Encyclopedia of

Plant Physiology New Series Volume 15 A

Editors

A. Pirson, G6ttingen M.H. Zimmermann, Harvard

Inorganic Plant Nutrition Edited by

A. LaucWi and RL. Bieleski

Contributors

C.l Asher L. Beevers R T. Besford R.L. Bieleski P. Boger E.G. Bollard H. Bothe D. Bouma G.D. Bowen F.C. Cannon C.C. Delwiche 1 Dobereiner W.M. Dugger D.G. Edwards lB. Ferguson T.l Flowers RC. Foster W.H. Gabelman G.C. Gerloff R.H. Hageman A. Lauchli U. Liittge D. Marme H. Marschner 1 Moorby M.G. Pitman A. Pollard A. Quispel A.D. Robson R Roth A.D. Rovira G. Sandmann lA. Schiff W.R. Ullrich D. Werner R.G. WynJones M.G. Yates

With a Foreword by E. Epstein

With 131 Figures

Springer-Verlag Berlin Heidelberg New York Tokyo 1983

Professor Dr. A. LXUCHLI University of California Department of Land, Air and Water Resources Hoagland Hall Davis, CA 95616jUSA

Dr. R.L. BmLESKI Department of Scientific and Industrial Research Division of Horticulture and Processing Private Bag Auckland New Zealand

ISBN-13 :978-3-642-68887-4 e-ISBN-13: 978-3-642-68885-0 DOl: 10.1007/978-3-642-68885-0

Library of Congress Cataloging in Publication Data. Main entry under title: Inorganic plant nutrition. (Encyclopedia of plant physiology; new ser., v. 15) 1. Plants-Nutrition. I. Liiuchli, A. (Andre), 1933-. II. Bieleski, R.L. (Roderick Leon), 1931-. III. Series. QK711.2.E5 n. s., vol. 15 581.1 s [581.1'3] 83-9861 [QK867] ISBN-13 :978-3-642-68887-4 (U.S.).

This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying machine or similar means, and storage in data banks.

Under §54 of the German Copyright Law where copies are made for other than private use, a fee is payable to "Verwertungsgesellschaft Wort" Munich.

© by Springer-Verlag Berlin-Heidelberg 1983 Softcover reprint of the hardcover 1st edition 1983

The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement that such names are exempt from the relevant protective laws and regulations and therefore free for general use.

2131/3130-543210

Foreword

The first book bearing the title of this volume, Inorganic Plant Nutrition, was written by D.R. HOAGLAND of the University of California at Berkeley. As indicated by its extended title, Lectures on the Inorganic Nutrition of Plants, it is a collection of lectures - the JOHN M. PRATHER lectures, which he was invited in 1942 to give. at Harvard University and presented there between April 10 and 23 of that year - 41 years before the publication of the present volume. They were not "originally intended for publication" but fortunately HOAGLAND was persuaded to publish them; the book appeared in 1944.

It might at first blush seem inappropriate to draw comparisons between a book embodying a set of lectures by a single author and an encyclopedic volume with no less than 37 contributors. But HOAGLAND'S book was a compre­hensive account of the state of this science in his time, as the present volume is for ours. It was then still possible for one person, at least for a person of HOAGLAND'S intellectual breadth and catholicity of interests, to encompass many major areas of the entire field, from the soil substrate to the metabolic roles of nitrogen, potassium, and other nutrients, and from basic scientific topics to the application of plant nutritional research in solving problems encountered in the field. Thus despite HOAGLAND'S admittedly more personal approach, a comparison of these two books serves to drive home the enormous progress that has been made in this science in the intervening years - and draws attention to areas that have lagged behind the broad surge of advancement of the field as a whole.

The first and most pervasive impression to emerge from a perusal of the two books is the effect that new techniques have had on the progress of inorganic plant nutrition, and the conviction that dazzling prospects are opening up by further advances in research tools and their application to this science. Just before America's entry into World War II HOAGLAND, in collaboration with the late, great P.R. STOUT, was among the very first investigators to apply radioisotopes of essential inorganic nutrients to the study of plant nutrition, in particular, of ion transport. I well remember the early days of radioactive tracers when, as a graduate student in that laboratory, I was in on the resump­tion of that work in the years immediately following World War II. We did our own target chemistry on material irradiated in the cyclotron up "on the hill." Our Geiger-Muller tubes were hand-made in the laboratory. I even had to determine the half-life of one of the radioisotopes I used, manganes,e-52, which had not been determined, and was obliged to do the job with a quartz fiber electroscope because our G.-M. counters were so unstable in their perfor­mance from day to day.

HOAGLAND relished this revolutionary innovation, but he did not live to see the enormous developments that the use of radioisotopes, and of stable

VI Foreword

isotopic tracers, especially nitrogen-15, would make possible in every branch of plant nutrition, from field studies to biochemical investigations. In the present volume nearly all chapters bear witness to the utility of isotopic tracers as powerful tools in the investigation of every aspect of this science.

Virtually simultaneous with the advent of tracer methodology was the devel­opment of chromatographic and electrophoretic techniques in all their variety. Their effect has been most pronounced in biochemical investigations. In the present context, they have played a large role in the advances in our understand­ing of the metabolism of nitrogen, phosphorus, and sulfur.

Biochemical events occur in space and time. The traditional approach of biochemists has been to disregard the former by disrupting the cell and studying the reactions between biochemical entities as a function of time - hence the emphasis on kinetics in classical biochemistry. Plant nutritionists cannot disre­gard space: membranes, sites, compartments, transport, immobilization, seques­tration, gradients, and fluxes are of the very essence in inorganic plant nutrition. Hence plant nutritionists have had to deal with structure, at levels ranging from the whole plant to subcellular entities. It is in studies of spatial relation­ships, especially in tissues and cells, that new technological tools-of-the-trade have made possible advances undreamed of 40 years ago. Electron probe X-ray microanalysis, laser probe analysis, ion probe mass analysis, and still other methods for pinpointing the distribution and localization of nutrient and other elements represent a whole new armamentarium at the disposal of the plant nutritionist. These and other localization techniques are already creating a revo­lution in inorganic plant analysis, yielding information entirely beyond the scope of traditional analytical techniques. Ion-sensitive microelectrodes are in this kit of new tools. Methods for the isolation of membranes, protoplasts, vacuoles, and other cellular organelles are also increasingly useful in sorting out the traffic patterns of inorganic nutrients (and other elements) in space and time.

One of HOAGLAND'S best-known contributions to whole-plant nutrition was his development, with his long-time collaborator T.e. BROYER, of what came to be known as "Hoagland solution," or rather, solutions, because there are two, the second containing ammonium as well as nitrate. These solutions are not in principle different from other such solutions that had been in use since the middle of the 19th century. In all of them, most nutrients are present in concentrations far in excess of their concentrations in typical soil solutions, to enable plants to grow for long periods by drawing on a large supply of nutrients contained in conveniently small volumes of solution.

HOAGLAND was aware that plants can grow well at much lower concentra­tions of nutrients in the medium, and do so in nature. But progress in developing the technology of culture media automatically maintained at predetermined, realistically low concentrations has been slow and sporadic. There is now, how­ever, a much wider awareness of the limitations of high-concentration, Hoag­land-type nutrient solutions, and an awareness as well that the technology for the development of sophisticated, low-concentration solution culture systems is "on the shelf." Progress so far in this field is recorded in the present volume. It will be exciting to read the report on this subject in the next edition of this work.

Foreword VII

Fundamental in any nutritional science is the question: what are the nu­trients? In inorganic plant nutrition, the problem is to determine what elements besides carbon, hydrogen, and oxygen are essential for the life of the plant. Forty years ago much attention was paid to this topic, with HOAGLAND and his collaborators in the van of the effort. The essentiality of molybdenum for higher green plants was discovered in HOAGLAND'S Division of Plant Nutrition and with his inspiration. Not long after his death in 1949, the impetus of this and related work led to the discovery of the essentiality of chlorine in the same laboratory. There followed the demonstration of the essentiality of cobalt for legumes fixing nitrogen symbiotically, accomplished independently by two groups, including the one founded by HOAGLAND.

As in the other instances discussed so far, it was the advent of new materials and techniques that made these discoveries possible. The main material was borosilicate glass, and the techniques were chemical procedures for purging the experimental solutions of inadvertent contaminants. Since that time new experimental and purification techniques have developed apace. They have been used by animal nutritionists to establish the essentiality of a whole raft of "new" inorganic nutrients: fluorine, silicon, vanadium, chromium, nickel, arse­nic, and selenium. The present volume does not, however, record a comparable interest in and effort toward the discovery of new plant micronutrients. On the other hand, great progress has been made in our understanding of the roles played by the known micronutrients, especially the heavy metals, in the function of enzymes and electron transfer processes.

New techniques, new machines and new methodologies thus have greatly advanced our knowledge of plant nutrition beyond its status 40 years ago. The cornucopia of the chemist, the physicist, and the engineer will continue to pour forth new tools that plant nutritionists will wield in the laboratory, the green­house, and the field.

The present volume, however, delineates developments other than those that depend largely or exclusively on new technology. Inorganic plant nutrition in both its classical period (the 19th century) and its neoclassical development (in the first half of the present century) bears the imprint of, mainly, continental Europe and the British Isles, the United States, and Australia. The motivation for pursuing it came almost exclusively from agriculture: plant nutritional re­search dealt with beans, barley, wheat, corn, tobacco, alfalfa, soybeans, and a few other economically important species. Considering the wide world and its wealth of varied plant life, plant nutrition thus has had an alarmingly narrow focus in terms of geography, ecosystems, and experimental plant materials. The present volume documents a broadening of the intellectual scope of the science of inorganic plant nutrition - almost entirely a development of the last few decades. For the further advancement of our science this development is no less significant than the new knowledge made possible by new techniques. In addition, it is extending the application of plant nutritional knowledge to agriculture everywhere, and to enterprises other than agriculture as well.

As for science per se, the processes of plant nutrition do more than nourish the plant. They are instrumental in injecting huge ~mounts of nutrient and other elements into the processes of global biogeochemical cycling. All elements

VIII Foreword

are involved to some extent, but the drain of phosphorus into the oceanic sinks is the one of greatest concern. Unlike nitrogen, phosphorus is not recycled, and its terrestrial supplies are ftnite.

Phosphate is of interest in another context. It is absorbed by most plants in a symbiotic relationship with fungi. Mycorrhizae seem to be nearly universal in terrestrial plants. Interest in mycorrhizae and their effects on the acquisition of phosphate (and some other nutrients) is unlikely to rival that in nitrogen fixation through the symbiosis between legumes and Rhizobium, but in due time it may come close.

Mycorrhizae had long been known to occur in forest trees. The recent realiza­tion that they are almost universal in terrestrial plants including crops has been one impetus, among several, leading to a greater rapport between plant nutritionists and ecologists than existed heretofore. Other factors in this interdis­ciplinary rapprochement have been (a) the realization of the importance of high concentrations of heavy metals in both natural and "manhandled" eco­systems; (b) the recognition that nutrient deftciencies can playa major, often the preponderant, role in the distribution of wild species, and (c) the under­standing that agricultural plant nutritionists interested in salinity and ecologists studying halophytes have much to learn from each other.

The response of plants to the adverse conditions of high metal concentra­tions, low soil fertility, and salinity is a function of the genotype. The possibility therefore exists of applying the concepts and techniques of physiological and biochemical genetics to the study of the responses of plants to these edaphic features. It is only in the last few decades that this possibility has begun to be realized; even now, the entire subject is still in its pioneering phase. What has been accomplished clearly demonstrates the potential of this approach, and the prospects are enticing.

The broader concepts and interdisciplinary connections of inorganic plant nutrition that have emerged in recent decades have profound implications for the applications of this science in the service of mankind. Sophisticated plant nutritional science will increasingly spread to areas where agriculture has re­mained in a traditional mold, and be applied to crops it has so far largely ignored, including tropical ones. Many tropical soils, especially in the humid tropics, present vexing plant nutritional problems: they are often acidic, with high concentrations of soluble aluminum, manganese, or both, and have an inordinate propensity for ftxing phosphate in forms unavailable to plants. Other nutritional problems, especially micronutrient deftciencies, are endemic in many of them. There is no way in which the traditional methods for coping with these problems - liming, use of amendments and fertilizers - can by themselves cure these ills. It will be necessary to develop lines of crops better adapted to these conditions than are the present varieties.

But it is by no means only in the tropics that a genetic appr9ach will have to be taken. The crops of the agriculturally advanced countries have been select­ed and bred to bestow on them desirable traits such as disease resistance, cold hardiness, early maturation, and many more. They have also been bred for high yield under nutritionally luxuriant conditions of ample fertilization. They may thus have been selected inadvertently against effIciency in mineral nutrition,

Foreword IX

including avid absorption from soils of low fertility in respect to one or more inorganic nutrients, rapid translocation of nutrients throughout the plant body, effective storage when supplies are ample, and frugal metabolic utilization when their concentrations in the tissue are relatively low. It is thus quite possible that many of the successful crops of the temperature zone are genetically defec­tive or crippled in their plant nutritional capabilities.

It is a reflection on our science that it is based in so large a measure on findings from experiments with these plants. More attention than is evident in this volume should be paid to the inorganic nutrition of wild plants - plants that have been under the selective pressure of often scanty nutrient supplies throughout their evolutionary history.

In the future it may no longer be possible, even in agriculturally advanced countries, to apply fertilizer virtually ad lib, because of constraints in availabi­lity, dollar cost, energy cost, and objections on environmental grounds. In many agriculturally less advanced countries such profligate application of fertilizer has never been affordable. These considerations lend force to the argument that plant nutritionists ought to collaborate with geneticists and breeders to develop nutrient-efficient genotypes of crops. They will take maximal advantage of the natural fertility of the soil, and of what fertilizer may be applied out of the bag. Plant nutritional studies of biologically productive wild plants can provide guidelines as to what traits should be incorporated into these new, nutrient-conserving varieties.

Salinity impairs agricultural productivity in arid and semi-arid regions where crop production depends on irrigation. Like heavy metal toxicity and low ferti­lity, this adverse condition has also been dealt with primarily by capital-inten­sive, energy-intensive measures: reclamation, drainage, overirrigation, and other technological operations. The existence of halophytes and of heritable variation in salt tolerance even in crop species points the way to a genetic approach to this problem as well: the development of salt-tolerant crops. This represents yet another challenge for collaboration between plant nutritionists and plant geneticist-breeders.

It may be that soils now considered marginal for agricultural production can be used to good advantage for this purpose if crops genetically tailored to cope with the soil conditions are developed. Still poorer soils may surely be used for the production of energy crops or the cultivation of plants yielding special materials such as lubricants and medicinals. The joint efforts of plant nutritionists and breeders will be needed in these labors as well.

The editors of this volume have assembled an array of distinguished scientists who collectively report a wealth of new knowledge derived from the imaginative and skillful application of powei:ful new tools and methodologies, and who convey the message that inorganic plant nutrition is broadening its intellectual perspective and forging interdisciplinary linkages with other plant and environ­mental sciences on a scale that has no precedent. Users of this volume whose reading measures up to the work that authors and editors have put into it will be amply rewarded, and spurred on in their efforts to advance still further the science of inorganic plant nutrition.

EMANUEL EpSTEIN

Contents Part A

Introduction A. LXUCHLI and R.L. BIELESKI

I. General Chapters of Inorganic Plant Nutrition

1.1 General Introduction to the Mineral Nutrition of Plants H. MARSCHNER (With 11 Figures)

1

1 Introduction and Historical Resume ..... 5 1.1 Essential Mineral Elements - Plant Nutrients 5 1.2 Function of Essential Mineral Elements 6 1.3 Beneficial Mineral Elements 7 1.4 Recent Developments 9

1.4.1 Calcium 10 1.4.2 Potassium . 11 1.4.3 Phosphorus 13 1.4.4 Nitrogen 13 1.4.5 Copper . . 14 1.4.6 Chlorine 15

2 Uptake and Long-Distance Transport of Mineral Elements 16 2.1 Ion Concentration at the Root Surface, Role of the "Rhizosphere" 16 2.2 Long-Distance Transport in the Xylem ....... 18

2.2.1 From the Roots to the Shoot ......... 18 2.2.2 Into Fruits, Seeds and Storage Organs ..... 19 2.2.3 Retranslocation of Mineral Elements from Leaves 20

3 Calcium Nutrition of Higher Plants 22 3.1 Introduction . . . . . . . . . . . 22 3.2 Calcium Demand of Higher Plants 22 3.3 Calcium Uptake by the Roots 23 3.4 Long-Distance Transport of Calcium 23

3.4.1 Xylem Transport ...... 23 3.4.2 Phloem Transport . . . . . . 26 3.4.3 Xylem Versus Phloem Transport 27

3.5 Role of Phytohormones and Growth Regulators 29 3.6 Conclusion and Outlook . . . . . . . . . . . 29

4 Mineral Nutrition and Physiology of Yield Formation - Sink-Source Relationship ....................... 30 4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . 30 4.2 Effect of Mineral Nutrition on Phytohormone Level and Sink

Formation . . . . . . . . . . . . . . . . . . . . . 31 4.3 Effect of Mineral Nutrients on Fertilization ...... 33 4.4 Source-Sink Interactions in Relation to Mineral Nutrition 34

5 Environmental Aspects of Mineral Nutrition 37 5.1 Introduction . . . 37

5.1.1 Nitrogen 38 5.1.2 Heavy Metals . . . . . . . . . 39

XII Contents Part A

5.2 Heavy Metal Toxicity . . . . . . . 39 5.3 Heavy Metals in the Food Chain . . 40 5.4 Heavy Metals in the SoiljPlant System 41

5.4.1 Content of Soils . . . . . . . 41 5.4.2 Soil Factors Affecting Heavy Metal Accumulation in Plants 43 5.4.3 Genotypic Differences in Heavy Metal Uptake . 44 5.4.4 Distribution Within the Plants and Their Organs 46 5.4.5 Heavy Metal Tolerance 48

5.5 Concluding Remarks 49 References .......... 49

1.2 The Significance of Rhizosphere Microflora and Mycorrbizas in Plant Nutrition A.D. ROVIRA, G.D. BOWEN, and R.C. FOSTER (With 7 Figures)

1 Introduction ......... 61 2 Energy Supplies in the Rhizosphere 61

2.1 Exudates 61 2.2 Secretions . . . 62 2.3 Plant Mucilages 62 2.4 Mucigel . . . . 63 2.5 Lysates 63

3 Microbiology of the Rhizosphere 64 3.1 Populations of Micro-Organisms 64 3.2 Colonization of Roots by Micro-Organisms 64

4 Mathematical Modelling of the Rhizosphere 65 5 Microscopy of the Rhizosphere ....... 66

5.1 Light Microscopy . . . . . . . . . . . . 66 5.2 Scanning Electron Microscopy (S.E.M.) . . 66 5.3 Transmission Electron Microscopy (T.E.M.) 69

5.3.1 General Description ........ 69 5.3.2 Origin and Fine Structure of Root Mucilage 70 5.3.3 Microbial Invasion of the Mucilage and the Formation of Mucigel 72 5.3.4 Functions of Root Mucilage and Mucigel . . . . 72 5.3.5 The Outer Rhizosphere . . . . . . . . . . . . 72 5.3.6 Invasion of the Root by Microorganisms 73

6 The Role of Rhizosphere Microorganisms in Plant Nutrition 73 6.1 Availability of Nutrients . . . . . . . . 74

6.1.1 Nutrient Release and Immobilization 74 6.1.2 Nitrification and Denitrification 74 6.1.3 Nitrogen Fixation .. . . . 74 6.1.4 Phosphate Availability 74 6.1.5 Minor Nutrients . . . . . . 74

6.2 Growth and Morphology of Roots 75 6.2.1 Root Length and Root Hairs 75 6.2.2 Proteoid Roots 75

6.3 Nutrient Uptake Processes . 76 6.4 Physiology and Development 76

7 Mycorrhizas . . . . . . . . . 76 7.1 Plant Responses to Infection 78 7.2 Mechanisms of the Response 79

7.2.1 Nutrient Availability . 80 7.2.2 Absorption Characteristics of the Root 80 7.2.3 Absorption by the Fungus Component 80

7.3 Energy Requirements of Mycorrhizas 82 7.4 Overview of Mycorrhizas ........ 83

Contents Part A

8 General Conclusions References .....

1.3 Modern Solution Culture Techniques C.J. AsHER and D.G. EDWARDS (With 3 Figures)

XIII

84 86

1 Major Differences Between Solution Culture and Soil Culture 94 1.1 Mechanical Support . . . . . . . . . . . . . . . 94 1.2 Spatial Variation in Root Environment Parameters 95 1.3 Temporal Variation in Root Environment Parameters 97

1.3.1 Nutrient Depletion . . . . . . . . . . . . . 97 1.3.2 pH Shifts . . . . . . . . . . . . . . . . . 98

1.4 Root-Microorganism Interactions . . . . . . . . . 98 2 Uses and Limitations of Existing Solution Culture Methods 99

2.1 Non-Renewed or Intermittently Renewed Water Cultures and Sand Cultures . . . . . . . . . . . . . . . . . . . . 99 2.1.1 Use in Teaching, Demonstration, and Diagnosis 99 2.1.2 Production of Roots for Ion Transport Studies 101 2.1.3 Nutrient Essentiality . . . . . . . . . . . . 101 2.1.4 Effects of Root Environment Parameters 101 2.1.5 Establishment of Critical Tissue Concentrations 105 2.1.6 Control of Plant Nutrient Status . . . . . . . 105 2.1.7 Study of Symbiotic Associations with Microorganisms 106 2.1.8 Commercial Crop Production 108

2.2 Mist Culture . . . . . . . . . . . . . . . . 108 2.3 Flowing Solution Culture .......... 109

2.3.1 The Flow Rate Problem ........ 109 2.3.2 Composition of Flowing Culture Solutions 110 2.3.3 Research Applications 111 2.3.4 Likely Future Developments . 113 2.3.5 Commercial Crop Production 114

3 Summary and Conclusions 115 References ............. 115

1.4 Diagnosis of Mineral Deficiencies Using Plant Tests D. BOUMA (With 5 Figures)

1 Introduction 120 2 Plant Analysis . . . . . 121

2.1 Physiological Basis 121 2.2 Choice of Tissue .. 123 2.3 Factors Affecting the Relationship Between Nutrient Concentration and

Yield . . . . . . . . . . . . . . . . 124 2.3.1 Plant Development . . . . . . . . . 124 2.3.2 Effects of Changes in Age of Tissue 125 2.3.3 Plant Age and Critical Levels 126 2.3.4 Interactions Betweeri Nutrient Elements 127 2.3.5 Environmental Factors . . . . . . . 128 2.3.6 Other Factors Affecting Nutrient Composition 130

3 Physiological and Biochemical Approaches to Diagnosis 131 3.1 Introductory Remarks . . . . 131 3.2 Physiological Approaches ....... 131

3.2.1 Physiological Assessment . . . . . 131 3.2.2 Nutrient Stress ......... 132 3.2.3 Approaches Based on Photosynthesis 132 3.2.4 Other Approaches . . . . . . . . 133

XIV

3.3 Biochemical Approaches . . . . 3.3.1 Nitrogen and Molybdenum 3.3.2 Phosphorus . . . . . . . 3.3.3 Potassium and Magnesium 3.3.4 Iron and Manganese 3.3.5 Copper . . . . 3.3.6 Zinc .....

Contents Part A

4 Prospects for the Future

135 135 136 137 138 139 140 140 141 References ...... .

1.5 Interactions Between Nutrients in Higher Plants A.D. ROBSON and M.G. PITMAN (With 9 Figures)

1 Introduction ........................... 147 2 Interactions Between Nutrients in Monoculture ............ 152

2.1 Interactions Between Nutrients Affecting the Absorption of Nutrients 152 2.1.1 Interactions Occurring in the Soil ............. 152 2.1.2 Absorption from Solution at the Root Surface . . . . . . .. 156

2.2 Interactions Between Nutrients Affecting the Utilization of Nutrients Within the Plant 160 2.2.1 Distribution . . . . . . . . . . . . . . . . . . . . . .. 161 2.2.2 Function . . . . . . . . . . . . . . . . . . . . . . .. 164

2.3 Complex Interactions Between Nutrients Involving Several Processes 167 2.3.1 Calcium/Aluminium/Phosphate ...... 167 2.3.2 Zinc/Phosphate ............. 169

3 Interactions Between Nutrients in Mixed Communities 170 4 Conclusion 173 References ................... 173

1.6 Import and Export of Mineral Nutrients in Plant Roots U. LUnGE (With 10 Figures)

1 Introduction: The Dual Role of Roots in the Evolution of Higher Land Plants ............................ 181

2 Relations Between Structure and Transport Functions Along the Length of Roots ........................... 182 2.1 The Phenomenon of Variations in Transport Functions Along the

Length of Roots ........ . . . . . . . . 182 2.2 Structure-Function Relations in Various Root Zones 183

2.2.1 The Root Surface 183 2.2.2 The Cortex 189 2.2.3 The Endodermis . 190 2.2.4 The Stele . . . . 193

3 Variations of Physiological Activities Along the Length of Roots 199 3.1 Growth, Differentiation and Hormonal Gradients . . . 199 3.2 Bioelectrical Fields Along Roots .......... 200 3.3 Differences in Ion Transport Mechanisms Along Roots 201

4 Root-Shoot Interactions and Circulation in the Whole Plant 202 4.1 Some Examples Illustrating General Aspects of Circulation 202 4.2 Nitrogen, Sulphur and Phosphorus 203

5 Conclusion 204 References 204

1.7 Cycling of Elements in the Biosphere c.c. DELWICHE (With 5 Figures)

1 The Sources of Plant Constituents 212 1.1 Soil and Atmospheric Sources 212 1.2 The Weathering Process . . . 212

Contents Part A

2 The Nature of Cycles 2.1 The Hydrologic Cycle . 2.2 The Sedimentary Cycle 2.3 The Magmatic Cycle 2.4 The Geobiological Cycles

3 The Nitrogen Cycle 3.1 Overall Cycle Features 3.2 Nitrification . . . 3.3 Denitrification . . 3.4 Nitrogen Fixation 3.5 Human Influences

4 The Sulfur Cycle , . . 4.1 Comparison with the Nitrogen Cycle 4.2 Microbial Oxidation 4.3 Sulfate Reduction 4.4 Patterns of Sulfur Movement 4.5 Human Influences

5 The Phosphorus Cycle 5.1 Oxidation and Reduction 5.2 Movement and Transport in the Biosphere 5.3 Human Influences ......... .

6 Other Elements ............ . 6.1 Biological Cycling ......... . 6.2 The Special Significance of Iron and Aluminum 6.3 Hydrogen Ion ..... . 6.4 Characteristics of Sediments . . . . . . . 6.5 Passive Cycling . . . . . . . . . . . . . 6.6 Possibilities of Deficiency ....... .

7 "Open" Versus "Closed" Agricultural Systems References ................ .

II. Inorganic Nitrogen Nutrition

11.1 Physiology, Biochemistry and Genetics of Dinitrogen Fixation H. BOTHE, M.G. YATES, and F.C. CANNON (With 3 Figures)

xv

214 214 215 217 217 219 219 221 222 223 224 225 225 227 227 228 228 229 229 230 231 232 232 232 233 234 235 235 236 237

1 The Nitrogen-Fixing Organisms and the Nitrogenase Reactions 241 1.1 Introduction .............. 241 1.2 Nitrogen Fixation by Free-Living Organisms 244 1.3 Symbiotic Nitrogen Fixation. 245 1.4 Substrates of Nitrogenase . . . . . . 247

2 Biochemistry of Nitrogen Fixation 248 2.1 Introduction ........... 248 2.2 Nomenclature of Nitrogenase Proteins 249 2.3 Physicochemical Properties of Nitrogenase Proteins 249 2.4 Metal Clusters in Nitrogenase Proteins . . . . . 251 2.5 EPR and Mossbauer Spectroscopy on the MoFe Protein 252 2.6 The FeMo Cofactor and the Fe Protein . . . . . 253 2.7 Nitrogenase Proteins in Photosynthetic Organisms . . . 254 2.8 The Mechanism of Nitrogenase Activity ....... 254

2.8.1 The Roles of the Two Proteins . . . . . . . . . 255 2.8.2 Evidence for Interaction of MgA TP and MgADP with the MoFe

Protein .......... 257 2.8.3 The Nature of the Active Site(s) 257 2.8.4 Pathways of N2-Reduction 258

3 Electron Transport to Nitrogenase 259 3.1 Introduction 259 3.2 Ferredoxins . . . . . . . . 260

XVI Contents Part A

3.3 Flavodoxins .................... 260 3.4 Electron Donors . . . . . . . . . . . . . . . . . . . 261

4 Mechanisms to Protect Nitrogenase Against Damage by Oxygen 263 4.1 In Free-Living Organisms . . . . . . . . . . . 263 4.2 The Heterocysts of Blue-Green Algae . . . . . . 264 4.3 The Role of Leghaemoglobin in Legume Nodules 265

5 Regulation of Nitrogenase Activity and Biosynthesis 265 5.1 Regulation of Nitrogenase Biosynthesis . . . . . 265 5.2 Regulation of Nitrogenase Activity . . . . . . . 267

6 The Hydrogenase-Nitrogenase Relationship . . . . . 268 7 The Molecular and Genetic Characterization of Nitrogen Fixation Genes 271

7.1 Introduction 271 7.2 The nif Genes . . . . . . . . . . 272 7.3 nifGene Products . . . . . . . . 273 7.4 Cloning of K. pneumoniae nifGenes 274 7.5 A Physical Map of nifGenes 275 7.6 Interspecies Homology of Nitrogenase Genes 276

References . . . . . . . . . . . . . . . . . . 276

11.2 Dinitrogen-Fixing Symbioses with Legumes, Non-Legume Angiosperms and Associative Symbioses A. QrnsPEL (With 7 Figures)

1 Introduction . . . . . . . . . . . . . . . . . . . . . 2 Description of the Main Symbiotic Dinitrogen-Fixing Systems

2.1 Associative Symbioses 2.2 Symbioses with Cyanobacteria . . .

2.2.1 Distribution ....... . 2.2.2 Description and Development 2.2.3 N2 Fixation (C2H2 Reduction)

2.3 Root Nodules with Actinomycetes: Actinorhizas 2.3.1 Distribution ..... . 2.3.2 Description ....... . 2.3.3 Infection and Development . . 2.3.4 N 2 Fixation (C2H 2 Reduction)

2.4 Leguminous Root Nodules with Rhizobium 2.4.1 Distribution ......... . 2.4.2 Description ......... . 2.4.3 Infection and Nodule Development 2.4.4 N2 Fixation (C2H2 Reduction)

2.5 Non-Leguminous Root Nodules with Rhizobium 3 The Dinitrogen-Fixing Micro-Symbionts: Isolates and Cultures

3.1 Introduction ............. . 3.2 Cyanobacteria . . . . . . . . . . . . . . 3.3 Frankia, the Endophyte from the Actinorhizas

3.3.1 Isolation and Cultivation 3.3.2 Specificity . . . . . 3.3.3 Nutrient Requirements 3.3.4 Metabolic Activities .

3.4 Rhizobium ...... . 3.4.1 Isolation and Description 3.4.2 Taxonomy . . . . . . 3.4.3 Metabolism ..... 3.4.4 N2 Fixation (C2H2 Reduction) 3.4.5 Genetics . . . . . . . . . .

4 Symbiotic Relations . . . . . . . . . 4.1 Chemotaxis and Rhizosphere Accumulation 4.2 Binding of Rhizobium to Root Hairs

286 287 287 287 287 287 288 288 288 289 291 291 291 291 291 292 295 295 295 295 296 297 297 298 298 299 299 299 300 300 302 303 304 304 305

Contents Part A

4.3 Root Hair Deformation and Infection-Thread Formation 4.4 Cell Wall Degrading Enzymes ........ . 4.5 The Role of Plant Hormones in Nodule Formation 4.6 Miscellaneous Problems

5 The N 2-Fixing System . . . . . .. . 5.1 Introduction ......... . 5.2 Bacteroids .......... . 5.3 The Bacteroid-Containing Plant Cells 5.4 Nitrogenase . . . . . . . . . . . 5.5 NH3 Assimilation . . . . .... 5.6 Oxygen Regulation and Leghaemoglobin 5.7 Hydrogen Production and Hydrogen Uptake

6 Root Nodules as Part of the Whole Plant 7 Concluding Remarks . References . . . . . . . . . . . . . . . . . .

11.3 Dinitrogen Fixation in Rhizosphere and Phyllosphere Associations J. DOBEREINER (With 2 Figures)

1 Introduction . . . . . . . . . . . . . . 2 Cbaracterization of Rhizocoenoses

2.1 Sugar Cane - Beijerinckia . . . . . . . 2.2 Paspalum notatum - Azotobacter paspa/i 2.3 Azospirillum Rhizocoenoses . . . .

2.3.1 Taxonomy of Azospirillum spp. 2.3.2 Root Infection . . . .... 2.3.3 Host Plant Specificity 2.3.4 Physiology of Azospirillum . .

2.4 Associations with Other N 2-Fixing Bacteria 3 Agronomic Aspects . . .

3.1 Plant Genotype Effects 3.2 Environmental Effects 3.3 Inoculation . . . . .

4 Phyllosphere Associations 4.1 Microorganisms in the Phyllosphere 4.2 Nitrogen Fixation in the Phyllosphere

5 General Conclusion References . . . . . . . . . . . . . . .

11.4 Uptake and Reduction of Nitrate: Bacteria and Higher Plants L. BEEVERS and R.H. HAGEMAN

1 Introduction . . . . . . . . . . . . . . . . . . . . . 2 Available Nitrogen Sources . . . . . . . . . . . . . ..

2.1 Species Differences in Ammonium and Nitrate Utilization 2.2 Influence of Ammonium or Nitrate on Cation Uptake 2.3 Nitrate Uptake ................. . 2.4 Influence of Ammonium on Nitrate Uptake and Utilization

3 Nitrate Reduction . . . . . . . . . . . . . 3.1 Bacteria .................... . 3.2 Dissimilatory Nitrate Reductase . . . . . . . . . . . 3.3 Assimilatory Nitrate Reduction in Bacteria . . . . . . 3.4 Characterization of Nitrate Reductase from Higher Plants

4 Molybdenum in Nitrate Reduction 5 Nitrite Reduction . . . . . .

5.1 Assimilatory Bacteria 5.2 Dissimilatory Bacteria 5.3 Nitrite Reductase in Plants

XVII

307 307 308 310 311 311 312 314 315 315 317 318 319 323 323

330 330 331 332 332 333 334 336 337 340 341 341 342 342 343 344 344 344 345

351 352 352 353 354 355 356 356 356 358 358 360 361 361 361 361

XVIII Contents Part A

6 Location of Enzymes of Nitrate Assimilation in Higher Plants 7 Provision of Reductant for Nitrate Assimilation in Higher Plants 8 Regulation of Nitrate Reductase in Higher Plants

8.1 Substrate . . 8.2 Hormonal 8.3 Molybdenum 8.4 Ammonium . 8.5 Light 8.6 Genetic ... 8.7 In Vivo Controls

9 Concluding Thoughts References . . . . . .

II.S Uptake and Reduction of Nitrate: Algae and Fungi W.R. ULLRICH (With 4 Figures)

363 363 364 364 365 365 366 366 366 367 368 369

1 Introduction . . . . . . . . . . . . . . 376 2 Nitrate and Nitrite Reduction in Algae 377

2.1 Nitrate Reductase of Eucaryotic Algae . 377 2.2 Nitrate Reductase in Blue-Green Algae 380 2.3 Nitrite Reductase in Algae . . . . . . 380 2.4 Location of Nitrate and Nitrite Reduction in Algal Cells 381 2.5 Stoichiometry Between Nitrate Reduction and O2 Exchange 381

3 Nitrate Uptake in Algae 382 3.1 General Remarks 382 3.2 Substrate Affinity . . . . . . 383 3.3 Light Dependence ..... 384 3.4 pH-Dependence ...... 385 3.5 Dependence on Carbon Sources 385 3.6 Inhibition by Anions 386 3.7 Inhibition by Ammonia and Amino Compounds 387 3.8 Effect of Metabolic Inhibitors and Uncouplers 387 3.9 Stoichiometry Between the Uptake of Nitrate and that of Other Ions 388 3.10 Transport Mechanism . . . . . . . . . . . . . . . . 388

4 Nitrite Uptake in Algae ....... . . . . . . . . . . 389 5 General Remarks on Regulation of Nitrate and Nitrite Uptake 390 6 Uptake and Reduction of Nitrate and Nitrite in Fungi 391 References . . . . . . . . . . . . . . . . . . . . . . . . 393

III. Metabolism of Sulfur and Phosphorus

m.l Reduction and Other Metabolic Reactions of Sulfate J.A. SCIDFF (With 6 Figures)

1 Introduction . . . . . . . . . . . . . . . . . . . . . . . .. 401 2 The Place of Sulfate Reduction in the Sulfur Cycle . . . . . . .. 402 3 Phylogenetic Distribution of Reactions Involving Sulfate Transfer and

Reduction . . . . . . . . . . . . . . . . . . . . . 403 4 Sulfate Uptake, Activation and Transfer ....... 404 5 Sulfate Reduction ................. 406

5.1 Detailed Reactions of the Two Assimilatory Pathways 408 5.1.1 The APS Pathway . . . . . . . . . . . . . 408 5.1.2 The PAPS Pathway ............ . 410

5.2 Location of Sulfate Reduction in Tissues and Organs of Multicellular Plants ............................ 413

Contents Part A

6 Speculations on the Origin and Evolution of Pathways of Sulfate Reduction

References

m.2 Physiology and Metabolism of Phosphate and Its Compounds R.L. BIELESKI and LB. FERGUSON (With 4 Figures)

1 Introduction . . . . . . . . . . . . . . . . . . . . 2 Uptake and Transport of Phosphate ........ . 3 Efflux of Phosphate, and Aspects of Phosphate Deficiency 4 Phosphorus Compartments and Pools . . . . . . 5 The Form of Phosphorus in the Cell ... . . . 6 Synthesis and Turnover of Phosphorus Compounds 7 Dynamics of Phosphate Use in the Plant 8 Conclusions References ............. .

Author- and Subject Index (see Part B)

XIX

413 416

422 424 428 431 433 440 443 445 445

Contents Part B

IV. General Function of Inorganic Nutrients in Growth and Metabolism

IV.l Genetic Basis ofInorganic Plant Nutrition G.c. GERWFF and W.H. GABELMAN (With 2 Figures)

IV.2 Mineral Nutrition and Growth

453

J. MOORBY and R.T. BESFORD (With 24 Figures) . 481

IV.3 Proteins, Enzymes and Inorganic Ions R.G. WYN JONES and A. POLLARD (With 5 Figures) 528

IVA The Enzymological Function of Heavy Metals and Their Role in Electron Transfer Processes of Plants G. SANDMANN and P. BOOER (With 4 Figures) . . . . . . . . . . . . . 563

V. Special Functions of Some Elements

V.l Calcium Transport and Function D. MARME (With 2 Figures) . .

V.2 Boron in Plant Metabolism W.M. DUGGER (With 4 Figures)

V.3 Sodium Versus Potassium: Substitution and Compartmentation T.J. FLOWERS and A. LXUCHLI (With 6 Figures) ...... .

VA Silica Metabolism D. WERNER and R. ROTH (With 3 Figures)

V.5 Involvement of Unusual Elements in Plant Growth and Nutrition

599

626

651

682

E.G. BOLLARD (With 4 Figures) ........... .. . . . 695

VI. Synthesis and Outlook R.L. BmLESKI and A. LXUCHLI (With 1 Figure) 745

Author Index 757

Subject Index 829

List of Contributors Part A and B

C.J. AsHER Dept. of Agriculture University of Queensland St. Lucia Queensland 4067/ Australia

L.BEEVERS 770 Van Vleet Oval Dept. of Botany and Microbiology University of Oklahoma Norman, OK 73019(USA

R. T. BESFORD Glasshouse Crops Research Institute Worthing Road Littlehampton West Sussex BN16 3PU/ United Kingdom

R.L. BIELESKI Dept. of Scientific and Industrial Research Division of Horticulture and Processing Private Bag Auckland/New Zealand

P. BOGER Lehrstuhl fiir Physiologie und Biochemie der Pflanzen Universitat Konstanz Postfach 5560 D-7750 Konstanz/FRG

E.G. BOLLARD Dept. of Scientific and Industrial Research Division of Horticulture and Processing Private Bag AucklandfNew Zealand

H. BOTHE Botanisches Institut Universitat Koln Gyrhofstr.15 D-5000 Koln 41/FRG

D. BOUMA CSIRO Division of Plant Industry P.O. Box 1600 Canberra, ACT, 2601/Australia

G.D. BOWEN CSIRO Division of Soils Private Bag 2 Post Office Glen Osmond South Australia 5064/Australia

F.C. CANNON BioTechnica International, Inc. 85 Bolten Street Cambridge, MA 02140(USA

C.C. DELWICHE University of California Dept. of Land, Air and Water Resources Hoagland Hall Davis, CA 95616(USA

J. DOBEREINER EMBRAPA PNPBS, Km 47 Seropedica 23460 Rio de Janeiro/Brazil

W.M. DUGGER Dept. of Botany and Plant Sciences University of California Riverside, CA 92521(USA

D.G. EDWARDS Dept. of Agriculture University of Queensland St. Lucia Queensland 4067/ Australia

E. EpSTEIN University of California Dept. of Land, Air and Water Resources Hoagland Hall Davis, CA 95616(USA

XXII

I.B. FERGUSON Division of Horticulture and Processing DSIR Private Bag AucldandjNew Zealand

T.J. FLOWERS School of Biological Sciences University of Sussex Falmer Brighton BNl 9QG/United Kingdom

R.C. FOSTER CSIRO Division of Soils Private Bag 2 Post Office Glen Osmond South Australia 5064/Australia

W.H. GABELMAN Department of Horticulture University of Wisconsin 1575 Linden Dr. Madison, WI 53706/USA

G.C. GERLOFF Dept. of Botany Birge Hall University of Wisconsin-Madison Madison, WI 53706/USA

R.H. HAGEMAN Dept. of Agronomy University of Illinois 1102 S Goodwin Ave. Urbana, IL 61801/USA

A. LXUCHLI University of California Dept. of Land, Air and Water Resources Hoagland Hall Davis, CA 95616/USA

U. LUTTGE Institut fiir Botanik Fachbereich Biologie (10) Technische Hochschule Darmstadt SchnittspahnstraBe 3 D-6100 Darmstadt/FRG

D. MARME Institut flir Biologie III SchiinzlestraBe 1 D-7800 Freiburg/FRG

List of Contributors Part A and B

H. MARSCHNER Institut fUr Pflanzenerniihrung Universitiit Hohenheim Postfach 700562 D-7000 Stuttgart 70/FRG

J. MooRBY Agricultural Research Council 160 Great Portland St. London WIN 6DT/United Kingdom

M.G. PITMAN School of Biological Sciences, A12 University of Sydney NSW 2006/ Australia

A. POLLARD Dept. of Biochemistry and Soil Sciences University College of North Wales Bangor, Gwynedd Wales/United Kingdom

A. QUISPEL Botanical Laboratory Dept. of Plant Molecular Biology University of Leiden N onnensteeg 3 2311 VL Leiden/The Netherlands

A.D. ROBSON Dept. of Soil Science and Plant Nutrition Institute of Agriculture University of Western Australia Nedlands Western Australia 6009/Australia

R. ROTH Fachbereich Botanik der Phillipps-Universitiit Marburg Lahnberge D-3550 Marburg/Lahn/FRG

A.D. ROVIRA CSIRO Division of Soils Private Bag 2 Post Office Glen Osmond South Australia 5064/Australia

G. SANDMANN Lehrstuhl flir Physiologie und Biochemie der Pflanzen Universitiit Konstanz Postfach 5560 D-7750 Konstanz/FRG

List of Contributors Part A and B

J.A. SCHIFF Institute for Photobiology of Cells and Organelles Brandeis University Waltham, MA 02254/USA

W.R. ULLRICH Institut fUr Botanik Technische Hochschule Darmstadt SchnittspahnstraBe 3 D-6100 Darmstadt/FRG

D. WERNER Fachbereich Botanik der Philipps-U niversitiit Marburg Lahnberge D-3550 Marburg/Lahn/FRG

R.G. WYN JONES Dept. of Biochemistry and Soil Science

XXIII

University College of North Wales Bangor, Gwynedd Wales/United Kingdom

M.G. YATES Agricultural Research Council Unit of Nitrogen Fixation University of Sussex Falmer Brighton BNl 9QGfUnited Kingdom