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Can the Quest for Drought Tolerant Crops AvoidArabidopsis Any Longer?Albino Maggio a , Robert J. Joly b , Paul M. Hasegawa b & Ray A. Bressan ba National Center of Energy, Environment and Innovative Technology , C.R. Trisaia, S.S.Jonica, Km 419–500, 75026, Rotendella, MT, Italyb Purdue University, Center for Plant Environmental Stress Physiology , 1165 HorticultureBuilding, West Lafayette, IN, 47907-1165, USAPublished online: 15 Oct 2008.

To cite this article: Albino Maggio , Robert J. Joly , Paul M. Hasegawa & Ray A. Bressan (2003) Can the Quest for DroughtTolerant Crops Avoid Arabidopsis Any Longer?, Journal of Crop Production, 7:1-2, 99-129

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Can the Quest for Drought Tolerant CropsAvoid Arabidopsis Any Longer?

Albino MaggioRobert J. Joly

Paul M. HasegawaRay A. Bressan

SUMMARY. The use of Arabidopsis as a model system in plant re-search has been a powerful tool for biologists in the last twenty years, yetcrop scientists largely have considered Arabidopsis an unsuitable systemfor addressing agricultural problems. The realization that Arabidopsisgenes can function ectopically in other plant species, together with re-cent advances in our understanding of Arabidopsis gene function, havegreatly facilitated the potential for genetic manipulation of crop species.Based on the available data on function in Arabidopsis and on our cur-rent knowledge of phenological, morphological, and biochemical factors

Albino Maggio is affiliated with the National Center of Energy, Environment andInnovative Technology, C.R. Trisaia, S.S. Jonica, Km 419-500, 75026 Rotendella(MT), Italy.

Robert J. Joly, Paul M. Hasegawa, and Ray A. Bressan are affiliated with thePurdue University, Center for Plant Environmental Stress Physiology, 1165 Horticul-ture Building, West Lafayette, IN 47907-1165 USA.

The authors thank Jian-Kang Zhu, Andrew Hanson, Hans Bohnert, Brian Dilkes,and David Rhodes for many helpful discussions and suggestions. Ray A. Bressanthanks the University of Arizona and especially Rob Leonard and Brian Larkins for be-ing such generous hosts during the writing of part of this work. They gratefully ac-knowledge Becky Fagan for her assistance in manuscript preparation.

[Haworth co-indexing entry note]: “Can the Quest for Drought Tolerant Crops Avoid Arabidopsis AnyLonger?” Maggio, Albino et al. Co-published simultaneously in Journal of Crop Production (Food ProductsPress, an imprint of The Haworth Press, Inc.) Vol. 7, No. 1/2 (#13/14), 2003, pp. 99-129; and: Crop Produc-tion in Saline Environments: Global and Integrative Perspectives (ed: Sham S. Goyal, Surinder K. Sharma,and D. William Rains) Food Products Press, an imprint of The Haworth Press, Inc., 2003, pp. 99-129. Singleor multiple copies of this article are available for a fee from The Haworth Document Delivery Service[1-800-HAWORTH, 9:00 a.m. - 5:00 p.m. (EST). E-mail address: docdelivery@haworthpress.com].

http://www.haworthpress.com/store/product.asp?sku=J144 2003 by The Haworth Press, Inc. All rights reserved.

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affecting water stress tolerance in plants, we identify in this chapter pos-sible strategies to improve drought stress tolerance, using the powerfulgenetic model Arabidopsis. Specifically, we consider those Arabidopsisgenes and mutants, whose respective functions and phenotypes may bedirectly or indirectly involved in improving drought stress tolerance.Genes that shorten or delay the flowering time, for instance, have beencloned and can be used to ehance mechanisms such as drought escapeand avoidance. Similarly, genes that alter stomatal function, leaf shape,area, and other aspects of plant morphology such as leaf architecture,may be good candidates to design a more efficient phenotype in terms ofwater consumption. This objective may also be accomplished by trans-ferring traits such as hairiness and waxiness of the leaf surface, which areknown xerophytic adaptations that have been characterized in Arabid-opsis. In addition to their regulation of water loss, plants may avoiddrought stress by enhancing the capacity to take up water from the soil.Mutants with altered root morphology and architecture have been de-scribed and are excellent candidates for elucidating the complex coordi-nation between water uptake and loss in plants. These include mutantswith altered root hydraulic conductivity, variable diameter of vessels andamount of vasculature within the root or stem. Finally, considering thedifficulties underlying the possible improvement of plant water-use effi-ciency (WUE), we identify alternative strategies to improve yield in wa-ter-limiting environments by manipulating the harvest index (HI). [Arti-cle copies available for a fee from The Haworth Document Delivery Service:1-800-HAWORTH. E-mail address: <docdelivery@haworthpress.com> Website:<http://www.HaworthPress.com> 2003 by The Haworth Press, Inc. All rightsreserved.]

KEYWORDS. Gene function, gene manipulation, water stress tolerance

INTRODUCTION

I also saw in my dream seven ears growing on one stalk, full and good;and seven ears, withered thin, and blighted by the east wind, sprouted af-ter them, and the thin ears swallowed up the seven good ears. And I toldit to the magicians, but there was no one who could explain it to me.

Genesis 41.22-24

Joseph explained the Pharaoh’s dream. Egypt would experience after sevenbountiful years, seven years of awful famine brought by the desiccating eastwind that withered the crops. Growing food in an arid environment has been,and still is, a very risky undertaking. How much have we learned in the inter-

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vening 5000 years? How much do we now know about growing crops in aridclimates? It may be imminently appropriate to ask this question in light of theunprecedented pressure that a rapidly expanding human population is placingon agriculture (Evans, 1998).

Among those who have worked on the cellular basis of desiccation toler-ance there is kept a deep dark secret that is openly discussed only by peoplewho study how real plants in the real world tolerate dry, hot conditions: Plantscan’t grow without water! If this sounds too pessimistic, at least it could beasked: Can some plants grow more with less water? The amount of growth peramount of water used is known as water-use efficiency, and it is a subject ofsome debate. Generally, however, the answer is yes, some plants grow morewith less water, but not by much. In fact, when plants are faced with conditionsof severe desiccation, they don’t grow at all. They survive by becoming dor-mant, or produce structures (usually seeds) that are dormant, and very desicca-tion tolerant! So, how could it be possible to have crop plants that are verydrought tolerant? Dormant crops won’t do the trick. How are naturally droughttolerant plants able to be productive in a drought environment? Drought is ameteorological term referring to an environment receiving an amount of rain-fall deficient from an accepted norm (Passioura, 1996; Fischer and Turner,1978). However, one can consider that any plants growing with less than anoptimum amount of available moisture are also under drought stress. Naturalenvironments where moisture is consistently too low to produce crops withouta fallow period or irrigation can be considered arid. Plants that grow in arid re-gions or experience drought conditions, receive at least some water. Therefore,plant species that are adapted to these hot dry climates have evolved to exploitthe limited water that is available for growth. Fisher and Turner (1978) havereferred to the ecological classification of plants that are adapted to utilize lim-ited amounts of moisture into two groups, the aridopassive and aridoactiveforms. The aridoactive group is composed mainly of perennial succulents,shrubs and trees, so agricultural crops are confined mainly to the aridopassiveplants.

Several authors have described the mechanisms by which crop plants in aridclimates utilize limited available moisture (Passioura, 1996; Turner, 1986; Ev-ans, 1994; Passioura, 1986; Jones et al., 1981; Evans, 1993; Passioura, 1994;Fischer and Turner, 1978). The major factors include phenological character-istics of the plant and traits that strongly influence water loss and gain(Passioura, 1996; Jones et al., 1981). There also have been serious consider-ations of using natural xerophytes or halophytes as sources of food, fiber or en-ergy (O’Leary, 1984; Nerd et al., 1991; Nerd et al., 1993). However, theacceptance of new crops species faces serious economic and cultural con-straints (Janick, 1999). Therefore the genetic manipulation of important cropplants for the ability to be more productive in drought environments remainsan essential goal of agricultural research. Because of the tremendous natural

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variation that exists in native plants for phenological characteristics, we haveknown for considerable time (not 5000 years though) that genes capable ofcontrolling them exist. However, the power of molecular genetics to identifyand isolate specific genes has not been brought to bear on these traits. This islargely because the species that we normally associate with such genes are notreadily amenable to molecular genetic approaches. O’Toole (1989) has dis-cussed the use of molecular marker technology to assist breeding for suchcharacters, but concluded at that time that genetic engineering such traits maybe years into the future.

Now, perhaps the future has arrived, and model plant systems, especiallyArabidopsis thaliana, may be more useful to identify drought tolerance genesthan previously thought. One could think of many of the special genetic char-acters of native drought tolerant species not so much as the result of com-pletely unique genes, but more as the special way in which genes of a muchmore generic nature are used. That is, by expressing the same genes, or slightlydifferent forms of genes, in a somewhat different manner, special characteris-tics are produced. This may not be so far from reality. In fact, Somerville(2000) argues that the evolutionary time between the appearance of floweringplants and the present has been so short that most plant genes have not di-verged greatly. They hypothesize that the majority of phenotypic differencesbetween plants have arisen by specialized expression programs that control theeffects of genes on phenotype (Somerville, 2000). From this view, most of oneplant’s genes are pretty much another plant’s genes. What is important is theparticular subclass of genes (regulatory genes) that control when and how theothers are used. To see this more clearly, it may be useful to imagine Beetho-ven’s 5th Symphony versus the Rolling Stones’, Can’t Get No Satisfaction.They both use basically the same notes, A through G. It is how they are ar-ranged and the timing of their playing that produces such different results. Thisconcept holds out the hopeful possibility that any plant’s genes are for hire andcan be used successfully in other plants. There is much experimental evidenceto support this (see Holland, 1999 and references therein). Yet it is also clearthat this will not be universally true because of incompatible gene product in-teractions between species (Martin, 1999).

As for all of the genetic manipulations that we will describe in this chapter,initial tests of their impact on drought tolerance can be performed usingArabidopsis as a model, but the ultimate usefulness of the genes in questionrests with their use in crop species. The ability to manipulate crop plants bythis approach will be determined largely by two factors. These are: (1) the abil-ity of Arabidopsis genes to function ectopically in another plant (crop) species;and (2) in case of failure of the first, our ability to use sequence informationfrom Arabidopsis genes and other model systems to identify functional coun-terpart genes in the species of interest (bioinformatics). The emerging field of

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bioinformatics is allowing us to identify, more and more easily, genes thathave homologous functions in different species. Therefore, if a gene from spe-cies A does not function in species B, we eventually should be able to identifythe species B homologue of that gene, and make appropriate expression orfunctional alterations to achieve our phenotype goals. Even if species A and Bare taxonomically distant and the gene in question is too different betweenthem to recognize, homologous gene identification may be achieved by a sortof island hopping, using species that are taxonomically in between A and B.One could carry out a sort of gene by gene recapitulation of phylogeny. In fact,it is expected that phylogenetic comparisons of gene homologues will teach usmuch about how genes undergo subtle changes in their sequences that controlimportant phenotype changes (Holland, 1999). The identification of functionalcounterpart genes from different species by bioinformatics is being greatly fa-cilitated as gene sequence libraries are compiled for crop plants (dbEST). Un-derstanding the relationship between degree of sequence identity and functiondivergence of genes from different species may also be greatly facilitated inthe near future by determining the phenotypes of mutants in genes of similarsequence from different species.

The exciting years ahead will tell if our newly gained abilities to identifyand manipulate genes and apply them to a goal of achieving drought tolerantcrops represents an oasis in the desert or just a shimmering mirage.

ARABIDOPSIS, THE MODEL,AND THE GENOMICS REVOLUTION

For the past two decades a small plant (Arabidopsis thaliana) from the mus-tard family, increasingly has become a facile and favorite model organism inplant biology research. With the advent of the genomics revolution, Arabid-opsis research has increased explosively. The identification of genes that con-trol or influence numerous plant characteristics and processes has reached afrenetic pace. Several developments are responsible for this rapid progress, es-pecially the availability of a genome sequence that is rapidly nearing comple-tion and thus is allowing the positional cloning of genes with greater ease.Further, the publicly accessible collections of tagged mutants and their corre-sponding DNA pools are rapidly increasing in size, facilitating both forwardand reverse genetic screens (Weigel et al., 2000; Krysan et al., 1999). In fact,with the potential development of a virus (tobacco rattle virus) expression sys-tem in Arabidopsis, fast-forward genetics (Baulcombe, 1999) would be cou-pled with the advantages of Arabidopsis. With the coming availability ofpopulations of insertion tagged mutants in Arabidopsis that virtually saturatethe genome (Weigel et al., 2000; Koornneef et al., 1991; http://stress-genomics.org), reverse genetics eventually will allow the observation of phenotypes re-

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sulting from mutation of every gene in the genome. Owing to these and manyother important advantages, Arabidopsis has been used as a genetic tool to se-lect for mutants affected in virtually all aspects of growth and development(http://Aims.cps.msu.edu/aims), including tolerance to abiotic stresses (Zhu,2000). Results obtained from selected mutations and the cloning of the corre-sponding genes responsible for changes in salinity tolerance (Liu and Zhu,1998; Liu et al., 2000; Zhu, 2000) have been especially informative to our un-derstanding of osmotic aspects of desiccation tolerance.

Largely overlooked in the enthusiasm to utilize the Arabidopsis system hasbeen drought stress tolerance as it is viewed by crop scientists. This is undoubt-edly due, at least in part, to the overwhelming opinion that drought itself is acomplicated environmental syndrome not easily duplicated in the lab or evenin the field. Also, even though selection of Arabidopsis plants in the lab for tol-erance at low tissue water potential may be feasible, such tolerance generally isassociated with highly reduced productivity, making most such model selec-tion systems unattractive to crop scientists. But perhaps an even greater hin-drance may be the long-held view that drought tolerance that could retain cropproductivity is genetically complex, since in nature it is substantially con-trolled by phenological characteristics having to do with either outright escapefrom or at least avoidance of drought stress. This has made it seem quite un-likely that drought tolerance could be significantly impacted by single genesand certainly could not be examined in a laboratory setting. Upon close inspec-tion of the torrent of mutants and genes being identified in Arabidopsis, onecould surmise that this indeed may not be the case.

In this chapter we will discuss the possibility of using Arabidopsis mutantsand genes to study their potential for manipulating the ability of plants to growand produce a harvestable product (seed or fruit) by avoiding or escapingrather than tolerating the deleterious effects of drought. We will outline the ba-sic characteristics that are understood to control avoidance of drought stressand subsequently discuss numerous known Arabidopsis mutants and/or genesthat are related to these characteristics. We want to emphasize, however, thatwe have not exhaustively reviewed all relevant genes, and the discovery ofnew Arabidopsis mutants/genes is progressing very rapidly. Certainly addi-tional relevant genes, even beyond the categories that we have listed, will soonbe discovered. These discoveries should provide an even greater wealth of ge-netic material to examine with respect to their impact on drought escape andavoidance.

A TRIP TO ARIZONA, OR ALMOST ANYWHERE IN AUSTRALIA

Our concepts of how plants survive and grow in arid environments haveflowed from our observations and studies of the flora of these seemingly hos-

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tile places. These dry desert climates occur at many sites around the world, butnote from our bibliography the disproportionate number of Australian scien-tists who study them. We owe much to the long history of dedication by Aus-tralian (and of course some others) scientists to the study of arid plant biology.

Drought escape and avoidance can be distinguished from true tolerance bythe absence of occurrence of a significant decline in tissue water potential(Jones et al., 1981). Although mentioned as drought tolerance with high waterpotential by Turner (1986), this is essentially avoidance as put forth long agoby Levitt (1972) and more recently described by Evans (1993). This differsfrom escape in that the latter derives from either phenological development orenvironmentally-induced plasticity that attunes the timing of the plant’s lifecycle with available moisture so that the plant is dormant (as a seed or dormantplant) during periods of low moisture availability (Turner, 1986). In fact, es-caping drought stress by shortening or “timing” the plant’s life cycle repre-sents the best form of yield tolerance known (Turner, 1986; Evans, 1993). Thisis emphasized by the observation that the greatest reductions in plant produc-tivity result when drought occurs during anthesis (Passioura, 1994). Thesefacts are elegantly recounted in other reviews (Passioura, 1996; Turner, 1986;Evans, 1994; Passioura, 1986; Jones et al., 1981; Evans, 1993; Passioura,1994). Although Evans professes in his preface the hope of a synergistic inter-action between the old world of traditional agriculturists and crop physiolo-gists and the emerging world of “Drosophila and Arabidopsis,” it seems thatthe wealth of the Arabidopsis world as it applies to many goals of agriculturistsis still, some 10 years later, far from being realized. We attempt here to revealsome of this genetic wealth of Arabidopsis, hoping that open-minded and ea-ger agriculturists, crop physiologists, and plant breeders will spend it on thegoal of drought tolerance, as well as other traits of interest to agriculture.

Before we begin to outline the application of Arabidopsis genetics to spe-cific aspects of drought avoidance and escape, we want to emphasize two im-portant realizations in plant biology that are allowing the merger of the worldsof Arabidopsis and traditional agriculture and crop physiology. First, biotech-nology, or genetic engineering technology, now affords us the ability to trans-fer genes from any organism to any other organism, where transformationtechnology is established (this now includes all major crop plants). Second,genomics and bioinformatics is revealing the fact that between organismsthere is a surprisingly close relatedness of the structures and sequences ofgenes. As indicated earlier, this bioinformatics approach is allowing us toidentify functionally counterpart genes between organisms. For example,NPR, ETR, and TOLL are a few of the many genes that function in disease re-sistance and reproductive development and are sufficiently similar in sequenceto recognize between species (Geisler et al., 1992; Cao et al., 1997; Wilkensonet al., 1995; Schaller and Bleecker, 1995; Medzhitov et al., 1997). As we will

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see later, many genes involved in flowering also have highly conserved se-quences between species. This means that genes discovered in Arabidopsismay be directly transferred to crop plants or may provide useful “leads” to dis-cover their functional counterparts in crop species by using the rapidly ex-panding gene sequence databases (dbEST). With these possibilities in mind,we will now examine several specific traits related to drought escape/avoid-ance and discuss presently and potentially identified genes in Arabidopsis thatcould control such traits.

Escaping Drought by Timing of the Life Cycle

As many authors have indicated, the most crucial trait in determiningdrought escape is the time of flowering (see Passioura, 1996; Turner, 1986;Evans, 1994; Passiouira, 1986; Jones et al., 1981; Evans, 1993; Passioura,1994). Flowering signifies the beginning of the completion of the life cycleand the development of reproductive structures (seeds and fruits) that are theusual components of yield. Thus, attainment of flowering and production ofsubsequent harvestable yield before stress becomes too severe allows escape.Although selection for flower timing and other avoidance and escape charac-terization has been used in breeding for drought tolerance in some crops(Duvick, 1992; Dwyer and Tollenaar, 1989; Pantuwan et al., 1996; Garrity andO’Toole, 1995; Champoux et al., 1995; Dingkuhn et al., 1991), the genes in-volved were not identified and thus could not be used directly or indirectly tomanipulate other species. Selection for such traits by necessity is then per-formed on each crop independently.

There is a plethora of information on genes that control flowering timing(transition to flowering) in Arabidopsis. Genes involved in floral induction inArabidopsis participate in three parallel signal transduction pathways that ap-parently interact with each other (Sheldon et al., 1999; Koornneef et al., 1991;Levy and Dean, 1998; Pineiro and Coupland, 1998; Samach and Coupland,2000). One pathway affects flower timing independent of environmental cuesand may be controlled by the hormone gibberellic acid. Effects on flower tim-ing by genes in the other pathways are influenced by photoperiod and vernal-ization, respectively (Koornneef et al., 1998; Devlin and Kay, 2000). Longdays, a cold period, and gibberellic acid all stimulate flowering in Arabidopsis.The identity of genes that cause both early and late flowering have been re-ported (Levitt, 1972; Levy and Dean, 1998; Pineiro and Coupland, 1998;Samach and Coupland, 2000; Michaels and Amasino, 1999) as well as genesthat control many aspects of floral development and structure (Riechmann andMeyerowitz, 1997; Weigel, 1995; Schultz and Haughn, 1993). Of particularinterest to drought escape would be genes that promote early flowering. Suchgenes when mutated should lead to late flowering, and several examples of

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these have been identified (Michaels and Amasino, 1999; Riechmann andMeyerowitz, 1997; Putterill et al., 1995; Huala and Sussex, 1992). Some ofthese have been tested in transformation experiments, and it is clear that al-tered expression of flower timing genes in Arabidopsis can dramatically affectthe onset of flowering (Michaels and Amasino, 1999; Putterill et al., 1995;Nilsson and Weigel, 1997). The leafy mutant fails altogether to produce nor-mal floral structures. When the LEAFY gene is overexpressed, flowers areformed immediately after germination without any environmental signal re-quired (Nilsson et al., 1998), representing the extreme case of alleviating floraldevelopment repression. The Arabidopsis LEAFY gene has also been used intransgenic experiments in unrelated species such as aspen where it also wasable to affect flowering time (Rottmann et al., 2000; Weigel and Nilsson,1995). In fact, striking similarity between sequence and function of floweringgenes in Arabidopsis and Antirrhinum majus suggests that the genes control-ling flowering time may be highly conserved across the plant kingdom (Weigel,1995).

Two other considerations concerning the developmental program of plantsregarding flowering and drought escape merit attention. The first involves theplasticity of the escape mechanism (Angus and Moncur, 1977; Turner et al.,1978). It may be additionally advantageous to induce (early) flowering at theonset of stress thereby maximizing the time that the plant spends in the vegeta-tive growth phase prior to entering the reproductive stage. This could, with aproper genetic background, increase the reproductive capacity (yield) by fullyutilizing available moisture to provide a larger, more robust, photosyntheticbase for floral development. Since several promoter elements that control re-sponsiveness to desiccation and other drought-related signals have been de-scribed (Hasegawa et al., 2000), the use of appropriate early-flower-timinggenes with a drought inducible promoter is feasible and may lead to a plant thatis attuned to escape a pending drought episode by flowering and completingreproductive growth in response to the onset of stress. Of course this strategydepends on the nature of the drought cycle environment. Under certain condi-tions the opposite strategy of delayed flowering to “ride out” reduced moistureperiods may be more effective.

The second consideration that may increase the effectiveness of phenologicaldrought escape is the amount of vegetative growth that occurs prior to the on-set of stress. Vegetative growth may be maximized prior to stress and subse-quent induced flowering by the use of genes that allow rapid germination.Mutants that affect seed dormancy have been discovered from many species ofplants, including Arabidopsis (Bewley, 1997). The aba, abi (Koornneef andKarssen, 1994), and rdo (Léon-Kloosterzeil et al., 1996) mutants that are defi-cient and sensitive to ABA are good examples of genetic alterations that im-pair dormancy. The ABI3 and ABI1 genes have been cloned and encode a

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transcription factor and protein phosphatase, respectively (Giraudat et al.,1992; Leung et al., 1994). As we will discuss later, appropriate genes fromArabidopsis also may be modified genetically to allow rapid vegetative growthafter germination, during a period of ample soil moisture followed by the in-duction of flowering when soil moisture decreases. Rapid growth allowing in-creased soil coverage by foliage has been associated with more efficient wateruse in moisture limited environments (Passioura, 1986). We will discuss laterseveral genes that may affect vegetative growth rate.

Drought Avoidance Through Reduced Water Loss

Stomatal Characteristics

Although many factors influence the loss of water from plants, stomatalmorphology and behavior contribute by far the greatest to overall control ofwater movement out of the plant. It is well established that a very close rela-tionship exists between the amount of water transpired and the amount of bio-mass produced by plants (Hanks, 1983). In this respect, restricting the amountof water that is transpired in order to avoid drought stress suffers from a certainaspect of diminishing returns. Nevertheless, particular behavior of stomatasuch as mid-day closure to avoid the highest degree of evaporative demand is acommon feature of plants adapted to arid environments (Tenhunen et al.,1987; Schulze and Hall, 1982). We are unaware of particular genes that controldiurnal behavior of stomatal at this time. However, genes involved in control-ling circadian characteristics have been recently identified in Arabidopsis(Somers et al., 2000). It is also quite likely that mutants for stomatal behaviorhave not been vigorously sought. It certainly may be feasible to screen for suchmutants in Arabidopsis by providing a toxic gas (e.g., SO2 or O3) only duringthe period when the stomata are desired to be closed (or at least partiallyclosed). Another possible way to screen for mutations affecting stomatal func-tion was demonstrated by Raskin and Ladyman (1988). Using infra-red pho-tography, they found that leaves with more closed stomata can be distinguishedfrom those with more open stomata.

Some mutations that affect stomatal behavior are known. Most notable arethe mutants that are impaired in metabolism or responsiveness to ABA. Be-sides the well-known mutants of this sort in tomato and other species (Bray etal., 1999; Taylor et al., 1988; Raskin and Ladyman, 1988; Nagel et al., 1994;Neill and Horgan, 1985), such mutants also have been described in Arabidopsis,and a number of the genes controlling the ABA responsiveness of stomatahave since been cloned (Leung et al., 1994; Geisler et al., 1998; Koornneef etal., 1984; Finkelstein and Somerville, 1990; Schnall and Quatrano, 1992;Vartanian et al., 1994; Cutler et al., 1996; Pei et al., 1998; Li et al., 2000). Un-der the control of appropriate promoters, these genes might be used to allow

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the opening of stomata only under favorable conditions. Alternatively, oncemore components of the stomatal signalling mechanisms are discovered, vari-ous options towards genetic manipulation of stomatal behavior will appear.

Mutations affecting the formation, distribution and density of stomata inArabidopsis also have been described. The multicellular stomatal structure de-velops from precursor meristemoids (Larkin et al., 1997; Geisler et al., 1998).The mutants, too many mouths (tmm), four lips (flp), and r558 significantly af-fect the developmental fate of the meristemoids and thus the density of stomataon the leaf surface (see Larkin et al., 1997; Yang and Sack, 1995). These mu-tants could be used in model experiments to examine the relationships betweentranspiration, drought avoidance, and growth. An interesting mutation affect-ing the response of stomata to light has also been described in Arabidopsis(Lascève et al., 1997), suggesting additional stomatal function mutants couldbe isolated.

Leaf Shape and Area

During drought, plants exert control over leaf area as another mechanism ofavoidance (Passioura, 1994; Fischer and Turner, 1978). Reduction of overallleaf area greatly diminishes the use of the soil water supply (Briggs and Shantz,1914; Fischer and Turner, 1978). Many processes can contribute to leaf area re-duction, from leaf excision to reduced leaf expansion and altered leaf shape andmorphology (Fischer and Turner, 1978). These avoidance characteristics arealso manifested as permanent adaptive features of xerophytic plants, reachingfamiliar extremes in cacti and other plants where leaves are reduced to stem orspine-like structures (Fischer and Turner, 1978; Herbert, 1983).

Many mutations in genes of several plant species including Arabidopsis af-fect leaf structure and morphology, and several in Arabidopsis have profoundaffects on leaf area (see Berná et al., 1999 and references therein). Most of theobservations regarding these mutations have been focused on developmentalaspects of the leaf, rather than on rates of enlargement. However, several geneshave been identified that control the cell division cycle in plants (Jacobs,1997), and sometimes manipulation of such genes can dramatically affectgrowth rate and size of leaves (Hemerly et al., 1995). Since leaf area also is ex-pected to affect strongly reproductive yield, these specific genetic alterationsin Arabidopsis afford us the opportunity to examine the result of very specificmorphological changes in leaves on both water use and reproductive yield inisogenic backgrounds.

Some other specific leaf mutations are of particular interest with respect todrought avoidance. The rot3-1 mutant of Arabidopsis has defective polar elon-gation of leaf cells, and the gene responsible (a cytochrome p450) causes elon-gated leaves to form when overexpressed (Kim et al., 1999). The elongata

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mutants produce even more narrow leaves approaching the spine-like shapefound on xerophytic plants (Berná et al., 1999). In addition, many mutants pro-duce leaves that are thicker and more isodiametric than normal (Berná et al.,1999). Combinations of these characteristics can be found in some instancessuch as revoluta or argonaute mutants (Bohmert et al., 1998), or even more ex-treme leaf shapes might be produced by combining these types of mutations indouble or triple mutants. Another very interesting leaf phenotype from thestandpoint of drought avoidance is that of the curled mutants. Ultracurvata(Berná et al., 1999) has a leaf lamina curled downward, potentially creating ahighly humid microenvironment for stomata. This would represent a featurequite similar to that seen in many plants that exhibit leaf rolling (Dingkuhn etal., 1989). Additional mutants that exhibit highly curled leaves such as curlyleaf and tousled have been described, and genes controlling these phenotypeshave been isolated (Roe et al., 1993; Goodrich et al., 1997), making it possibleto test ectopic function in other species. Some genes such as KNOTTED-1 typecan cause the formation of succulent-like lobed leaves when overexpressed(Lincoln et al., 1994). The effect of such leaf morphology changes on bothdrought avoidance and biomass productivity could easily be examined inArabidopsis. In addition to genes that control specifically leaf morphology,other mutations and genes have been identified that generally control thegrowth of the root or shoot. Many such mutations, often categorized as dwarfsthat have impaired synthesis or perception of growth-mediating hormoneshave been described in Arabidopsis (Kurata and Yamamoto, 1998; Heddenand Kamiya, 1997; Wilson et al., 1996; Peng et al., 1997; Yang et al., 1999;Stirnberg et al., 1999; Choe et al., 1999; Riou-Khamlichi et al., 1999; Noguchiet al., 1999; Halliday et al., 1996). Many of these mutations are pleiotropic af-fecting other plant characteristics, but some are rather confined in their affectsto shoot growth (Torii and Deng, 1995). These may prove useful, when manip-ulated for timed or environmentally-cued expression, to restrict shoot growthunder periods of rapidly diminishing moisture.

Genetic engineering to allow the expression of these altered leaf pheno-types only in response to decreasing soil moisture may allow some quiteintriguing experiments to be conducted, by combining these types of charac-teristics with altered flowering time phenotypes. This would allow the extraor-dinary opportunity to examine, in an isogenic context, the effects on droughtescape and avoidance abilities of very complex phenological and morphologi-cal characteristics that are otherwise found differing only between plants withdrastically different genetic backgrounds.

Reflection of Radiation

Water loss from plant surfaces also is affected significantly by incident ra-diation (Evenari et al., 1971; Kozlowski, 1976; Begg and Torsell, 1974; Moo-

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ney et al., 1977; Orshan, 1963). When stomata are partially closed, high leaftemperatures caused by excessive absorbed radiation can lower water-use effi-ciency (Jones, 1979). A number of specific adaptive features used by plants toreduce incident radiation could be addressed by using Arabidopsis genetics.Leaf angle or other architectural features of leaves (Berná et al., 1999), hairi-ness (Szymanski et al., 1998a; Larkin et al., 1996; Perazza et al., 1999;Szymanski et al., 1998b; Schnittger et al., 1999; Oppenheimer et al., 1997;Payne et al., 1999), and waxiness (Aarts et al., 1995; Negruk et al., 1996;Hannoufa et al., 1996; Lemieux, 1996; St. Pierre et al., 1998; Xia et al., 1997;Benveniste et al., 1998; Millar et al., 1999; Todd et al., 1999) of the leaf surfacecan increase the reflectance properties of leaves; such traits have been geneti-cally analyzed in Arabidopsis with several genes affecting these propertieshaving already been isolated. Many drought avoiding plants employ thesestrategies, and in many instances they are induced by water scarcity. Again, theplasticity of these traits could affect relative productivity when stress is or isnot present. The use of stress-responsive promoters (Hasegawa et al., 2000)may allow such plasticity in trans-gene approaches.

Trichome formation in Arabidopsis has been studied extensively, and manymutants have been described affecting trichome density and morphology(Chien and Sussex, 1996; Hülskamp et al., 1994; Larkin et al., 1996; Marks etal., 1991) including several for which the genes have been cloned (Szymanskiand Marks, 1998; Millar et al., 1999; Schnittger et al., 1999; Oppenheimer etal., 1997). The GL1 gene from Arabidopsis is a good example of a molecularlead that can eventually allow ecotopic function of a gene from one species toanother. Overexpression of GL1 in Nicotiana tabacum did not cause supernu-merary trichome production. However, another related gene (MIXTA) belong-ing to the same class of myb transcription factors from Antirrhinum majus,when overexpressed in Nicotiana tabacum, did result in increased density oftrichomes (Payne et al., 1999). This observation illustrates the power of genomesequence comparisons (bioinformatics). Although in its infancy, bioinfor-matics has the potential to allow the identification of the counterpart genes(orthologues) from different species. As indicated earlier, this may be neces-sary if a gene controlling an important trait is found in Arabidopsis (or anyother plant) and is unable to function (as was found with GL1) in another spe-cies of interest because there has been insufficient conservation of compatibil-ity with interacting gene products in the recipient species.

Avoiding Drought Through Alterations in Water Uptake Characteristics

Root Characteristics

Besides controlling the degree of water loss, plants may avoid droughtstress by exhibiting enhanced ability to extract soil moisture (Passioura, 1994;

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Hackett, 1969). This is usually accomplished by changing the structure and/orfunction of roots. Root architecture has a dramatic influence over the ability ofplants to extract soil water (Passioura, 1994; Kummerow, 1980; Taylor, 1980;Passioura, 1983; Passioura, 1981; Derera et al., 1969). The co-ordination ofroot development with the pattern of rainfall and soil type also greatly affectsability to exploit available water from the soil for growth (Passioura, 1994;Passioura, 1983). Some aspects of better soil water extraction capability re-main somewhat mysterious, as with observed differences between sorghumand sunflower (Passioura, 1986). Differences in root pattern can be observedbetween these two species but cannot be confidently associated with water ex-traction ability because of the disparate genetic backgrounds. Root morphologyand architecture mutants of Arabidopsis could be used in a more controlledfashion to evaluate specific relationships between root characteristics and wa-ter extraction abilities since the root mutants of Arabidopsis exist in isogenicbackgrounds. In addition, Arabidopsis may provide an extremely facile systemfor selecting mutations (and subsequently genes) with specific root character-istics. It should be possible to select for deep root growth mutants using nutri-ent gradients or reverse toxin gradients, selecting for plants with roots thatgrow rapidly toward nutrients or away from toxins. Very often drought avoidingplants maintain a very large root/shoot ratio and can in some instances producea root mass nearly 10 times the shoot mass (St. Pierre et al., 1998). The root/shoot ratio also can be affected dramatically by the environment (Quisenberryet al., 1981; Blum, 1988). This characteristic increases the phenological plas-ticity of plants not only to environmental cues associated with drought but alsoto nutritional deficiency (Blum, 1988). For instance, root/shoot ratios increasein response to PO4 starvation (Raghothama, 1999). In this regard, more sophis-ticated technical opportunities may be brought to bear using Arabidopsis. Itmay be possible to identify genes that control root/shoot ratios using PO4 starva-tion induction. Genes induced by PO4 starvation that are involved in control-ling PO4 acquisition have been identified (Raghothama, 1999). The expressionof these genes, and others involved in relative root/shoot growth, must be re-sponsive to a low PO4 environment. This perception is subsequently trans-duced to activate genes controlling PO4 acquisition, and very likely root/shootgrowth also, since these signal pathways most likely overlap. Fusion of a lowPO4-inducible promoter to a visible marker gene such as LUC (Raghothama,2000), allows the very efficient selection of low-PO4 response mutants usingvery large populations of small seedlings without actually determining theroot/shoot ratios. Mutants can then be tested for changes in relative root/shootgrowth.

Many Arabidopsis mutants with altered root characteristics have alreadybeen described (Schnittger et al., 1999; Oppenheimer et al.,1997; Payne et al.,1999; Watson et al., 1998; Cristina et al., 1996; Masucci and Schiefelbein,

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1994; Schiefelbein and Somerville, 1990; Oyama et al., 1997). Some of thesecould have profound implications for drought avoidance. Especially mutantsand the corresponding genes that affect root growth independently of shootgrowth may, under conditions of appropriately controlled expression, have alarge impact on the ability to extract soil moisture. The CYC1 gene is such anexample, as it causes increased, but normal root growth when ectopically ex-pressed under control of the cdc2a promoter (Doerner et al., 1996). In addition,the roots of these transgenic plants even more dramatically increase theirgrowth in response to IAA by greatly increasing lateral root growth and devel-opment (Doerner et al., 1996). Mutations in the Arabidopsis TTG or GL2 genes(Dolan, 1996) and expression of the yeast CDC25 gene in plants (McKibbin etal., 1998) control the development of root epidermal cells into root hairs, andthereby can have dramatic impacts on the number of root hairs. Such mutantsalso may have significantly altered water uptake characteristics. Since they re-sult from single genetic changes, they may be useful to further describe the roleof root hairs in different environments.

Hydraulic Conductivity

Many authors agree that resistance of water flow through the plant, particu-larly the root system, plays an important role in drought stress (Kaufmann,1981; Jones et al., 1981; Taylor, 1980; Paleg and Aspinall, 1981). Several im-portant questions remain unanswered or controversial such as the relative im-portance of hydraulic conductivity of shoots and the basis of genetic variationfor conductance (Jones et al., 1981; Taylor, 1980; Paleg and Aspinall, 1981). Itis generally agreed, amongst earlier investigators that the morphology of thewater conducting tissue (xylem vessels) has the greatest influence over hy-draulic conductivity of the plant (Taylor, 1980; Rieger and Litvin, 1999). Im-portant factors also include diameter of vessels and amount of vasculaturewithin the root or stem. The biochemical composition of cell walls such aslignin content may also influence water flux. Several mutants of Arabidopsishave been described that exhibit altered vasculature (Hobbie and Estelle, 1994;Scheres et al., 1995; Turner and Somerville, 1995; Turner and Somerville,1997; Zhong et al., 2000). A number of genes controlling both morphology ofthe vascular system (Taylor et al., 1999; Hardtke and Berleth, 1998; Zhong etal., 1999) and cell wall composition (Chapple and Carpita, 1998; Humphreyset al., 1999; Marita et al., 1999) have been isolated and described, but the influ-ence of such mutations on water uptake flux have not been investigated.

The exact pathway that water follows during absorption by roots and move-ment through the plant has always been considered somewhat uncertain sincemultiple pathways are available. Water uptake by plants and transport acrossthe root radius can be mediated by one of three parallel pathways: the

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apoplastic, symplastic or cell-to-cell (transcellular) pathway (Kjellbom et al.,1999; Steudle and Peterson, 1998). Transcellular movement of water has beenhistorically thought to occur via transmembrane diffusion. The identificationof plant aquaporins, together with evidence that they make up 5 to 10% of totalprotein in membranes, has opened important new avenues of thinking aboutpossible modes of regulation of both inter- and intracellular water transport(Johansson et al., 1996; Chrispeels et al., 1999). It is now generally acceptedthat diffusional water permeability is not the primary contributor to membranehydraulic conductivity. Rather, water transport is mediated predominantly bywater-specific channels called aquaporins (Maggio and Joly, 1995; Steudleand Henzler, 1995; Henzler and Stuedle, 1995; Chrispeels et al., 1999; Kjellbomet al., 1999). Plant aquaporins (Agre et al., 1993; Chrispeels and Agre, 1994),located both in the plasma membrane and tonoplast, facilitate the passivetransport of water down a water potential gradient (Maurel, 1997; Chrispeelset al., 1999; Kjellbom et al., 1999; Schnaffer, 1998). These aquaporins aremembers of the major intrinsic protein superfamily (MIP) (Maurel, 1997;Chrispeels et al., 1999; Kjellbom et al., 1999; Schnaffer, 1998), so named forthe archetype protein identified in the bovine lens membrane (Gorin et al.,1984). CHIP (channel forming integral protein) 28 was the first characterizedto have water transport activity (Preston et al., 1992). Today, it is known thatMIP sequences and function are conserved from bacteria to mammals (Chrispeelset al., 1999; Kjellbom et al., 1999). Plant aquaporins currently are divided intothree discrete families, based on function and bioinformatics: PIPs (plasmamembrane intrinsic proteins), TIPs (tonoplast intrinsic proteins), and NLMs(nodulin26-like MIPs) (Maurel, 1997; Kjellbom et al., 1999; Schaffner, 1998).There are at least 30 known aquaporin encoding genes within the Arabidopsisgenome, and 12 of these appear to encode PIPs which should provide the majorpathway for axial water movement into the vascular system of roots, therebycontributing most to the control of hydraulic conductivity. At this time the con-tribution of each PIP gene to water flux through plant tissue is unknown. How-ever, genetic manipulation of water channel gene expression has demonstratedthe importance of these genes to plant water relations (Johansson et al., 2000).Because there are so many PIP isoforms encoded in the genome, it is verylikely that different PIP genes are expressed in separate tissues at specific timein plant development. In the future, reverse genetics approaches to identify spe-cific PIP gene mutations should further clarify the role of individual PIP genes inthe ability of plants to grow and be productive in drought environments.

An Even More Exotic Genetic Future

We indicated earlier that we expect many more genes with potential impacton drought tolerance to be identified in the future using Arabidopsis and other

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model organisms. Some of these will be unexpected and even unexplainableby today’s understanding. We can try to glimpse a little into the future withsome intriguing hints from today’s discoveries. As an example, we cite the in-teresting developments with genes that control cell division and expansion. Itis well known that an important cellular response of plants to desiccation is analtered pattern of cell division and expansion. Both desiccation and salinitystress cause plant cells to disrupt the normal cycle of cell expansion and divi-sion resulting in smaller cells (Bressan et al., 1990). It seems likely that percep-tion of osmotic stress in plants triggers a disruption (resetting) of this controlmechanism allowing cells to enter mitotic division at a smaller size. Genesgoverning cell size homeostasis have been well-studied in yeast where theWEE1 gene product blocks entry into mitosis (Lundgren et al., 1991), and thephosphatase CDC25 stimulates cell division by dephosphorylating CDK1(Lundgren et al., 1991; Russell and Nurse, 1987). A similar genetic checkpointtriggering cell division at a certain cell size has been observed in plants(Lundgren et al., 1991; Armstrong and Francis, 1985). Also, mitotic regulationof plant cells in culture has been associated with phosphorylation of CDKs(Zhang et al., 1996). A homologue of the WEE1 gene has been identified inplants and appears to play a role in the control of cell division during endo-reduplication in endosperm cells (Sun et al., 1999). Recently, the Arabidopsishomeodomain-leucine zipper transcription factor HB7 was found to causeslow growth when overexpressed (Soderman et al., 2000). Because this gene isalso induced by desiccation stress (Soderman et al., 1996), it may be part of animportant control pathway connecting reduced growth to osmotic stress sig-nals. These cell cycle control genes may constitute a rheostat mechanism thatadjusts cell division and growth rates in response to the changes in the environ-ments such as nutrient availability or osmotic stress. Once all of the plant genesthat control the cell growth response to stress are discovered, our ability to ma-nipulate productivity under stress conditions could improve dramatically.Eventually it may be possible to uncouple the connection between osmotic ad-justment and slow growth, which has been pointed out to be a crucial factor inproductivity under osmotic stress (Bressan et al., 1990).

Getting More from Less?

Regardless of the occurrence of environmental stress or not, the most im-portant factor governing the impressive increases in crop yield during the pastcentury has been genetic and cultural changes that control the proportion of theplant that comprises the harvested product (Constable and Hearn, 1978;Turner et al., 1989). In fact, it is instrumental to consider that the moisture in-put (rainfall) to a crop is fixed usually within narrow boundaries, and the effi-

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ciency of water use, as indicated earlier, is difficult to alter. It follows then,from the often cited relationship of these parameters to yield:

Y = T � WUE � HI

Y = yield; T = transpiration; WUE = water-use efficiency; HI = harvest in-dex that the only way to have a major impact on yield is to manipulate the har-vest index. However, this calculation of yield does not consider growth andmaintenance respiration which may also vary between genotypes (Day et al.,1985). A number of Arabidopsis mutants exhibiting altered respiratory charac-teristics have been isolated (Somerville and Ogren, 1981; Somerville andOgren, 1979). With appropriate selection schemes, perhaps using respirationinhibitors, it certainly could be possible to identify Arabidopsis mutants withaltered respiratory efficiencies that impact HI. Nevertheless, there have beenmany successful breeding approaches to improving HI, even without consider-ing the respiration issue, and some mutations and corresponding genes inArabidopsis appear to be applicable. Several loci were associated with seedsize in Arabidopsis (Alonso-Blanco et al., 1999). Even though this trait ap-pears to be controlled by several genes, mutations in a single locus have beenfound to alter seed size significantly (J.K. Zhu personal communication). Wehave also found mutants among T-DNA tagged populations of Arabidopsis,with dramaticaly increased biomass of the inflorescence compared to the vege-tative portion of the plant (Bressan et al., unpublished).

CONCLUSIONS

It has not been our intent to cover here all possible applications of Arabidopsisgenetics potentially affecting plant phenology and drought escape/avoidance.Our main aim has been to point out some interesting possibilities concerningthe use of Arabidopsis mutants and genes that have the potential to affect par-ticular phenological traits to study the potential impact and use of these spe-cific genes under defined drought environments. We hope that by illustratingthese possibilities that interest can be generated to conduct experiments thatcould eventually lead to the genetic manipulation (genetic engineering) ofcrops to be more reliably productive in specific arid environments already un-der cultivation (Edmeades et al., 1989). Beyond this, additional genes that arealready, or will soon be identified in Arabidopsis may be recognized by othersas potentially influential on drought adaptation in ways that we have not evencovered here.

We can foresee two distinct phases in experimental evaluation of specificgenes that might be effective in drought escape or avoidance. The first stagewould involve experiments with Arabidopsis as a model plant. Genes could be

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manipulated in Arabidopsis and the effects on productivity during specific dif-ferent patterns of moisture modeled after rainfall patterns of important regions(Edmeades et al., 1989) could be directly determined (Figure 1). In caseswhere mutants are available but the genes remain to be cloned, experimentswould be restricted to this stage. In a second phase, genes that have been iden-

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A. Wildtype

B.Transgenic

FIGURE 1. Hypothetical comparison between Arabidopsis wildtype and trans-genic lines with altered genes that control flower-time and root development.Several genes that affect these traits have been identified in Arabidopsis sothat manipulation of them through overexpression or suppression is possible.Shown is a time-line of plant development with the profile (shaded or blue) ofavailable soil moisture becoming farther from the surface. A deeper more ex-tensive root system allows moisture availability to the plant for a longer periodafter germination. Earlier flowering allows pod and seed production to beginand be completed at a time of greater moisture availability. Drawing by M.Paino D’Urzo.

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tified in Arabidopsis (or other model systems) could be tested in a model cropthat can be transformed easily such as tomato or rapeseed. Part of this stage ofexperimentation would involve bioinformatic analyses of genes that are ho-mologous (orthologues) in the model crop plants. In the end, as always, the re-sults of experimentation with model plants will need to be tested using majorcrop species.

We would end by re-emphasizing the unprecedented rapid pace of plant ge-netic research with the advent of Arabidopsis-based genomics approaches.The subject of the potential marriage of the two cultures of Arabidopsis genet-ics and crop physiology to produce crop plants able to escape drought willneed frequent updating. Realizing this, we hope that this chapter will serveonly as a new beginning of a happy and fruitful marriage.

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