to crops without reducing yields.

PLANT PATHOLOGY TODAY AND FUTURE DIRECTIONS

Molecular Plant Pathology

Since 1980, great emphasis has been placed on deter-mining the specific molecule and the “genetic connec-tion” of any substance involved in disease development.Because viruses and bacteria are small in size and because a great deal of background information is available on them, more molecular studies have beencarried out with them than with the much larger fungiand nematodes. Already the number, location, size,sequence, and function of most or all genes of manyviruses are known in detail. Many of these genes havebeen excised from the virus and have been transferredeither to host plants, to which they often convey resist-ance, or into bacteria, in which they are expressed andthe proteins they code for are isolated and studied.Similar transfers have been accomplished with a few bac-terial and fungal genes coding for certain pathogenesis-related proteins.

The beginnings of molecular plant pathology canprobably be traced to the isolation by W. Stanley in1935 of the tobacco mosaic virus as a crystallineprotein, which he believed to be infectious. Although 2years later it was shown that the protein also containeda small amount of RNA, it was not until 1956, whenGierrer and Schramm showed that the ribonucleic acidand not the protein of tobacco mosaic virus was respon-sible for the infection of plant cells and for the repro-duction of complete virus particles. In the meantime, in1941 Beadle and Tatum showed that one gene codes forone enzyme. The following year (1942) Flor showedthat a single gene is responsible for pathogenicity in theflax rust fungus and that the rust fungus gene corre-sponds to a single gene for resistance in the flax plant(the gene-for-gene concept). In 1953, Watson and Crickshowed that DNA exists in a double helix and their dis-covery impacted greatly all of biology. In the mid-1960s,studies of tobacco mosaic virus led to the full elucida-tion of the genetic code according to which specific basetriplets of DNA (and RNA) code for a certain aminoacid. This was followed by the description in the 1970sthrough the 1990s of all the genes of tobacco mosaicand of many other viruses.

By the mid-1970s, the studies of A tumefaciensrevealed that the T-DNA of its Ti plasmid contained

several genes of which two, coding for growth regula-tors, were responsible for the production of tumors(galls) by the infected plants. It was later shown that thetwo genes could be removed and replaced with one ormore genes from other organisms such as plants, otherbacteria, viruses, and even animals, genes that could betransferred into and expressed (translated) by the plantcells. This discovery made possible the introduction offoreign genes into plants at will and, combined withtissue culture, which made possible the production ofwhole plants from single cells, it ushered in the era ofgenetic engineering of plants. Subsequently, it was dis-covered that foreign DNA can be introduced into plantcells in several ways, including using viruses as vectors,bombarding plant cells with foreign DNA, and growingplant cells in the presence of foreign DNA. Several viralgenes coding for the coat protein or other structural ornonstructural proteins, and some noncoding regions,have been engineered into plants, and many of themhave been shown to make the plant more or less resist-ant to the virus. Also, some bacterial and fungal genes,coding for enzymes that break down the cell wall of thepathogen, have been engineered into plants and haveprovided the plant with resistance to these pathogens.

In 1984, P. Albersheim and colleagues identified themolecule in the cell wall of the oomycete Phytophthoramegasperma that acts as the elicitor of the defenseresponse in its soybean host. It was shown later that theelicitor accomplishes this by interacting with a receptor molecule on the plant cells. In the same year, the firstavirulence gene was isolated from the bacteriumPseudomonas syringae pv. glycinea by B. J. Staskawiczand colleagues. These two discoveries helped launchresearch that improved our understanding of pathogenvirulence and plant disease resistance greatly. In 1986,bacterial hypersensitive response protein (hrp) geneswere discovered. It was thought at first that the hrpgenes were required for bacterial pathogenicity and production of the hypersensitive response; it is knownnow that they affect the transport of proteins in patho-genic bacteria and also the transport of bacteria intoplant cells.

The first practical results of molecular plant pathol-ogy in improving disease resistance came in 1986 whenR. Beachy and colleagues obtained tobacco plants resist-ant to tobacco mosaic virus (TMV) by transformingthem; i.e., introducing into them the coat protein geneof the virus in a way that the plants could express thegene and produce the virus protein. Such transformedplants are called transgenic, and the resistance theyacquire is called pathogen-derived resistance. In 1989,M. B. Dickman and P. E. Kolattukudi transformed afungus, that normally could enter host plants onlythrough wounds, with a cloned gene coding for the

PLANT PATHOLOGY TODAY AND FUTURE DIRECTIONS 55

enzyme cutinase. That enzyme enabled the fungus topenetrate host plants directly through the cuticle,thereby proving that cutinases play a role in the directpenetration of some plants by fungi. Two years later, in 1991, R. Broglie and co-workers showed that plantstransformed with the gene that codes for chitinaseexhibit enhanced resistance to disease by fungi thatcontain chitin in their cell walls. In the meantime, in1990, R. Cheim and colleagues obtained transgenictobacco plants that expressed increased disease resist-ance by transforming them with the gene for stilbenesynthetase, the enzyme that synthesizes a phytoalexin.

Discoveries in molecular plant pathology came fastand furious in the 1990s. The concept of systemicacquired resistance (SAR) burst onto the scene throughthe discovery of D. F. Klessig and colleagues and J. Ryalsand co-workers that salicylic acid, a relative of aspirin,is associated with SAR. The first fungal avirulence gene(avr9) was isolated from Cladosporium fulvum by P. J.G. M. De Wit, while the first plant resistance gene (Hm-1) was isolated from corn by S. P. Briggs and J. D.Walton. The latter also showed that Hm-1 operates byproducing a protein that detoxifies the host-selectivetoxin of the pathogen Cochliobolus carbonum. The onlyresistance gene conferring resistance in tomato to a bac-terial pathogen through the hypersensitive response wasisolated by G. B. Martin and colleagues in 1993. In sub-sequent years, dozens of plant disease resistance geneswere isolated from many plants. All these genes shareda leucine-rich repeat in the protein they coded for.Tomato plants transformed by B. Baker and co-workerswith the tobacco plant resistance gene N, which makestobacco resistant to tobacco mosaic virus, were alsomade resistant to the virus, proving that at least someresistance genes may function in species other than theone in which they normally occur. Furthermore, it wasshown by V. M. Williamson and colleagues (1998) thata single cloned disease-resistance gene from tomato canconfer resistance to both a nematode pathogen and aninsect. It was also shown during this period (T. Shiraishiet al., 1992) that plant pathogens produce proteins thatactively suppress the defense reactions of their hostplants. In addition, the avirulence proteins of somepathogens contain signals that allow these proteins notonly to be introduced into plant cells, most likelythrough the bacterial hrp protein system, but also tomove into and function in the plant nucleus.

A new type of defense against pathogens was unveiledwhen it was discovered that many organisms, includingplants, fungi, and animals, are capable of “RNA silenc-ing,” i.e., of regulating genes based on targeting anddegrading sequence-specific RNAs. In plants, RNAsilencing has been shown to serve as a defense againstvirus infections. As would be expected, however, many

plant viruses carry genes that encode proteins that sup-press the silencing of their RNA by the plant. RNAsilencing can be induced experimentally and targeted toa single specific gene or to a family of related genes. Itis believed that RNA silencing genes will soon play animportant role in engineering resistance into plants.

Advances in molecular plant pathology have also pro-vided a new set of diagnostic tools and techniques thatare used to detect and identify pathogens even whenthey are present in very small numbers or in mixtureswith other closely related pathogens. Such tools includedetection with monoclonal antibodies, analysis ofisozymes or of fatty acid profiles of pathogens, analysisof fragments of their nucleic acids produced by specificenzymes, calculation of percentages of hybridization oftheir nucleic acids, and determination of nucleotidesequences of the nucleic acids of the pathogens. Sincethe mid-1980s, segments of DNA (probes), comple-mentary to specific segments of the nucleic acid of themicroorganisms, have been labeled with radioactive iso-topes or with color-producing compounds and are usedextensively for the detection and identification of plantpathogens. Numerous techniques, often referred to bytheir acronyms, have been developed and are used; someof them are better suited for diagnosing one or moretypes of pathogens. For at least some pathogens, PCR,with selected differential random sequences of differentspecies, can be effective for the detection and identifi-cation of each of these species. At other tests, PCR ofsequence segments of rDNA internal transcribed spacer(ITS) regions are used or PCR of other genes or spacersof the fungal DNA is carried out. The product is thendifferentiated by digestion with restriction enzymes andgel electrophoresis and detection of differential randomfragment length polymorphisms (RFLP) or use of PCRtogether with DNA hybridization in a reverse dot blothybridization (RDBH) assay using PCR of selectedRAPD markers. Reverse transcription PCR (RT-PCR) orimmunocapture RT-PCR (IC/RT-PCR), direct bindingPCR (DB-PCR), and a combination of PCR and enzyme-linked immunosorbent assay (ELISA) tests are oftenused successfully, especially for viruses.

An area of molecular plant pathology that is going topay multiple dividends in the future is that of genomics,i.e., sequencing of the entire genomes of plants and theirpathogens. Already, the genomes of the experimentalplant Arabidopsis thalliana, of several plant viruses andviroids, and of the plant pathogenic bacteria Ralstoniasolanacearum and Xylella fastidiosa, the white rotfungus Phanerochaete chrysosporium, and the modelnematode Caenorhabditis elegans have been sequencedin their entirety. Significant progress has already beenmade in sequencing the entire genomes of the verydestructive plant pathogenic fungi Magnaporthe grisea,

56 1. INTRODUCTION

cause of rice blast; Ustilago maydis, cause of corn smut;Cochliobolus heterostrophus, another pathogen of corn;Botrytis cinerea, the gray mold of many fruits and veg-etables; Fusarium graminearum, cause of head scab ofwheat; and Phytophthora infestans, cause of the blightof potato and of many other pathogens of crops. Oncethe genomes have been sequenced, it will be easier tolocate, identify, compare, isolate, and manipulate thegenes for pathogenicity in the pathogens and of resist-ance in their host plants, as well as manipulate the intro-duction of them into specific locations of the plantgenome where they would be most effective.

The molecular phase of plant pathology is expectedto develop a great deal more and to make contributionsin ways that we can hardly imagine at present. One areain which molecular plant pathology is expected to con-tribute greatly and to provide tremendous benefits is the

area of detection, identification, isolation, modification,transfer, and expression of genes for disease resistancefrom one plant to another. Several such resistance geneshave already been identified, isolated, transferred intosusceptible plants, and, when expressed, made the plantsresistant. The possibility that molecular plant pathologycan modify and combine resistance genes makes likelythe future utilization of resistance genes from unrelatedplants or from other organisms, and perhaps even thesynthesis of artificial genes for resistance for incorpora-tion into crop plants. The practical implications of suchdevelopments cannot be overestimated, as they are likelyto revolutionize the control of plant diseases by provid-ing us with cultivars that can resist disease in the pres-ence of the pathogen, without the need to use anypesticides.

BOX 12 Plant biotechnology — the promise and the objections

Plant biotechnology can be defined asthe use of tissue culture and genetic engi-neering techniques to produce geneti-cally modified plants that exhibit new orimproved desirable characteristics. Thedesirable characteristics include, amongothers, better yields, better quality, andgreater resistance to adverse factors,including diseases, pests, and environ-mental conditions such as freezes,drought, and salinity. Plant biotechnol-ogy also makes possible the productionin plants of useful proteins coded bymicrobial, animal, or human genes.Plant biotechnology has shown that allof these goals are attainable, at least inthe kinds of plants on which they havebeen attempted. The number of crop,ornamental, and forest plants that havebeen modified genetically and releasedby university and industry scientistsaround the world is in the thousands andcontinues to grow.

There are numerous cases in whichplant biotechnology is used successfullyto produce crop plants that avoid orresist certain plant pathogens. Someplants have been rendered resistant tospecific pathogens by genetically engi-neering (transforming) them with iso-lated specific genes that provide

resistance against these pathogens.Transformed plants become resistant bycoding for enzymes that mobilize otherenzymes that carry out numerous defen-sive functions, such as breaking downthe structural compounds of thepathogen. Several of the enzymesproduce compounds in the plant that aretoxic to or otherwise inhibit the growthand spread of the pathogen boththrough the plant and to other plants.Other plants have been transformedwith animal (mouse) genes that code forantibodies (plantibodies) against a coatprotein of the pathogen. Genetic engi-neering has been particularly effective inproducing plants resistant to viruses byincorporating viral genes in the cropplants that code for virus coat protein,for altered movement protein, or byincorporating in the plant noncodingsegments of virus nucleic acid or evensegments of the nonsense strand of thevirus nucleic acid. Many of these cropplants have been tested for resistance inthe field with excellent results.

Practical examples of successfulgenetic engineering of disease-resistantplants include melon, squash, tomato,tobacco, and papaya crops that are pro-tected from a variety of viral diseases.

The success of genetically engineeredpapaya for resistance to papaya ringspotvirus has saved the papaya as a crop inHawaii and in the Far East (Fig. 1-40).Numerous other cases are still underdevelopment. For example, engineeringtobacco with a chimeric transgene con-taining sequences from two differentviruses (turnip mosaic and tomatospotted wilt) resulted in new plantsresistant to both viruses. Similarly, engi-neering tomato plants with a truncatedversion of the gene coding for the DNAreplicase of one of the very destructivegeminiviruses resulted in plants resistantnot only to the virus from which thetransgene was obtained, but also to threeother viruses. In other work, potatoplants engineered with a chimeric geneencoding two insect proteins exhibitingantimicrobial activities showed signifi-cant resistance to the late blightoomycete and their tubers were pro-tected in storage from infection by thesoft rot-causing bacteria. In other work,raspberry plants engineered with thegene coding for the common plant polygalacturonase-inhibiting protein(PGIP) became resistant to the gray moldfungus Botrytis cinerea, although thetransgene in raspberry, but not in other

ASPECTS OF APPLIED PLANT PATHOLOGY

ASPECTS OF APPLIED PLANT PATHOLOGY 57

FIGURE 1-40 Increased resistance to disease through biotechnology. Comparison of “Sunrise” papaya plants sus-ceptible to papaya ringspot virus (PRSV) surrounding a block of the genetically similar “Rainbow” papaya plants thathad been transformed for resistance to PRSV. Both “Sunrise” and transgenic “Rainbow” plants were inoculated bynatural PRSV inoculum. (A) “Sunrise” (left) and transgenic “Rainbow” (right) plants 9 (B) 18, and (C) 23 monthsafter transplanting. (D) Aerial photograph of the “Rainbow” block 28 months after transplanting, by which time the“Sunrise” plants surrounding the “Rainbow” block are almost totally destroyed by the virus, whereas the transgenic“Rainbow” plants remained free of virus, look healthy, and produced excellent yields. [Photographs courtesy of Ferreira (2002). Plant Dis. 86, 101–105.]

plants, is expressed only in immaturegreen fruit.

In addition to helping us engineerplants resistant to disease, molecularbiology and biotechnology have madepossible the development and use ofnontoxic chemical substances that, whenapplied to plants externally, stimulatethe plants and elicit the activation oftheir natural defense mechanisms, i.e.,activation of the localized defense mech-anism (hypersensitive response) and sys-temic-aquired resistance (SAR). Twosuch chemical substances that have beenproven effective and are used commer-cially are Actigard, where one applica-

tion increases the plants’ resistanceagainst some bacterial and some fungaldiseases for several weeks, and Messen-ger, derived from the fire blight bac-terium gene coding for the proteinharpin, which elicits a hypersensitiveresponse and SAR in plants. Messenger,which also promotes plant growth, iseffective against a variety of diseases ofseveral crops, including strawberry,tomato, and cotton.

In transforming plants for diseaseresistance or for any other characteristic,it is necessary to modify their nucleicacid by adding genetic material fromanother plant or, rarely, from an animal

or a pathogen. In most cases, thesenucleic acids are or become active, pro-ducing in the plant compounds that maybe toxic to pathogens or pests and, pos-sibly, to humans. In addition, some ofthis nucleic acid may find its way,through cross-pollination or throughtransfer by microorganisms, into weedsor other wild plants, making these plantsalso resistant to the pathogen or pest.Several kinds of plants have been engi-neered to produce toxins against certaininsects; to produce vaccines againstcertain human pathogens; to produceanimal or human growth hormones; orto produce pharmaceutical compounds

continued

58 1. INTRODUCTION

that can be used to treat diseases ofhumans and animals. The fear by somepeople that some or all of these productswill get into the human diet or in theanimal food chain and cause allergiesand other adverse health effects hasresulted in significant unfavorable pub-licity for such products and for biotech-nology. That type of publicity has, inturn, led many large buyers to refuse tobuy and use products produced bygenetically modified organisms (GMO).Following the adverse publicity, severalgovernments, especially in Europe,passed laws and raised barriers to theimportation of products derived fromgenetically modified organisms.

In addition to the argument againstintroducing into crops, through geneticengineering, new proteins that may causeallergic reactions in some people, therehave also been arguments againstbiotechnology because it takes posses-sion of, patents, and monopolizes geneticmaterial that was previously availableand free to everybody; it replaces thenumerous sustainable local varieties witha few genetically engineered ones, theseed of which the farmers must buy fromlarge companies every year; it threatensthe development of pests and pathogensthat can resist or overcome the trans-formed resistant crops; it threatens tolead to the use of larger amounts of

herbicides with crops like those madeherbicide resistant while the weeds arestill susceptible; it threatens unknownnumbers of nontarget organisms thatmay be affected adversely by the protein;it threatens to upset the plant balance,and through it the entire biotic balanceof the environment, by having such newgenes transferred naturally to nontargetplants and their proteins, harmless ornot, consumed by microorganisms,animals, and humans unaccustomed tosuch proteins; it threatens the occurrenceof accidents in which crops transformedfor the production of pharmaceuticals,vaccines, and so on become mixed withedible crops.

BOX 13 Food safety

In recent years, food safety has beenthreatened by a number of events anddevelopments that allow foodbornemicroorganisms pathogenic to humans,e.g., the bacteria Salmonella, Listeria,Escherichia coli strain 0157:h17, theprotozoa Cyclospora, Cryptosporidium,and Giardia, and the hepatitis A virus,to reach and contaminate our food in avariety of ways. These include (a)increased processing of fresh plantproduce (e.g., fruit juices, fruit or veg-etable purees, cole slaw, fruit sectionsand cut-up vegetables for salads in bulkor in plastic bags) that may sometimescontain produce that carries a significantamount of food-spoiling bacteria andmycotoxin-producing fungi; (b) inade-quate food processing procedures thatallow survival of human pathogens inthe processed product; (c) long storageof foods that encourages the develop-ment of pathogenic microorganisms; (d)application to fruit and vegetable fieldsof improperly aged or poorly treatedmanure that carries human pathogens;(e) application on the plants of irrigationwater that may be carrying one or manyof the aforementioned human pathogensdue to contamination by humans andanimals through run-off of waste waters,etc.; (f) unacceptable hygiene of har-vesters, handlers, and packers after usingthe toilet that results in the contamina-tion of fruits and vegetables with humanpathogens; and (g) the presence of pets,

livestock, and wildlife animals, some ofwhich may carry human pathogens ontheir bodies or in their feces to fruits andvegetables. To these should be added theever-increasing shipment of food itemsamong various geographical points of acountry and worldwide, which maygreatly multiply and expand the effectsof a local contamination of food products.

One of the main effects of fears aboutfood safety is economic. Not only is itcostly to take all measures necessary tosecure food safety, but there is also thefear and cost of rejection of produceshipments at the point of destination.Similarly, there is the possibility ofrefusal of buyers to purchase producefrom farms that do not meet the buyer’sfood safety standards. In the UnitedStates and other developed countries,many of the large buyers of food products for their mills, processing factories, or chain stores demand third-party audits of farms by certified spe-cially trained individuals and consultingfirms regarding the employment by thefarm of all necessary precautions in thetype of manure they may be using, the quality of water used for irrigation,the health and hygiene of their workersand plant handlers, and so on. Also, toavoid unjustified accusations of offeringcontaminated produce, farmers are orwill soon be expected to have a trace-back system in place. This will happen

by identifying all produce leaving thefarm as to origin and date of packing sothat if contamination is found in theproduce in the marketplace, the sourcewill be easy to identify and appropriatemeasures may be taken. Also, it willbecome necessary to keep food safetyrecords, such as documenting workertraining sessions, recording the results ofwater tests, details of manure applica-tions, if any, of dates, methods, and ratesof irrigation, and so on, as well as ofdisease outbreaks among the farmworkers. To protect themselves frompurchasing contaminated produce,buyers of large quantities will test orhave the produce tested with serologicaland molecular-based diagnostic tech-niques that can already detect, forexample, as few as three Salmonella cellsper 25 grams of naturally contaminatedfood.

In addition to the aforementionedtypes of contamination of food withpathogens, there are the additionalthreats of contamination with patho-genic microorganisms that are resistantto antibiotics, such as streptomycin andtetracyclines used in plants, as well as inhumans and animals; the presence in thefood of genetically engineered plantsthat contain genes for chemicals toxic toinsects, such as the Bacillus thuringien-sis toxin; genes for antibiotics againstother human pathogens; genes for acti-vating defensive mechanisms of plants,

ASPECTS OF APPLIED PLANT PATHOLOGY 59

often through the production of proteinsand phenolic compounds that make theplants resistant to insects, diseases, andto herbicides; genes for edible or other-wise delivered human vaccines and anti-bodies (plantibodies) against humanpathogens; genes for unrelated proteinsthat may be allergenic in some individu-als; and even genes for producing plastic.There is fear in some segments of thepopulation, especially in developedcountries, that although some of thesegenes are introduced into inedible plantssuch as tobacco, plants with such geneswill intentionally or accidentally findtheir way into foods and feed and willaffect adversely the health of animals

and humans. Many large produce dis-tributors or retailing companies andmanufacturers of food products simplyrefuse to buy any produce that comesfrom genetically modified organisms(GMOs), plants, or animals. Molecular-based diagnostic tests have also beendeveloped that detect introduced genesthat may not have been declared as beingpresent.

Since the horrendous terrorist attackin New York and Washington, DC, inSeptember of 2001 and the subsequentlydeclared war against terrorists whereverthey exist, there is an added fear ofhaving food contaminated intentionallyby terrorists. Contamination could be

carried out with human pathogenicmicroorganisms, such as those men-tioned earlier or with others, e.g., the bacterium causing the disease an-thrax, or with toxic substances. Conta-mination of produce can be done whilethe latter is still in the field, in transit, orin grocery stores. There is also fear ofhaving the drinking water or the waterused for irrigation of fruits and vegeta-bles contaminated intentionally by ter-rorists with pathogenic microorganismsor with toxic substances that will thenfind their way to humans via the food distribution system. This subject is dis-cussed further in the following section.

BOX 14 Bioterrorism, agroterrorism, biological warfare, etc. who, what, why?

Bioterrorism is loosely defined here asthe use, or threat of use, of biologicalagents, mainly pathogenic microorgan-isms that could infect people and causedisease and, thereby, instil fear andterror in all of the populace. Bioterror-ism may differ from biological warfarein that the latter is usually directedagainst enemy armies and its purpose isto incapacitate or kill enemy soldiers,whereas in bioterrorism the purpose is tofrighten and terrorize civilian popula-tions, although casualties in largenumbers may or may not occur. Themost vivid example of bioterrorismoccurred in the fall of 2001 whenpersons in various positions in politicsand the television news media in NewYork and Washington received lettersthrough the mail containing spores ofthe bacterium Bacillus anthracis, thecause of the severe and often deadlyanthrax disease. It became apparent atthe time that the perpetrators of theanthrax bioterrorism, or others, couldeasily expand to other forms of bioter-rorism by either contaminating agricul-tural products such as vegetables, milk,or meat on the farm or in the store withmicroorganisms pathogenic to humans,which would scare buyers away from

such products (agroterrorism), or byspreading selected plant pathogenicmicroorganisms on certain crops, e.g.,cereals, potatoes, and corn, which theycould infect and destroy to variousextents, thereby causing devastatinglosses that would further increase thefear of the people.

Biological warfare has been talkedabout for several decades and many ofthe larger countries have been producingand stockpiling pathogenic microorgan-isms, such as the anthrax bacterium, forpotential use against the army of anenemy country with which they might goto war. At the same time, however,several countries have been experiment-ing with and stockpiling microorganismsthat can infect and destroy importantstaple food crops for certain countries,e.g., rice, potatoes, wheat, or beans,which could affect the availability offood and thereby survival of the people,or at least, their will to fight and prolongthe war. This type of agricultural bio-logical warfare has revolved aroundimportant pathogens of such crops, e.g.,Magnaporthe grisea, the fungus causingthe blast disease of rice; Phytophthorainfestans, the oomycete causing the lateblight of potato; and Puccinia graminis,

the fungus causing the rust diseases ofwheat and other small grains.

As the specialization of crops in eacharea increases and as our knowledge ofdiseases of such crops increases, itbecomes evident that such areas or coun-tries become extremely vulnerable toagroterrorism or agrosabotage. Thishappens even if, or especially if, theygrow relatively small areas of such spe-cialty crops, e.g., bananas, citrus, coffee,and cacao, which are the main exportcrop and the main source of foreign cur-rency for these countries. For each areaproducing such a crop there arepathogens of the crop elsewhere that, ifintroduced, could destroy the crop forthe year to come and, possibly, forever.The pathogens that would be used onsuch clonal, genetically uniform, peren-nial crops are likely to be insect-vectoredbacteria, phytoplasmas, or viruses. Suchpathogens can be introduced into a fieldas a few bacteria- or virus-carryinginsect vectors that would feed on andinfect some of the plants and then, in thesame or in subsequent years, multiplyand spread the pathogen they carry tomore plants over a continually expand-ing area.

60 1. INTRODUCTION

WORLDWIDE DEVELOPMENT OF PLANTPATHOLOGY AS A PROFESSION

As mentioned earlier, plant pathology had its origins inplant pathological observations and studies made bybotanists, naturalists, and physicians in Europe in themid- to late 1800s. Soon after, plant pathological activ-ity shifted primarily to the United States, where it hasremained at a high level to date.

The students of the first, self-made, plant pathologistsbegan to be hired as plant pathologists by state agricul-tural experiment stations, by the federal Department ofAgriculture, and by universities at which they taughtcourses in plant pathology. In 1891, the plant patholo-gists in the Netherlands formed the Netherlands Societyof Plant Pathology and began publishing the Nether-lands Journal of Plant Pathology in 1895. In 1908, theplant pathologists in the United States organized into the American Phytopathological Society, and they toodecided to publish a journal of plant pathology in whichthey could present the results of their own research andcould read about the work of their colleagues. Thejournal, named Phytopathology, began to be publishedin 1911 as an international journal of plant pathology.The Phytopathological Society of Japan was founded in1916, and its journal began to be published in 1918. Insubsequent decades, plant pathologists formed associa-tions and began publishing plant pathological journalsin several other countries, e.g., Canada (1930) and India(1947). In the second half of the 20th century, plantpathologists in nearly 50 more countries organized intoprofessional associations; some of them, as in Brazil,published their own national journals, whereas othersformed multinational unions, e.g., the Latin AmericanPhytopathological Association, or published a regionaljournal such as Phytopathologia Mediterranea. In 1968,an International Society of Plant Pathology was formedand it held the first International Congress of PlantPathology in London that same year. By the end of the20th century most or all countries have one or moreplant pathologists, although in many developing coun-tries that person is an administrator of some kind or aprofessor at a university. Nevertheless, in many parts ofthe world, plant pathology is generally unknown orrarely practiced, and losses from plant diseases in devel-oping countries are still great.

International Centers for Agricultural Research

In the mid-1940s, the Rockefeller Foundation, in coop-eration with the Mexican government, established a

program in Mexico for interdisciplinary research onbasic food crops such as wheat, corn, potatoes, andbeans. That program was so successful in improvingcrops and in training personnel in the technologies thatsimilar Rockefeller Foundation programs were estab-lished in Colombia, Chile, and India. It soon becameapparent, however, that it would not be possible to havesuch programs in every developing country; rather, itwould be preferable to have a few international centersconcentrating on one or a few basic crops. So, with thecooperation of the local governments and funding fromthe Rockefeller and the Ford foundations, the Interna-tional Rice Research Institute (IRRI) was established inthe Philippines in 1960, the International Maize andWheat Improvement Center (CIMMYT) in Mexico in1966, the International Institute of Tropical Agriculture(IITA) in Nigeria in 1968, and the International Centerof Tropical Agriculture (CIAT) in Colombia in 1969(Fig. 1-41).

The success of these centers suggested the need foradditional ones. As the finances required to operate theearlier and the new centers were beyond the means ofthe Ford and the Rockefeller foundations, they, in col-laboration with the World Bank, set up a consortium ofpotential donors interested in financing internationalagricultural research. The consortium, known as theConsultative Group on International AgriculturalResearch (CGIAR), consists of wealthy countries, devel-opment banks, and other foundations and agencies. TheCGIAR receives help in determining research prioritiesfrom a technical advisory committee, which consists of13 scientists and economists. Additional centers estab-lished by the consultative group include the Interna-tional Crops Research Institute for the Semi-AridTropics (ICRISAT) in India in 1972 and the Interna-tional Potato Center (CIP) in Peru, also in 1972. A similarly operating center but not funded by the con-sultative group, namely the Asian Vegetable Researchand Development Center (AVRDC) in Taiwan, was alsoestablished in 1972. More recent centers include theInternational Center for Agricultural Research in theDry Areas (ICARDA) in Syria, the West Africa RiceDevelopment Association (WARDA) in Gold Coast, and some others (Fig. 1-41): IFPRI, International FoodPolicy Research Institute; ISNAR, International Servicefor National Agricultural Research; IPGRI, Interna-tional Plant Genetic Resources Institute; ILRI, Inter-national Livestock Research Institute; ICRAF,International Center for Research in Agroforestry; IIMI,International Irrigation Management Institute; CIFOR,Center for International Forestry Research; andICLARM, International Center for Living AquaticResources Management.

WORLDWIDE DEVELOPMENT OF PLANT PATHOLOGY AS A PROFESSION 61

Each of the aforementioned centers studying plantsincludes several plant pathologists working on diseasesof the specific crop(s) studied by the center. The contri-butions of the resident plant pathologists to the study ofthese diseases and to the development of disease-resistant cultivars and other controls against the diseasesof these crops have been truly great. These pathologistshave also helped train many other scientists not only ofthe host country, but from many other developing coun-tries attempting to grow these crops, have taught plantpathology courses in universities with which their centeris affiliated, and have generally helped to significantlyreduce losses of crops caused by plant diseases.

The need for plant pathology has always been par-ticularly great in tropical countries primarily because thetropical climate (hot and usually humid) favors the sur-vival and multiplication of pathogens throughout theyear, as well as the prolonged or continuous presence ofprimary and alternate hosts and large numbers of activevectors such as insects. Tropical climates also favor multiple and continuous infections by pathogens, whichoften lead to devastating epidemics. These problems in tropical countries are further compounded by loweducational levels and lack of funds for carrying outeffective plant disease control programs. Moreover,

tremendous losses from disease occur in the tropics inall types of produce after harvest because many har-vested products are already infected or contaminatedwhile still in the field and also because harvested prod-ucts often rot in storage or transit due to lack of ap-propriate decontamination and lack of any kind ofrefrigeration. It is not surprising, therefore, that so manyof the international centers for agricultural researchhave been established in the tropics, nor that their con-tributions have had a big and immediate impact onreducing losses from disease. Much more, however,remains to be done.

Trends in Teaching and Training in Plant Pathology

The first course in plant pathology was offered atHarvard University by M. A. Farlow in 1875. In theearly 1900s, departments of plant pathology began tobe established at some of the larger universities, often asdepartments of botany and plant pathology. The earlycourses were, by necessity, primarily descriptive of thediseases of various types of crops (vegetables, fruit trees,field crops), in addition to providing information on

IFPRI

CIMMYT

CIAT

CIP

WARDA

ISNAR

IPGRI

ICARDA

ICRISAT

IIMI

CIFOR

AVRDC

IRRI

ICLARM

ICRAFILRC

FIGURE 1-41 The global agricultural research system.

62 1. INTRODUCTION

the development of some of the pathogens and diseasesand on possible control measures. General textbooks inplant pathology appeared in several languages. In theUnited States the main textbooks were those by Duggar(1906), Stevens and Hall (1921), Heald (1926, 1943),and Walker (1950). In the meantime, specialized bookswere published on plant pathogenic fungi and, later on,bacteria, viruses, and nematodes and the diseases theycause, as well as on all types of diseases of groups ofcrops, such as vegetables, field crops, and fruit crops.Starting in the 1960s, more specialized books on thephysiology, biochemistry, epidemiology, and genetics ofplant diseases were published.

Students training to become plant pathologists tookas many relevant courses as were available at their uni-versity, but they learned most of their trade by watch-ing and working together with their mentor–professorplant pathologist and by themselves, under some super-vision, doing research on a specific plant disease orpathogen. Such studies, when successful, eventuallyearned them a doctor of philosophy (Ph.D.) degree inplant pathology, which indicates that they have theability, knowledge, and training to do research, i.e., tosolve scientific, and possibly practical, problems in plantpathology. This type of training continues to date exceptthat, because of the tremendous increase in the amountof knowledge in plant pathology, students specialize agreat deal more in what they learn and do. This has beenparticularly evident in the years after 1985 during whichmolecular plant pathology has attracted many of thestudents working toward their Ph.D. in plant pathology.Most of the holders of a Ph.D. in plant pathology findjobs as professors in colleges or universities, or asresearchers in universities, government, or industry.Some develop their own business as private practition-ers or consultants to growers. A few, usually one or twoper state, work as extension plant pathologists in stateland grant universities and experiment stations, wherethey are responsible for transferring plant pathologyinformation from plant pathology researchers togrowers and county agents, visiting crop fields and iden-tifying diseases, identifying diseases in plant samplessent in by growers, and developing and disseminatingdisease control recommendations.

Similar but less extensive and intensive course workand research training can lead to a master of science(M.S.) degree in plant pathology. This enables the holderto work for the same agencies as the Ph.D. holders butwith reduced responsibility and benefits. Several depart-ments of plant pathology also offer bachelor of science(B.S.) degrees in plant pathology, which serve either asintermediate steps for advanced degrees or enable theholders to work in university, government, and industrylaboratories, for various types of agribusinesses as

chemical, seed, etc., company representatives, or asprivate practitioners.

Plant pathology, unlike its sister sciences of medicineand veterinary medicine, deals with plant diseasescaused by pathogens and, to some extent, by environ-mental factors. It does not have teaching and trainingprograms that will produce practitioners similar to thegeneral practitioner physicians and veterinarians, i.e.,professionals capable of identifying all types of causesof disease and injury to plants and of making recom-mendations to control or manage these. Such practi-tioners (plant doctors) would also be trained inidentifying and making control recommendations forinsects, weeds, damage by animal wildlife, and the nutri-tional and other environmental conditions that affectplant health. Development of a program leading to aprofessional doctor of plant medicine or doctor of plant health degree, similar to the M.D. (doctor ofmedicine) and D.V.M. (doctor of veterinary medi-cine) degrees, had been discussed since the late 1980sand was offered for the first time by the College of Agriculture and Life Sciences of the University of Floridain the year 2000.

Plant Disease Clinics

For many years, most states operated a plant diseaseclinic through their department of plant pathology.Growers, county extension agents, and home ownerswould send diseased plants, soil from areas with dis-eased plants, and sometimes insects to the plant diseaseclinic and the pathogen or insect would be identified and control measures would be recommended, all freeof charge. At first, the plant disease clinics were set uprather informally and were supervised by the extensionplant pathologist, with most of the diagnoses made byadvanced plant pathology graduate students assisted sig-nificantly by more junior graduate students. Early plantdisease clinics were equipped primarily with surfacesterilants, dissecting scopes, microscopes, culture dishesand test tubes, and nutrient media for culturing fungiand bacteria. Later, much of the day-to-day operationof plant disease clinics was turned over to M.S. or Ph.D.plant pathologists hired specifically for that purpose. At the same time, nematode isolation from roots or soiland plant nematode identification became integral func-tions of the plant disease clinics. Virus disease identifi-cation was still made by host symptomatology alone,but some host range tests for diagnostic purposes werecarried out.

Since the 1970s, every state has at least one plantdisease clinic and some have several; e.g., Florida hasfour plant disease clinics. In addition to state-funded

WORLDWIDE DEVELOPMENT OF PLANT PATHOLOGY AS A PROFESSION 63

plant disease clinics, in some states there may be one ormore privately run plant disease clinics and, in a fewstates, a plant disease clinic may also be operated by thestate department of agriculture. Today’s plant diseaseclinics often have one scientist with an advanced degreeand one or more laboratory assistants; they are alsoequipped for viral disease diagnosis through host rangetests, serological tests, cell inclusion identification, electron microscopy of plant sap, and dot-blot assays of radioactive or color-producing DNA probes. Plantdisease clinics also have modern computers with data-bases and expert systems for disease and pathogen iden-tification, computerized distance diagnostic systems thattransmit plant disease images directly from the field toan expert diagnostician, CD videodisc capabilities, ande-mail for transmitting the results of diagnosis and therecommendations for control to their clientele. Also,however, due to increased costs for these tests and serv-ices, plant disease clinics in many states have now estab-lished fees that must be paid by all commercial users andhome owners submitting samples of diseased plants fordiagnosis.

The Practice and Practitioners of Plant Pathology

The science of plant pathology has been and continuesto be developed primarily by highly specialized pro-fessors or researchers who have advanced, usually doctorate, degrees. For many discoveries, considerablecontributions are made by graduate students who arethemselves working toward M.S. or Ph.D. degrees atdepartments of plant pathology, botany, or biology andat agricultural experiment stations.

The practice of plant pathology, however, is carriedout at a much lower scientific and professional level.Medicine and veterinary medicine also have Ph.D.-holding scientists who do research. These scientistsadvance the respective sciences at various universitiesand research centers. In addition, however, both medi-cine and veterinary medicine have numerous highlytrained practicing physicians (doctors of medicine) andveterinarians (doctors of veterinary medicine) who arethe practitioners of each science. They diagnose the ail-ments and prescribe treatments for humans and animals,both individuals and populations. In contrast, plantpathology has few well-trained practicing plant pathologists.

In general, most states have one or two extensionplant pathologists. Their duty is to (a) transfer the infor-mation developed by the researchers in the state andelsewhere to county extension personnel and to growersand (b) demonstrate its effectiveness to those who needit, i.e., the growers. The same extension plant patholo-

gists are expected to be able to diagnose all diseases onall types of plants, regardless of their cause, and to rec-ommend measures for their control. The extension plantpathologists also train the county extension agents, whousually have little formal education or training in plantpathology, so that they can diagnose and offer recom-mendations for the control of plant diseases common intheir county. Many states have a plant disease clinic towhich samples of diseased plants or plant parts are sentby growers, home owners, and county agents for diag-nosis and control recommendations. In some of the mostagriculturally oriented states, a few persons, whousually have varying levels of education and training inplant pathology (B.S., M.S., or Ph.D.), offer their serv-ices as private practitioners (plant doctors) to individualgrowers or groups of growers, or they operate their ownprivate plant disease clinics. Much of the time, however,growers receive information on plant diseases and rec-ommendations for plant disease control from salesmenof pesticides, seeds, or fertilizers, and from other pro-fessionals (agronomists, horticulturists, entomologists,etc.) who may have little or no education and trainingin plant pathology.

Under the present conditions, therefore, mostgrowers often receive rather limited, delayed, or inac-curate information on the kinds and development of dis-eases affecting their crops and, similarly, incomplete andsometimes inaccurate information about their control.As a result, plant diseases are often detected late and aresometimes misdiagnosed, and frequently the wrong pes-ticides or excessive dosages of pesticides are recom-mended and applied for their control. The amount ofcrop losses to plant diseases, therefore, and possiblycontamination of the environment with pesticides aswell, is often greater than need be.

Certification of Professional Plant Pathologists

When a professional such as a physician, veterinarian,lawyer, or engineer offers his or her services to individ-uals, the individuals expect the professional to haveappropriate education and training that meet or exceedcertain professional and ethical standards. At the sametime, the professional and the public also expect that no person who does not meet such a standard will beallowed to provide such services: the professionalsbecause they do not want such persons to compete forbusiness with them and the public because they want tobe certain that the person to whom they go for suchservices can actually provide them correctly. These two expectations are generally guaranteed through thelicensing programs operated by each state and country.

64 1. INTRODUCTION

Since the 1960s and 1970s, many states have requiredthe licensing of pest control advisers, pesticide applica-tors, etc. In addition, several professional societies, suchas the American Society of Agronomy, the Soil ScienceSociety of America, the Crop Science Society ofAmerica, and the Entomological Society of America,have established professional certification programs that resulted in certified agronomists, certified soil sci-entists, certified crop scientists, certified entomologists,and so on.

A proposal for establishing an American registry ofprofessional plant pathologists was submitted to theAmerican Phytopathological Society in 1980, but it wasnot approved until 1991. The following year, a certifiedprofessional plant pathologist program was developedthat set professional and ethical standards. A board ofsix plant pathologists, named by the American Phy-topathological Society, was authorized to review andcompare the credentials (course work, experience, ref-

erences) of each applicant with the standard and todetermine their eligibility to become certified profes-sional plant pathologists. Because there were alreadymany practicing plant pathologists (private consultants)when the certification program came into being, thestandards for certification were set so that it wouldinclude most of them. The standards include a B.S.degree in plant pathology and 5 years of professionalexperience, a M.S. in plant pathology and 3 years ofprofessional experience; or a Ph.D. in plant pathologyand 1 year of professional experience. The board alsoset a curriculum that would enable new students tobecome certified professional plant pathologists. Inaddition, the board set standards for continual educa-tion and training so that certified professional plantpathologists can keep abreast of new information, tech-niques, conditions, regulations, and requirements in thearea of plant health management.

BOX 15 Plant pathology as a part of plant medicine: the doctor of plant medicine program

In the last two decades, considerableefforts have been made to broaden theconcepts of both plant health and plantprotection. The American Phytopatho-logical Society, realizing the need forsuch a broader concept, launched a newelectronic journal called “Plant HealthProgress,” which publishes articles on allfacets of plant health.

It has become apparent, however, thattrained professionals are needed who candeal with the whole health of the plantand give recommendations for its main-tenance or restoration. Such profession-als would be able to diagnose all causesof plant problems, be they pathogens(fungi, bacteria, viruses, nematodes, par-asitic algae and parasitic higher plants,protozoa, etc.), insects, mites, vertebrate(birds, field mice, deer) and invertebrate(snails, slugs) wildlife, weeds, soil condi-tions, weather extremes, pollutants, andso on, and to recommend strategies fortheir management or control. To developsuch a broad expertise in plant protec-tion, however, it is necessary that qualified graduates in a biological oragricultural science attend a 3- to 4-yearprofes-sional graduate degree program.The University of Florida’s College ofAgriculture and Life Sciences createdsuch a program in 1999 and accepted its

first graduate students in the fall semes-ter of 2000. The Doctor of Plant Medi-cine (DPM) program, as it is called, had14 students the first year, 15 the secondyear, and 10–14 students per year thereafter.

The degree is called Doctor of PlantMedicine rather than Doctor of PlantHealth because it parallels the other twodoctorates in the health professions,those of medicine (MD) and of veteri-nary medicine (DVM), in so manyaspects that its goals and functions areeasier to understand by this name. Inaddition, just like the MD and the DVM,the DPM is a professional, practitioner’sdegree, not a research degree as is thePh.D. None of these degrees (MD,DVM, DPM) are replacing the Ph.D.s intheir respective areas. Instead theyprovide a mechanism by which the infor-mation generated by the researcherPh.D.s is used for the correspondingclientele (humans, animals, plants), theailments of which are diagnosed andmanaged or controlled. Also, just likeMD and DVM students, DPM studentsdo several projects that involve mainlyapplied-type research and write appro-priate reports, but they do not doresearch on a single project and do notwrite a thesis or dissertation.

The DPM program accepts studentswho have graduated with a bachelor’s ora master’s degree, preferably, but notnecessarily, in a biological or agricul-tural discipline. Entering students mustmeet all criteria other graduate students(for Ph.D. or M.S. degrees) must meet.DPM students take 90 credits of gradu-ate courses in the appropriate academicdepartments, most courses with labora-tories, generally being the same coursestaken by the graduate students of eachdepartment or discipline. About 65 ofthese credits are in required courses, aminimum of 18 in plant science, includ-ing courses in crop production, soils andcrop nutrition, and weed science, 17 inentomology, 18 in plant pathology, 5 innematology, 2 in acarology, 2 in wildlifethat damage plants, 5 in plant pest man-agement, and courses in agribusinessmanagement, marketing, and agricul-tural law. The elective credits may beused by the student to specialize in acommodity area of his/her choice (e.g.,agronomic crops, horticultural crops,ornamental crops and/or turf, forestryand/or urban forestry, education coursesfor college teaching, etc.).

In addition to the 90 credits ofcourses, DPM students must also do 30credits of internships or practicums by

PLANT PATHOLOGY’S CONTRIBUTION TO CROPS AND SOCIETY 65

spending appropriate lengths of time(2–3 credits each) in the soil analysis lab-oratory, the plant disease clinic, the nem-atode assay laboratory, the insectidentification laboratory, and the weedidentification laboratory. The studentsmay also elect to do internships byworking side by side with the extensionweed scientist, horticulturist, plantpathologist, or entomologist, or theymay elect to do an internship at an agri-cultural experiment station, at an agri-chemical or seed company, or workingside by side with an experienced cropconsultant. The location of internshipsmay vary from local to international.The entire curriculum is expected,

although not required, to be completedwithin 3 or 4 years. Part-time studentsmay take considerably longer.

Upon completion of the program,DPM graduates receive the doctoratedegree and are fully educated andtrained plant doctors who can identifyjust about anything, living and nonliv-ing, that causes damage to plants andcan provide quick and correct re-commendations for their managementor control. Their education, training,expertise, and the doctorate degreequalify them for a variety of well-payingjobs within the United States and inter-nationally, including private practition-ers as crop consultants; working for

large farms or agribusinesses; workingfor the state or federal extension service(as county agents, IPM coordinators,pesticide information coordinators,etc.), for state or federal regulatory agen-cies [e.g., the Animal and Plant HealthInspection Service (APHIS), the PlantProtection and Quarantine (PPQ)Service, ship and airport inspectors,etc.); working for agrichemical, seed,and large food companies such as DelMonte and Campbell, teaching variousbiological courses at 2- and 4-year col-leges and universities; and working formid- to large size municipalities.

PLANT PATHOLOGY’S CONTRIBUTION TOCROPS AND SOCIETY

Some Historical and Present Examples of LossesCaused by Plant Diseases

Plant diseases affect the existence, adequate growth, andproductivity of all kinds of plants and thereby affect oneor more of the basic prerequisites for a healthy, safe lifefor humans. This happened since the time humans gaveup their dependence on wild game and fruits andbecame more stationary, domesticated, and began topractice agriculture more than 6000 years ago. Destruc-tion of food and feed crops by diseases has been an alltoo common occurrence in the past. It has resulted inmalnutrition, starvation, migration, and death of peopleand animals on numerous occasions, several of whichare well documented in history. Similar effects areobserved annually in developing agrarian societies inwhich families and nations are dependent for their sus-tenance on their own produce. In more developed soci-eties, losses from diseases in food and feed produceresult primarily in financial losses and higher prices. Itshould be kept in mind, however, that loss of anyamount of food or feed because of plant diseases meansthere is less available in the world economy. Consider-ing the chronically inadequate amounts and distributionof food available, rich people and rich countries will beable to acquire such foodstuffs from wherever they areavailable, whereas many poor people somewhere in theworld will be worse off because of these losses, and willgo hungry.

Some examples of plant diseases that have causedsevere losses in the past are shown in Tables 1-2 and 1-3.

Plant Diseases and World Crop Production

There are no dependable surveys of numbers of humansliving on the earth before the year 1900. It is estimated,however, that there were about 300 million people livingon the earth in the year a.d. 1, 310 million in a.d. 1000,400 million in a.d. 1500, and 1.3 billion in a.d. 1900.During the 20th century there has been a dramaticexplosion in the human population. Despite recentefforts to reduce the rate of population growth, thenumber of new humans added to the world populationeach year and the additional demands for food, energy,and other resources from our planet are frightening.Thus, the world population in 1993 was about 5.57billion, and, at the present rate of 1.7% annual growth,it was expected to be 6.2 billion by the year 2000, be7.1 billion by the year 2010, and be 8.5 billion by 2025.Currently, the world population increases by 1 billionevery 11 years (see Fig. 1-42).

Paradoxically, the developing countries, in whichfrom 50 to 80% of the population is engaged in agri-culture, have the lowest agricultural output, their peopleare living on a substandard diet, and they have thehighest population growth rates (2.64%). Because of thecurrent distribution of usable land and population, ofeducational and technical levels for food production,and of general world economics, it is estimated that eventoday some 2 billion people suffer from hunger, malnutrition, or both. To feed these people and the additional millions to come in the next few years, allpossible methods of increasing the world food supplyare currently being pursued, including (1) expansion ofcrop acreages, (2) improved methods of cultivation, (3) increased fertilization, (4) use of improved varieties

66 1. INTRODUCTION

of crops, (5) increased irrigation, and (6) improved cropprotection.

Crop Losses to Diseases, Insects, and Weeds

There is no doubt that the first five of the aforemen-tioned measures must provide the larger amounts of

food needed. Crop protection from pests and diseasescan only reduce the amount lost after the potential forincreased food production has been attained by properutilization of all means possible. Crop protection, ofcourse, has been important in the past and is importantnow. For example, it is estimated that in the UntiedStates alone, despite the control measures practiced,each year, crops worth $9.1 billion are lost to diseases,

TABLE 1-2Examples of Severe Losses Caused by Plant Diseases

Disease Location Comments

Fungal1. Cereal rusts Worldwide Frequent severe epidemics; huge annual losses2. Cereal smuts Worldwide Continuous, although lesser, losses on all grains3. Ergot of rye and wheat Worldwide Infrequent, poisonous to humans and animals4. Late blight of potato Cool, humid climates Annual epidemics, e.g., Irish famine (1845–1846)5. Brown spot of rice Asia Epidemics, e.g., the great Bengal famine (1943)6. Southern corn leaf blight U.S. Historical interest, epidemic 1970, $1 billion lost7. Powdery mildew of grapes Worldwide European epidemics (1840s–1850s)8. Downy mildew of grapes U.S., Europe European epidemic (1870s–1880s)9. Downy mildew of tobacco U.S., Europe European epidemic (1950s–1960s); epidemic in North America (1979)

10. Chestnut blight U.S. Destroyed almost all American chestnut trees (1904–1940)11. Dutch elm disease U.S., Europe Destroying American elm trees (1918 to present)12. Pine stem rusts Worldwide Causing severe losses in many areas13. Dwarf mistletoes Worldwide Serious losses in many areas14. Coffee rust Asia, South America Destroyed all coffee in southeast Asia (1870s–1880s) since 1970 present

in South and Central America15. Banana leaf spot or Sigatoka Worldwide Great annual losses

disease16. Rubber leaf blight South America Destroys rubber tree plantations17. Fusarium scab of wheat North America Severe losses in wet years

Viral18. Sugar cane mosaic Worldwide Great losses on sugar cane and corn19. Sugar beet yellows Worldwide Great losses every year20. Citrus tristeza (quick decline) Africa, Americas Millions of trees being killed21. Swollen shoot of cacao Africa Continuous heavy losses22. Plum pox or sharka Europe, North America Spreading severe epidemic on plums, peaches, apricots23. Barley yellow dwarf Worldwide Important on small grains worldwide24. Tomato yellow leaf curl Mediterranean countries, Severe losses of tomatoes, beans, etc.

Caribbean Basin, U.S.25. Tomato spotted wilt virus Worldwide On tomato, tobacco, peanuts, ornamentals, etc.

Bacterial26. Citrus canker Asia, Africa, Brazil, U.S. Caused eradication of millions of trees in Florida in 1910s and again

in the 1980s and 1990s27. Fire blight of pome fruits North America, Europe Kills numerous trees annually28. Soft rot of vegetables Worldwide Huge losses of fleshy vegetables

Phytoplasmal29. Peach yellows Eastern U.S., Russia Historical, 10 million peach trees killed30. Pear decline Pacific coast states and Canada Millions of pear trees killed

(1960s), Europe

Nematode diseases31. Root knot Worldwide Continuous losses on vegetables and most other plants32. Sugar beet cyst nematode Northern Europe, Western U.S. Continuous severe annual losses on sugar beets33. Soybean cyst nematode Asia, North and South America Continuous serious losses on soybean


$7.7 billion to insects, and $6.2 billion to weeds. Cropprotection, however, becomes even more important inan intensive agriculture, where increased fertilization,genetically uniform high-yielding varieties, increasedirrigation, and other methods are used. Crop losses todiseases and pests not only affect national and worldfood supplies and economies but also affect individualfarmers even more, whether they grow the crop fordirect consumption or for sale. Because operatingexpenditures for the production of the crop remain thesame in years of low or high disease incidence, harvestslost to disease and pests lower the net return directly.

The amount of each crop lost to pests varies with thecrop (e.g., 23.4% for fruits, 34.5% for cereals, 55.0%for sugar cane). Crop loss varies with the type of climate(warm, humid, rainy, dry, etc.), the particular year, avail-

ability of pesticides, availability of trained personnel,and educational level of growers. Also, the importanceof each kind of pest (diseases, insects, weeds) varies withthe crop. Generally, diseases, which are more difficult todetect, identify, and control on time, cause losses ofabout 14% of the crop; insects, if left unchecked, wouldcause tremendous losses but because they can bedetected, identified, and controlled on time with effec-tive insecticides cause losses of about 10% of the crop;and weeds, which still are poorly controlled in much ofthe world because of unavailability of herbicides due tocost, cause losses of about 12% of the crop. The totalcrop loss from diseases and pests is estimated at about36% or one-third of the potential production of theworld. To these losses should be added 6–12% posthar-vest losses to pests, which brings the total (preharvest

TABLE 1-3Additional Diseases Likely to Cause Severe Losses in the Future

Disease Comments

Fungal1. Late blight of potato and tomato New mating type of fungus spreading worldwide2. Downy mildew of corn and sorghum Just spreading beyond southeast Asia3. Karnal bunt of wheat Destructive in Pakistan, India, Nepal; since the 1980s introduced into Mexico and in the 1990s into U.S.4. Soybean rust Spreading from southeast Asia and from Russia; already in Hawaii, Puerto Rico, and South America5. Monilia pod rot of cacao Very destructive in South America; spreading elsewhere6. Chrysanthemum white rust Important in Europe, Asia, and recently in California7. Sugar cane rust Destructive in the Americas and elsewhere8. Citrus black spot Severe in Central and South America9. Sweet orange scab Severe in Australia

Viral10. African cassava mosaic Destructive in Africa; threatening Asia and the Americas11. Streak disease of maize (corn) Spread throughout Africa on sugar cane, corn, wheat, etc.12. Hoja blanca (white tip) of rice Destructive in the Americas so far13. Bunchy top of banana Destructive in Asia, Australia, Egypt, Pacific islands14. Rice tungro disease Destructive in southeast Asia15. Bean golden mosaic Caribbean basin, Central America, Florida16. Tomato yellow leaf curl. East Mediterranean, Caribbean, the Americas17. Plum pox Destructive in Europe, spreading into U.S.

Bacterial18. Bacterial leaf blight of rice Destructive in Japan and India; spreading19. Bacterial wilt of banana Destructive in the Americas; spreading elsewhere20. Pierce’s disease of grape Deadly in southeast U.S.; spreading into California21. Citrus variegation chlorosis Destructive in Brazil; spreading22. Citrus greening disease Severe in Asia; spreading

Phytoplasmal23. Lethal yellowing of coconut palms Destructive in Central America; spreading into U.S.

Viroid24. Cadang-cadang disease of coconut Killed more than 15 million trees in the Philippines to date

Nematode25. Burrowing nematode Severe on banana in many areas and citrus in Florida26. Red ring of palms Severe in Central America and the Caribbean27. Pinewood nematode Widespread and becoming severe in North America

68 1. INTRODUCTION

and postharvest) food losses to pests in the United Statesto about 40% and for the entire world to about 45%of all food crops. These losses occur, of course, despiteall types of pest controls used. This is indeed a huge lossof needed food. It is apparent that losses are muchgreater in developing areas than they are in more devel-oped ones. Another point that can be made is thatinsects cause much greater losses than diseases in devel-oping countries, especially in Asia, because insects arecontrolled much more easily in developed countries thanin developing ones, whereas losses caused by diseasesseem to be as great in developed countries as they arein developing countries.

Crop losses caused by diseases, insects, and weedsbecome particularly striking and alarming when oneconsiders their distribution among countries of varyingdegrees of development. In developed areas (Europe,North America, Australia, New Zealand, Japan, Israel,and South Africa), in which only 8.8% of the popula-tion is engaged in agriculture, the estimated losses andpercentages of losses are considerably lower than thosein developing countries, i.e., the rest of the world, inwhich 56.8% of the population is engaged in agricul-ture. The situation becomes particularly painful if one

considers the fact that developing countries, which havemuch greater populations than developed countries,produce relatively less food and fiber and suffer muchgreater losses to plant diseases and to other pests. Takinginto account the kinds of crops grown in temperate cli-mates, where most developed countries are, and in thetropics, where developing countries are located, the totalpercentage losses differ considerably with the continent,as shown in Table 1-4. What is disheartening is that themore recent estimates by Oerke et al. (1994) indicatethat the proportion of crop produce lost to diseases,insects, and weeds has actually increased in all conti-nents (Table 1-4), despite presumably better and morewidely used control materials and methods.

It is estimated that the total annual production for allagricultural crops worldwide is about $1500 billion(U.S. dollars, 2002). Of this, about $550 billion worthof produce is lost annually to diseases, insects, andweeds. An additional loss of about $455 billion wouldoccur annually, but is averted by the use of various cropprotection practices. Approximately $38 billion is spentannually for pesticides alone (fungicides, insecticides,herbicides), primarily in western Europe and in NorthAmerica.

Entire world

Developing countries

9,000

8,000

7,000

6,000

5,000

Po

pu

lati

on

(mill

ion

s)

4,000

3,000

2,000

1,000

1940

2,141

1,490

651

1,023 1,120 1,195 1,266 1,374 1,440 1,525

2,253

2,831

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6,975

3,276

3,951

4,400

4,854

5,294

6,228

7,100

8,500

1950 1960 1970 1980 1990 2000 2010 2020 20300

Developed countries

FIGURE 1-42 Real and projected population changes from 1940 to 2000 and to the year 2025. The rates ofpopulation growth were estimated for the years 1975 to 2000 and, for this graph, were assumed unchanged tothe year 2025.


Pesticides and Plant Diseases

The weed killers used increasingly in cultivated fieldsmay cause injury to cultivated crop plants directly, butthey also influence several soil pathogens and soilmicroorganisms antagonistic to pathogens. Other chem-icals, such as fertilizers, insecticides, and fungicides,alter the types of microorganisms that survive and thrivein the soil, which sometimes leads to a reduction in thenumber of useful predators and antagonistic microor-ganisms of pathogens or their vectors. The use of fungi-cides and other pesticides specific against a particularpathogen often leads to increased populations anddisease severity caused by other pathogens not affectedby the specific pesticide. This occurs even with somerather broad-spectrum systemic fungicides that controlmost but not all pathogens, e.g., benomyl. Where suchfungicides are used regularly and widely, some fungi,such as Pythium, that are not affected by them, maybecome more important as pathogens than when othermore general fungicides are used.

The use of pesticides to control plant diseases andother pests had been, for many years since themid–1950s, increasing steadily at an annual rate ofabout 14% (Fig. 1-43A). By 1999, nearly 2.6 billionkilograms (5.7 billion lbs) of active ingredients of pesti-cides were used per year worldwide at an annual cost of nearly $36 billion (Figs. 1-43B and 1-43C). In theUnited States alone, more than 550 million kg (1244million lbs) of pesticides worth $11.2 billion (Figs. 1-43B–1-43E) were used in 1999. The relative amounts ofactive ingredient of herbicides, insecticides, fungicides,

and other pesticides used in the United States and theworld in 1998 or 1999 are shown in Figs. 1-43B–1-43E.Up to 1995, about 35% of all pesticides were appliedin the United States and Canada, 45% in Europe, andthe remaining 20% in the rest of the world. In the lastseveral years, the use of pesticides has begun to declinein the United States and Europe, but as more countriesbecome developed and can afford to buy pesticides, theuse of pesticides in developing countries continues toincrease sharply.

A large industry of pesticide research, production,and marketing has developed in the United States andsome of the other countries. There are also hundreds ofthousands of people who apply pesticides on crops asneeded. The amount of pesticides applied on crops and the number of pesticide applicators varies consid-erably from region to region. This depends on the sizeof agriculture in the region, the climate of the region,and the kinds of crops grown in each. The Environ-mental Protection Agency has grouped the United Statesinto 10 agricultural regions (Fig. 1-44A) and has esti-mated that the number of private pesticide applicators(i.e., individual farmers) and of commercial pesticideapplicators varies from about 10,000 in some regions(No.1, New England states) to more than 300,000 inother regions (No.4, southeastern United States) (Fig. 1-44B).

There is little doubt that pesticide use has increasedthe yields of crops in most cases in which they have beenapplied. The cost of production, distribution, and appli-cation of pesticides is, of course, another form of eco-nomic loss caused by plant diseases and pests (Table1-4). Furthermore, such huge amounts of poisonoussubstances damage the environment and food as theyare spread over the crop plants several times each year.There are also the issues of worker protection fromexposure to pesticides and poisonings of workers andconsumers from pesticides.

Public awareness of the direct, indirect, and cumula-tive effects of pesticides on organisms other than thepests they are intended to control has led to increasedemphasis on the protection of the environment. As aresult, many pesticides have been abandoned or their usehas been restricted, and their functions have been takenover by other less effective or more specific pesticides orby more costly or less efficient methods of control. Theeffort to control diseases and other pests by biologicaland cultural methods is still growing while at the sametime more restrictions are being imposed on the testing,licensing, and application of pesticides. The pesticideproducers must provide more detailed data on the effec-tiveness, toxicity, and persistence of each pesticide, andthe application of each pesticide must be licensed foreach crop on which it is going to be applied. Further-

TABLE 1-4Percentage of All Produce (1967 Estimate) and of Eight MajorCrops (1994 Estimate) Lost to Diseases, Insects, and Weeds by

Continent or Regiona

Produce lost to diseases, insects, and weeds (%)

Continent or region 1967 estimateb 1994 Estimatec

Europe 25 28.2Oceania 28 36.2North and Central America 29 31.2Russia and China 30 40.9South America 33 41.3Africa 42 48.9Asia 43 47.1

aReprinted from Oerke et al. (1994). The crops included are rice,wheat, barley, maize, potatoes, soybeans, cotton, and coffee.

bFrom H. H. Cramer (1967).cThe average worldwide loss to diseases, insects, and weeds was

estimated at 42.1%.

70 1. INTRODUCTION

A

30Herbicides

25

20

15

10

5

0

1960

Bill

ion

s o

f U.S

. Do

llars

Years

1970 1980 1990 1999

35

Insecticides

Fungicides

Others

Mill

ion

s o

f Po

un

ds

Mill

ion

s o

f Do

llars

Mill

ion

s o

f Po

un

ds

of A

I

Mill

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s o

f Do

llars

6000

5000

4000

3000

2000

1000

0

$40,000

$35,000

$30,000

$25,000

$20,000

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$0

Pesticide TypePesticide Type

Year

Year

1,600

1,400

1,200

1,000

800

400

200

0

600

1980 1982 1984 1986 1988 1990 1992 1994 1996 1998

Herbicides Insecticides Fungicides Other Total Herbicides Insecticides Fungicides Other Total

$12,000

$10,000

$8,000

$6,000

$4,000

$2,000

$01980 1982 1984 1986 1988 1990 1992 1994 1996 1998

B

D

E

C

World Market

U.S. Market

World Market

U.S. Market

Herbicides

Insecticides

Fungicides

Other

Herbicides

Insecticides

Fungicides and Others

Other Conventional

FIGURE 1-43 (A) Estimated worldwide annual sales of pesticides through 1999 in billions of dollars. Compari-son of amounts of pesticides (in millions of pounds of active ingredient) used annually in the world and the UnitedStates (B) and of cost of pesticides (in millions of dollars) worldwide and the United States (C) at user level and bytype of pesticide (B and C, 1999 estimates). (D) Annual usage in the United States of the various types of pesticides(in millions of pounds of active ingredient) from 1980 through 1999. (E) Cost of pesticides (in millions of dollars)spent annually in the United States from 1980 through 1999. Source: U.S. Environmental Protection Agency.

BASIC PROCEDURES IN THE DIAGNOSIS OF PLANT DISEASES 71

more, in some countries, each prospective commercialapplicator of pesticides must pass an examination andbe licensed to apply pesticides on crop plants. In somestates, growers must clear with and get permission fromstate pest control advisors for the purchase and use ofcertain pesticides (prescription agriculture).

The desirability of using fewer and safer pesticides,however, is counteracted by the increasing demand ofconsumers over the last several decades for high-qualityproduce, especially fruits and vegetables free of any kindof blemishes caused by diseases or insects. A change inthe attitude of consumers to demand less extravagantaesthetic quality of produce could reduce considerably

the use of pesticides and the waste of perfectly whole-some foodstuffs, but such change in attitude may notoccur for some time yet.

BASIC PROCEDURES IN THE DIAGNOSIS OFPLANT DISEASES

Pathogen or Environment

To diagnose a plant disease it is necessary to first deter-mine whether the disease is caused by a pathogen or anenvironmental factor. In some cases, in which typical

WA

ORID

MT

NV

AK

CAUT

AZ

CO

MN

WIMI

IL INOH

VT

NYMANH

PA

WV VAKY

TNOK

NE

KS

IA

MO

AR

LA

NM

MS AL GA

FL

NC

SC

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ND

SD RI

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DEMDDC

CT

1

2

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7

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A

B

FIGURE 1-44 (A) Groups of states according to size and type of agriculture, and climate. (B) Numbers of privateand commercial pesticide applicators in each region. Source: U.S. Environmental Protection Agency.

72 1. INTRODUCTION

symptoms of a disease or signs of the pathogen arepresent, it is fairly easy for an experienced person todetermine not only whether the disease is caused by apathogen or an environmental factor, but by which one.Frequently, comparing the symptoms with those givenin books that list the known diseases and their causesfor specific plant hosts or in books like those of the com-pendia series of the American Phytopathological Societyhelps narrow the number of likely causes and often helpsidentify the cause of the disease. In most cases, however,a detailed examination of the symptoms and an inquiryinto characteristics beyond the obvious symptoms arenecessary for a correct diagnosis.

Infectious Diseases

In diseases caused by pathogens (fungi, bacteria, para-sitic higher plants, nematodes, viruses, mollicutes, andprotozoa), a few or large numbers of these pathogensmay be present on the surface of the plants (some fungi,bacteria, parasitic higher plants, and nematodes) orinside the plants (most pathogens). The presence of suchpathogens on or in a plant indicates that they are prob-ably the cause of the disease. Someone with experiencecan detect and identify pathogens, in some cases withthe naked eye or with a magnifying lens (some fungi, all parasitic higher plants, some nematodes). More frequently, identification can be accomplished only bymicroscopic examination (fungi, bacteria, and nema-todes) (see Fig. 1-3). If no such pathogens are presenton the surface of a diseased plant, then one must lookfor additional symptoms and, especially, for pathogensinside the diseased plant. Such pathogens are usually at the margins of the affected tissues, at the vasculartissues, at the base of the plant, and on or in its roots.

Diseases Caused by Parasitic Higher Plants

The presence of a parasitic higher plant (e.g., dodder,mistletoe, witchweed, or broomrape) growing on a plantis sufficient for diagnosis of the disease.

Diseases Caused by Nematodes

If a plant parasitic nematode is present on, in, or in therhizosphere of a plant showing certain kinds of symp-toms, the nematode may be the pathogen that causedthe disease or at least was involved in the production ofthe disease. If the nematode can be identified as belong-ing to a species or genus known to cause such a disease,then the diagnosis of the disease can be made with adegree of certainty.

Diseases Caused by Fungi and Bacteria

When fungal mycelia and spores, or bacteria, are presenton the affected area of a diseased plant, two possibili-ties must be considered: (1) the fungus or bacterium maybe the actual cause of the disease or (2) the fungus orbacterium may be one of the many saprophytic fungi orbacteria that can grow on dead plant tissue once thelatter has been killed by some other cause, perhaps byeven other fungi or bacteria.

Fungi

To determine whether a fungus found on or in a diseased plant is a pathogen or a saprophyte, one first studies under a microscope the morphology of itsmycelium, fruiting structures, and spores. The funguscan then be identified and checked in an appropriatebook of mycology or plant pathology to see whether ithas been reported to be pathogenic, especially on theplant on which it was found. If the symptoms of theplant correspond to those listed in the book as causedby that particular fungus, then the diagnosis of thedisease is, in most cases, considered complete. If no suchfungus is known to cause a disease on plants, especiallyone with symptoms similar to the ones under study, thenthe fungus found should be considered a saprophyte or,possibly, a previously unreported plant pathogen, andthe search for the proof of the cause of the disease mustcontinue. In many cases, neither fruiting structures norspores are initially present on diseased plant tissue, andtherefore no identification of the fungus is possible. For some fungi, special nutrient media are available for selective isolation, identification, or promotion ofsporulation. Others need to be incubated under certaintemperature, aeration, or light conditions to producespores. With most fungi, however, fruiting structuresand spores are produced in the diseased tissue if thetissue is placed in a glass or plastic “moisture chamber,”i.e., a container to which wet paper towels are added toincrease the humidity in the air of the container.

Bacteria and Mollicutes

Diagnosis of a bacterial disease and identification ofthe causal bacterium is based primarily on the symptomsof the disease, the constant presence of large numbersof bacteria in the affected area, and the absence of any other pathogens. Bacteria are small (0.8 by 1mm),however, and although they can be seen with a com-pound microscope, they all resemble tiny rods and haveno distinguishing morphological characteristics for iden-tification. Care must be taken, therefore, to exclude

BASIC PROCEDURES IN THE DIAGNOSIS OF PLANT DISEASES 73

the possibility that the observed bacteria are secondarysaprophytes, i.e., bacteria that are growing in tissuekilled by some other cause. Selective media are availablefor the selective cultivation of almost all plant patho-genic bacteria free of common saprophytes so that thegenus and even some species can be identified. Theeasiest and surest way to prove that the observed bacterium is the pathogen is through isolation andgrowth of the bacterium in pure culture and, using asingle colony for reinoculation of a susceptible hostplant, reproducing the symptoms of the disease andcomparing them with those produced by known speciesof bacteria. Since the late 1970s, immunodiagnostictechniques, including agglutination and precipitation,fluorescent antibody staining, and enzyme-linkedimmunosorbent assay, have been used to detect andidentify plant pathogenic bacteria. Such techniques arequite sensitive, fairly specific, rapid, and easy toperform, and it is expected that soon standardized, reli-able antisera will be available for serodiagnostic assaysof plant pathogenic bacteria.

Since 1980, newer techniques have been used involv-ing an automated analysis of fatty acid profiles of thebacteria or of the substances utilized by the bacteria forfood (Biolog). Additional identification tests includecomparison of the number of DNA pieces released by certain restriction enzymes, or degrees (percentages) ofhybridization of the DNA of an unknown bacteriumwith the DNA of a known one. Some of the moleculartechniques are now used for the identification of fastid-ious vascular bacteria.

Diseases caused by mollicutes appear as stunting ofplants, yellowing or reddening of leaves, proliferation ofshoots and roots, production of abnormal flowers, andeventual decline and death of the plant. Mollicutes aresmall, polymorphic, wall-less bacteria that live in youngphloem cells of their hosts; they are generally visibleonly under an electron microscope and, except for thegenus Spiroplasma, cannot be cultured on nutrientmedia. The diagnosis of such diseases, therefore, isbased on symptomatology, graft transmissibility, trans-mission by certain insect vectors, electron microscopy,sensitivity to tetracycline antibiotics but not to peni-cillin, sensitivity to moderately high (32–35.8°C) tem-peratures, and, in a few cases in which specific antiserahave been prepared, on serodiagnostic tests.

Diseases Caused by Viruses and Viroids

Many viruses (and viroids) cause distinctive symptomsin their hosts, and so the disease and the virus (or viroid)can be identified quickly by the symptoms. In the manyother cases in which this is not possible, however, the

diseases are diagnosed and the viruses are identified pri-marily as follows: (1) through virus transmission teststo specific host plants by sap inoculation or by grafting,and sometimes by certain insect, nematode, fungus, ormite vectors; (2) for viruses for which specific antiseraare available, by using serodiagnostic tests, primarilyenzyme-linked immunosorbent assays (ELISA), gel dif-fusion tests, microprecipitin tests, and fluorescent anti-body staining; (3) by electron microscopy techniquessuch as negative staining of virus particles in leaf dip or purified preparations, or immune-specific electronmicroscopy (a combination of serodiagnosis and elec-tron microscopy); (4) by microscopic examination ofinfected cells for specific crystalline or amorphous inclu-sions, which usually are diagnostic of the group towhich the virus belongs; (5) through electrophoretictests, useful primarily for detection and diagnosis of viroids and of nucleic acids of viruses; and (6) viahybridization of commercially available radioactiveDNA complementary to a certain virus DNA or RNA, or viroid RNA, with the DNA or RNA presentin plant sap and attached to a membrane filter(immunoblot).

Diseases Caused by More Than One Pathogen

Quite frequently a plant may be attacked by two ormore pathogens of the same or different kinds and maydevelop one or more types of disease symptoms. It isimportant to recognize the presence of the additionalpathogen(s). Once this is ascertained, the diagnosis ofthe disease(s) and the identification of the pathogen(s)proceed as described earlier for each kind of pathogen.

Noninfectious Diseases

If no pathogen can be found, cultured, or transmittedfrom a diseased plant, then it must be assumed that thedisease is caused by an abiotic environmental factor. Thenumber of environmental factors that can cause diseasein plants is almost unlimited, but most of them affect plants by interfering with normal physiologicalprocesses. Such interference may be a result of an excessof a toxic substance in the soil or in the air, a lack of anessential substance (water, oxygen, or mineral nutri-ents), or a result of an extreme in the conditions sup-porting plant life (temperature, humidity, oxygen, CO2,or light). Some of these effects may be the result ofnormal conditions (e.g., low temperatures) occurring atthe wrong time or of abnormal conditions broughtabout naturally (flooding or drought) or by the activi-

74 1. INTRODUCTION

ties of people and their machines (air pollutants, soilcompaction, and weed killers).

The specific environmental factor that has caused adisease might be determined by observing a change inthe environment, e.g., a flood or an unseasonable frost.Some environmental factors cause specific symptoms on plants that help determine the cause of the malady,but most of them cause nonspecific symptoms that,unless the history of the environmental conditions isknown, make it difficult to diagnose the cause accurately.

Identification of a Previously Unknown Disease:Koch’s Rules (Postulates)

When a pathogen is found on a diseased plant, thepathogen is identified by reference to special manuals;if the pathogen is known to cause such a disease and thediagnostician is confident that no other causal agents are involved, then the diagnosis of the disease may beconsidered completed. If, however, the pathogen foundseems to be the cause of the disease but no previousreports exist to support this, then the steps described onpage 27 under Koch’s postulates are taken to verify thehypothesis that the isolated pathogen is the cause of thedisease

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