crop adaptation to climate change (yadav/crop adaptation to climate change) || genetic adjustment to...

P1: SFK/UKS P2: SFK Color: 1C

BLBS082-13 BLBS082-Yadav July 12, 2011 14:31 Trim: 246mm X 189mm

Chapter 13

Genetic Adjustment to ChangingClimates: MaizeMark E. Westgate and Jerry L. Hatfield

Introduction

Climate model simulations based on IPCC emis-sions scenario A1B indicate fairly dramatic in-creases in the average air temperature and de-creases in precipitation will occur over the ma-jor maize-growing areas of the continental USwithin the next 20 years (Fig. 13.1: IPCC AR4multimodel ensemble). While the expected in-crease in atmospheric CO2 concentration willhave only modest impact on growth and wa-ter use of C4 plants like maize (Ainsworth andLong 2005), the increased prospect for more er-ratic rainfall patterns during mid-season will in-evitably lead to greater risk of yield loss due todrought when kernel number and size are beingestablished (Saini and Westgate 2000).

Drought limits the capacity toproduce and utilize photosynthatefor reproductive growth

Intensive selection for tolerance to high plantpopulation density has incrementally improvedgrain yield of maize hybrids under dryland con-ditions (e.g., Duvick 2005). Despite the appar-ent increase in “stress tolerance,” reproduc-

tive development in maize remains highly vul-nerable to soil water deficits. Lack of suffi-cient soil moisture inhibits leaf area expansionand to a lesser extent root elongation (Westgateand Boyer 1985), both of which limit canopydevelopment and potential for photosynthateproduction. Stomatal closure and leaf curling inresponse to moderate moisture deficits also de-crease the rate of photosynthesis (Boyer 1982).Growth of the female reproductive structures ofmaize [rachis, ovaries, and styles (silks)] is ex-tremely sensitive to water-deficit stress and thelack of photosynthate supply. As such, inhibi-tion of expansion growth and photosynthesisduring flower maturation (silk emergence andpollination) can cause significant yield losses.Numerous studies have shown that the yield lossis due to the failure of female flowers to de-velop synchronously with the male flowers andabortion of newly formed kernels (Westgate andBoyer 1986; Edmeades et al. 1993; Bolanos andEdmeades 1996; Zinselmeier et al. 1999, 2000).

The inhibition of photosynthesis decreasessucrose flux to the developing reproductive or-gans, which appears to trigger ovary abortion(Schussler and Westgate 1995; Zinselmeier et al.1995). Abscisic acid (ABA) levels also increase

Crop Adaptation to Climate Change, First Edition. Edited by Shyam S. Yadav, Robert J. Redden, Jerry L. Hatfield,Hermann Lotze-Campen and Anthony E. Hall.c© 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

314



GENETIC ADJUSTMENT TO CHANGING CLIMATES: MAIZE 315

Fig. 13.1. US Temperature and Precipitation Changes by 2030. The changes are shown as the difference between two 20-yearaverages (2020–2040 minus 1980–1999. (Adapted from Tebaldi et al. 2006.)

in stressed plants and may also inhibit photo-synthesis through stomatal closure (Setter et al.2001). In either case, disrupting assimilate fluxis very detrimental for ovule and seed develop-ment (Zinselmeier et al. 1999). Zinselmeier et al.(1999, 2000) demonstrated that the activity of theenzyme acid invertase, which has a central rolein providing sugars for the developing femaleflowers and young kernels, is highly sensitive toplant water deficits. The activity of the insolu-ble form of this enzyme is highly correlated withovary growth and final kernel number in well-watered and water-stressed plants, whether or notthey were supplied with supplemental sucrose(Zinselmeier et al. 2000). Such results have stim-ulated efforts to increase acid invertase activity indrought-stressed plants in an attempt to preventovary and/or kernel abortion. To our knowledge,there are no published reports confirming thatthis approach has been successful.

Andersen et al. (2002) showed the loss ofsoluble invertase activity in the pedicel tissues

of drought-stressed ovaries coincided with a de-crease in mRNA synthesis. Subsequent gene pro-filing studies, however, failed to couple changesin transcription of invertase (or starch syn-thesizing) genes within water-deficient ovarieswith the ultimate demise of ovary development(Zinselmeier et al. 2003; Yu and Setter 2003).This outcome might reflect the difficulty in doc-umenting tissue-specific and developmentallyspecific expression of these genes. But it is morelikely an indication that there are other physi-ological barriers acting in concert with the lossof invertase activity to inhibit reproductive devel-opment under stressful environmental conditions(Fig. 13.2). Studies designed to overcome thelack of assimilate supply when concurrent pho-tosynthesis and invertase activity are inhibitedby water stress clearly show that the plant doesnot mobilize stored sugars to the female flow-ers unless it is injected artificially into the stem(Zinselmeier et al. 1995, 1999). Although sug-ars normally are abundant in the stem and floral



316 CROP ADAPTATION TO CLIMATE CHANGE

Fig. 13.2. Depiction of several developmental and physiological barriers that render early reproductive development in maizehighly vulnerable to water-deficit stress. These include failure to compete effectively for available assimilates with well-established vegetative sinks, storage of sugars in growing tissues as hexoses, which are not available for remobilization, andrapid inhibition of sucrose metabolism to glucose within the developing female flowers at low tissue water potential (Westgate,unpublished).

rachis at flowering, they are not in a form that canbe translocated to the starving flowers (Schusslerand Westgate 1995). Competition for limited as-similate supply favors the well-established leaf,stem, and root tissues. And loss of metaboliccompetence within the ovaries limits their capac-ity to compete for assimilates even further. Theredundancy of these mechanisms and their tem-poral coincidence with seed formation and earlykernel development in maize makes the task ofimproving grain yield in drought-prone environ-ments a particularly daunting task. There is con-siderable optimism, however, in the seed industryas transgenic and genomic approaches are beingapplied to identify candidate genes, regulatoryelements, and metabolic pathways to manipu-late in the next generation of drought-tolerant

(or resistant) maize hybrids (Campos et al. 2004;Edmeades 2009).

Molecular approaches to improveperformance under drought

Numerous studies have shown that timely pro-duction of osmotically active compounds canimprove physiological function of plants grownunder water-limited conditions. Improved plantperformance under severe drought, for example,has been reported in transgenic plants express-ing genes to produce trehalose (Romero et al.1997; Garg et al. 2002), mannitol (Tarczynskiet al. 1993; Abebe et al. 2003), galactinol (Tajiet al. 2002), ononitol (Sheveleva et al. 1997),sorbitol (Sheveleva et al. 1998), proline (Kishor




et al. 1995), and glycine-betaine (Rathinasaba-pathi et al. 1994). Unlike the yield advantageobserved in small grains in response to gen-eral selection for increased osmotic adjustment(Morgan 1983; Blum 1989), accumulation ofthese “compatible solutes” in transgenic plantshas not proven useful in improving tolerance todrought in a practical agriculture setting.

Expression of a number of genes that codefor regulatory factors or are involved in hormonesynthesis, however, has been effective in improv-ing performance under drought conditions in anumber of species. Notable examples are theCAAT box element ZmNF-YB2 (Nelson et al.2007), DREB1A transcription factor (Pellegri-neschi et al. 2004), MAP kinase NPK1 (Shouet al. 2004), drought-responsive elements ABREand DRE (Narusaka et al. 2003), poly (ADP-ribose) polymerase (Vanderauwera et al., 2007),farsenyl transferase (Wang et al., 2009), late em-bryogenesis abundant proteins (Xu et al., 1996),NCED2 and LOS5 in ABA biosynthesis, SOS2 inoxygen-radical detoxification (Xiao et al. 2008),isopentenyl transferase in cytokinin biosynthesis(Rivero et al. 2007), and the mRNA chaperoneCspB (Castiglioni et al. 2008). A common char-acteristic of many on these factors is their respon-siveness to more than one environmental stressand their impact on the expression of multiplemetabolic or structural genes.

Maize hybrids expressing the CspB gene havebeen evaluated extensively and provide an in-formative example of a specific molecular ap-proach that has yielded fairly consistent benefitsin terms of grain yield under water-limited condi-tions (Castiglioni et al. 2008). Focus on this par-ticular gene is not an endorsement for this molec-ular approach, the company that is developingit, or the company’s genetic products. Rather, itreflects the availability of peer-reviewed infor-mation on the performance of transgenic maizehybrids expressing this particular gene.

CspB codes for a protein that binds to foldedRNA molecules presumably to maintain properinitiation of mRNA translation. The gene was

first identified in bacteria subjected to cold stressconditions, and its activity is thought to promotegrowth following stress and during periods ofhigh metabolic activity (Hunger et al. 2006).Castiglioni et al. (2008) reported that constitu-tive expression of cold shock genes (CSPs) fromBacillus subtilis in maize plants promoted theiradaptation to stressful growing conditions dur-ing vegetative and reproductive growth. Water-deficit treatments were imposed in a controlledenvironment 10–14 days prior to flowering,which decreased plant growth rate up to 50%,relative to well-watered plants. Averaged acrosstransgenic events, 14% more plants expressingthe CspB gene from B. subtilis produced kernel-bearing ears and set 112% more kernels perplant (Castiglioni et al. 2008). No data on kernelweight were reported.

In the field, the performance of transgenichybrids was evaluated under water-limited con-ditions that decreased grain yield approximately50%, relative to the average for productive maizecrops in the Midwest (∼7 Mg/ha). On average,yield of CspB-positive plants was 7.5% greaterthan the nontransformed controls (P < 0.01)(Fig. 13.3a). The two best-performing events inthese trials showed a yield advantage of about20% and 11%, respectively. These two eventsalso exhibited significantly faster leaf growthrates (P < 0.05), numerically greater leaf chloro-phyll contents, and higher photosynthetic ratesrelative to the nontransgenic controls. While nospecific molecular or physiological mechanismswere ascribed to the improvement in grain yieldof the CspB-positive plants, it is well establishedthat seed-set in maize is closely coupled to theproduction of photoassimilate during seed for-mation and early kernel development (Schusslerand Westgate 1990a, 1990b, 1995; Vega et al.2001; Boyer and Westgate 2004; Borras et al.2007).

Although transgenic expression for specificstress tolerance genes such as CspB is prov-ing fruitful in some cases, breeding systemsthat integrate whole plant physiology, molecular




Fig. 13.3. Examples of published yield results from commercial field evaluations under water-deficit conditions of transgenicmaize hybrids carrying genes with potential to improve drought tolerance. (a) Three hybrids from Monsanto expressing theCspB gene (RNA chaperone) exposed to water-deficit stress during the late vegetative growth or early grain fill (from Castiglioniet al. 2008). (b) Yield advantage for two “Drought II” transgenic events from Pioneer Hi-Bred evaluated in multiple hybridsacross a range of stress levels and years. Specific transgenic events are not specified (Butzen and Schussler 2009).

genetics, and transgenic approaches to develophybrids that express well-established drought-tolerant traits are likely to be more effectivein the long term. Traits such as more exten-sive root systems, rapid silk emergence, andrapid tip kernel development are closely linkedto greater kernel numbers per plant under stress-ful field conditions (Saini and Westgate 2000;Campos et al. 2004; Duvick 2005; Edmeadeset al. 2009). Results of recent commercialfield trials focusing on these traits and uti-lizing an integrated approach demonstrated a16% advantage, on average, for transgenic hy-brids compared to their conventional counter-parts in drought-stress environments in the Mid-west US (Butzen and Schussler 2009; Fig.13.3b). Because the specific transgenes testedin these trials have yet to be disclosed, it isnot possible to ascribe a particular metabolic,regulatory, or developmental process responsi-ble for the improved field performance. It islikely, however, that multiple processes are be-ing targeted and not all are specifically drought-responsive since these trials were conductedin several genetic backgrounds being devel-

oped for a range of environments across theUS Cornbelt.

Optimizing root architecture andfunction for drought tolerance

Numerous studies have demonstrated a func-tional relationship between root architecture, ca-pacity for nutrient acquisition, and drought tol-erance (Collins et al. 2008; Postma et al. 2008;Hochholdinger and Tuberosa 2009; Nord andLynch 2009). In a comparison of “old” and“new” hybrids, Campos et al. (2004) observednew hybrids were more effective in extractingwater from deeper soil layers than were older hy-brids when soil moisture became limiting. Cropmodeling simulations confirm that a shift in rootsystem architecture and capacity for water cap-ture to deeper soil layers would have a positiveeffect on biomass accumulation (Hammer et al.2009). Enhanced root growth explained observedhistorical yield trends more readily than did in-creased canopy photosynthesis. The advantageof deeper root systems may lie in the avoidance




of ABA production by roots in the drier uppersoil layers, as proposed by Giuliani et al. (2005).But detailed analyses of root length, rate of elon-gation, branching patterns, and aerenchyma for-mation in droughted plants show that all thesephenotypic traits contribute to increased droughttolerance under field conditions (Lynch 2007a,2007b; Zhu et al. 2010). QTLs associated withthese architectural characteristics have been de-tected by numerous investigators (Giuliani et al.2005; Landi et al. 2010; Zhu et al. 2005, 2006),which should make it possible to develop marker-based selection schemes for more favorableroot traits.

Greater tolerance to drying soil conditionsalso will be realized in hybrids expressing trans-genic proteins that limit predation by corn bor-ers and rootworm pests. Corn borer feeding onleaves and stalks reduces the number of func-tional vascular bundles, which restricts move-ment of water, photosynthate, and nutrients todeveloping vegetative and reproductive struc-tures. Likewise, damage to the root vascularsystem resulting from rootworm larvae feed-ing and subsequent infection by opportunis-tic fungal pathogens disrupts transport of wa-ter and nutrients to the shoot. Loss of trans-port capacity increases the likelihood for morerapid and extensive dehydration of shoot struc-tures even under moderate evaporative demand.Loss of functional root tissue can also limitthe transport of growth-promoting cytokininsto the shoot from root apices where they areproduced (Brzobohaty et al. 1993). There isabundant evidence that decreasing the levels ofcytokinins in the female flowers disrupts nor-mal seed formation and early kernel develop-ment (Dietrich et al. 1995; Jones and Schreiber1997; Jones and Setter 2000; Brugiere et al.2003).

Pipeline for analysis of candidategenes for drought tolerance

It is intuitive that directing changes in plant de-velopment requires shifts in meristem initiation,

assimilate partitioning, and organ growth—allof which involve complex and integrated physi-ological processes. As such, coupling transgeneexpression with selection for specific phenotypicoutcomes likely alters the temporal and spa-tial expression of multiples genes or gene sys-tems. Molecular breeding platforms must striveto identify the appropriate “gene expression fin-gerprint” for selecting individual plants for ad-vanced testing and couple it with a phenotypicselection program that is equally robust and ef-ficient at identifying those individuals. Moderngenomics facilities can quantify the expressionof tens of thousands of genes from a sample ofmRNA, identify thousands of molecular mark-ers in a sample of DNA, or establish the pres-ence of unique gene sequences or even singlenucleotides that might alter gene product func-tion. But most of this genomic information is not“functional” in the sense that it actually deter-mines the phenotypic character of interest. Pub-lished results of global gene expression in maizereproductive structures in response to drought,for example, provide abundant information ongene expression after the drought has developedand growth has ceased (Zinselmeier et al. 2002;Yu and Setter 2003). Even though their analysisfocused on genes that were either up-regulatedor down-regulated in response to drought in thereproductive tissues, loss of photosynthetic ca-pacity in leaves was far more detrimental tokernel set than was a loss in metabolic com-petence in the floral structures. These studies do,however, underscore the importance of couplingchanges in metabolic and regulatory gene ex-pression with specific phenotypic characteristics(in this case, photosynthesis and ovary growth)to identify new genetic opportunities for im-proving drought tolerance. It is also importantto note these gene expression studies were con-ducted on a small handful of hybrids. Quanti-fying such subtle changes in plant development,whether induced transgenically or through selec-tion under stressful conditions, on a scale use-ful in breeding programs remains a monumentalchallenge.




Success in accelerating the development ofmaize germplasm adapted to drought-proneenvironments may rest in the logical cou-pling of high throughput technologies for geneexpression and genetic marker analysis (ge-nomics), temporal and spatial metabolic pro-filing (metabolomics), and phenotypic evalu-ation (phenomics). Research being conductedat the Australian Centre for Plant functionalGenomics provides a practical example of howthese “omics” approaches are being integratedinto a successful program of functional ge-nomics for testing candidate genes in plantato improve drought tolerance (Sutton 2009).The Centre couples a forward genetics (mu-tational) approach to define the genetic basisfor variation in drought tolerance with devel-opment of a database of transcript, protein, andmetabolite responses to drought stress. They alsoare targeting specific genes with known rolesin drought-stress tolerance, such as the tran-scription factors and protein kinases mentionedearlier. Populations of closely related lines de-veloped for mapping chromosome regions im-portant for drought tolerance have been charac-terized for more than 40 phenotypic traits in 20environments. The challenge of high-throughputphenotyping is being addressed at a plant phe-nomics facility (The Plant AcceleratorTM) estab-lished at the University of Adelaide, which isdesigned to analyze more than 100,000 plantsannually (http://www.plantaccelerator.org.au/).The facility uses high-resolution imaging for au-tomated nondestructive measurements of phe-notypic characteristics such as shoot mass, leafnumber, shape, angle, leaf color, leaf senescence,leaf water and carbohydrate contents, and leaftemperature (Sutton 2009). Whether evaluatingthese indices on vegetative tissues will translateto improved grain yield for maize under inter-mittent or terminal droughts during reproduc-tive development remains to be seen. Develop-ing nondestructive methods to quantify seed for-mation and development on reproductive-stateplants would likely have a dramatic impact on

the effectiveness of this selection tool for im-proving drought tolerance.

Temperature effects on maizegrowth and yield

Temperature has a major effect on maize re-productive physiology, particularly as it inter-acts with decreasing water availability duringdrought. Higher temperature shortens the lifecycle and duration of the reproductive phase,causing a reduction in grain yield (Badu-Aprakuet al. 1983; Muchow et al. 1990; Almaraz et al.2008). Runge (1968) was one of the first toreport the interaction of daily maximum tem-perature and rainfall around anthesis on maizeyields. When rainfall was low (0–44 mm per8 days), yield was reduced by 1.2–3.2% per1◦C rise. Conversely, at high temperatures (Tmax

35◦C), yield was reduced 9% per 25.4 mm de-cline in rainfall. Muchow et al. (1990) observedthe greatest grain yields were obtained at loca-tions with relatively cool mean temperatures dur-ing the growing season (18.0–19.8◦C at GrandJunction, CO), compared to warmer sites, e.g.,Champaign, IL (21.5–24.0◦C), or warm tropicalsites (26.3–28.9◦C).

Adapting maize to higher temperatures pre-dicted under climate change requires a greaterunderstanding of physiological and genetic re-sponses to temperature stress. It is well es-tablished that pollination, kernel set, and earlykernel development all are negatively affected.Pollen viability decreases when exposed to tem-peratures above 35◦C (Herrero and Johnson1980; Schoper et al. 1987; Dupuis and Dumas1990). Hardacre and Eagles (1986) observedthat low temperatures reduced growth and yieldin the cooler growing regions of New Zealand,Europe, and North America; genetic differencesin growth were evident at temperatures below16◦C, but not in the warmer environments withaverage temperatures up to 28◦C. And Tollenaarand Wu (1999) concluded the primary reasonfor continued improvement in maize yields in




Canada was enhanced resistance to stresses,particularly during reproductive development.Clearly, evaluating corn hybrids for greater toler-ance to high-temperature stress during seed for-mation and grain filling would be a beneficialstrategy for adapting to climate change. Physi-ology studies provide a number of possible tar-gets for selection. Once pollen is shed from theplant, the rate at which it loses viability is a func-tion of its moisture content and strongly depen-dent on vapor pressure deficit (VPD) (Fonsecaand Westgate 2005). Pollen subjected to highair temperatures loses viability more rapidlydue to the exponential increase in VPD withtemperature. Susceptibility appears to be dueto inability of mature pollen grains to produceheat shock proteins (Dupuis and Dumas 1990;Magnard et al. 1996). Therefore, it might be pos-sible to sustain pollen viability by upregulatingHSP genes shown to be active earlier in pollendevelopment or by selecting for slower pollendehydration. Kernel set can be improved, par-ticularly at high temperature, by increasing thesynchrony of pollination within and among ears(Carcova and Otegui 2001). They observed pol-lination gaps of 2–4 days reduce kernel numberper ear up to 51%; the impact of asynchronouspollination was increased by exposure to hightemperatures. Higher night temperatures duringsilking also negatively affect kernel set by accel-erating ear and flower development. More rapiddevelopment effectively decreases photoassimi-late availability per flower, which is most criticalfor the late-formed flowers at the tip of the rachis(Cantarero et al. 1999).

Romay et al. (2010) reported that kernel depth(size) and temperature were the primary geno-typic and environmental covariates explainingthe variability in grain yield they observed inmaize populations grown across nine environ-ments. Numerous physiological studies supporttheir findings. In vitro evidence indicates thethermal environment during endosperm cell di-vision phase (8–10 days postanthesis) is mostcritical to the success of kernel development

(Jones et al. 1984). Temperatures of 35◦C dur-ing endosperm cell division reduced subsequentkernel growth rate and final kernel size, evenafter the plants were returned to optimal condi-tions (Jones et al. 1984, Wilhelm et al. 1999).Chronic heat stress restrains seed storage pro-cesses and disrupts starch metabolism (Wilhelmet al. 1999). The rate-limiting enzyme in en-dosperm starch biosynthesis, ADP-glucose py-rophosphorylase (AGPase), is extremely heatlabile (Hannah et al. 1980). Fortunately, thereare thermally stable forms of this enzyme, andtransgenic maize lines expressing a heat-stabileAGPase have shown increased capacity forstarch synthesis and yield (Giroux et al. 1996).A more difficult issue to resolve, however, is thedisruption of endosperm cell division and amy-loplast replication at temperatures above 30◦C,which dramatically reduces potential grain sizeand final yield (Commuri and Jones 2001).

Exposure to high temperatures during grainfilling affects photosynthetic efficiency; typi-cally, leaf photosynthesis rates reach an opti-mum between 33◦C and 38◦C (Oberhuber andEdwards 1993; Edwards and Baker 1993; Crafts-Brandner and Salvucci 2002). Ben-Asher et al.(2008), however, observed highest photosyn-thetic rates at 25/20◦C (day/night) for sweet cornplants grown in a controlled environment cham-ber. Rates were 50–60% lower at 40◦C/35◦C anddeclined for each 1◦C increase in temperatureabove the optimum. Apparently, the decrease inphotosynthesis rates at high temperature is dueprimarily to the inactivation of Rubisco (Crafts-Brandner and Salvucci 2002). While a completeinhibition of leaf photosynthesis will decreasethe rate and duration of dry matter accumula-tion in the grain, the primary impact of highertemperatures at this stage of grain growth is tohasten to onset of physiological maturity. Ac-celerated development and premature desicca-tion will lead to a shorter duration of grain fill-ing, even if photosynthate is available to supportcontinued grain growth (Westgate 1994). Thephysiological mechanisms regulating premature




termination of grain development under hightemperature or water-deficit stress remain largelyunexplored.

Prospects for the near future

Drought remains by far the single most impor-tant constraint to productivity for maize (andmost other crops) worldwide. And the prospectsfor more widespread and frequent droughtsplaces even greater pressure on breeding pro-grams to develop tolerant germplasm. Despitethe complexity of the maize plant’s responsesto water-limited conditions and the apparent re-dundancy of physiological mechanisms to limitseed formation, rational application of molec-ular/genomic approaches and high-throughputphenotyping holds promise for major genetic im-provements in drought tolerance of this impor-tant crop. In fact, several major seed companiesnow have drought-tolerant hybrids in their devel-opment pipelines directed towards commercialrelease.

The most promising outcomes, however, willlikely accrue from the emerging collaborationsamong international germplasm programs, pri-vate institutions, and international foundationsto link basic gene discovery with improvedcrop productivity in developing countries. Oneprominent example is the public–private part-nership funded by the Bill and Melinda Gatesand Howard G. Buffet foundations and coor-dinated by the African Agricultural Technol-ogy Foundation. The Water Efficient Maizefor Africa project (http://www.aatf-africa.org/wema) brings together scientific expertise fromthe International Maize and Wheat Improve-ment Center (CIMMYT), Monsanto, and BASF,and the national agricultural research centersin Kenya, Mazambique, Uganda, Tanzania, andSouth Africa. The goal is to increase yields oflocally adapted maize germplasm by 20–35%under moderate drought over the next 10 years.While this ambitious goal might be well withinreach of plant breeding programs using trans-genic and genomic technologies, the ultimate

success of such endeavors will depend on greatergovernment support for the agricultural sector inthese countries and much greater emphasis onsmall landholder involvement in evaluating andintegrating the new drought-tolerant germplasmprofitably into their production systems. As Mr.Gates recently stated, “Small landholder farm-ers are not a problem to be solved . . . they arethe solution.”1 Developing technologically ad-vanced seed alone will not overcome the chal-lenges posed by a changing climate without di-rectly engaging those who plant and nurture thecrop.

Endnote

1. 2009 World Food Prize Symposium. Des Moines, IA.

References

Abebe T, Guenzi AC, Martin B et al. (2003) Tolerance ofmannitol-accumulating transgenic wheat to water stressand salinity. Plant Physiology 131: 1748–1755.

Ainsworth EA, Long SP (2005) What have we learned from5 years of free-air Co enrichment (FACE)? A meta-analytic review of the responses of photosynthesis,canopy properties and plant production to rising CO2.New Phytologist 165: 351–371.

Almaraz JJ, Mabood F, Zhou X et al. (2008) Climatechange, weather variability and corn yield at a higherlatitude locale: Southwestern Quebec. Climatic Change88: 187–197.

Andersen MN, Folkard A, Wu Y et al. (2002) Soluble inver-tase expression is an early target of drought stress duringthe critical, abortion-sensitive phase of young ovary de-velopment in maize. Plant Physiology 130: 591–604.

Badu-Apraku B, Hunter RB, Tollenaar M (1983) Effect oftemperature during grain filling on whole plant and grainyield in maize (Zea mays L.). Canadian Journal of PlantScience 63: 357–363.

Ben-Asher J, Garcia A, Garcia Y, Hoogenboom G (2008)Effect of high temperature on photosynthesis and tran-spiration of sweet corn (Zea mays L. var. rugosa). Pho-tosynthesis 46: 595–603.

Blum A (1989) Osmotic adjustment and growth of barleycultivars under drought stress. Crop Science 29: 230–233.

Bolanos J, Edmeades GO (1996) The importance of theanthesis-silking interval in breeding for drought toler-ance in tropical maize. Field Crops Research 48: 65–80.

Borras L, Westgate ME, Astini J et al. (2007) Coupling timeto silking with plant growth rate in maize. Field CropsResearch 102: 73–85.




Boyer JS (1982) Plant productivity and environment. Science8: 443–448.

Boyer JS, Westgate ME (2004) Grain yields with limitedwater. Journal Experimental Botany 55: 2385–2394.

Brugiere N, Jiao S, Hantke S et al. (2003) Cytokinin oxidasegene expression in maize is localized to the vasculature,and is induced by cytokinins, abscisic acid, and abioticstress. Plant Physiology 132: 1228–1240.

Brzobohaty B, Moore I, Kristoffersen P et al. (1993) Releaseof active cytokinin by alpha-glucosidase localized to themaize root meristem. Science 262: 1051–1054.

Butzen S, Schussler J (2009) Pioneer research to developdrought-tolerant corn hybrids. Crop Insights 19: 1–4.

Campos H, Cooper M, Habben JE et al. (2004) Improvingdrought tolerance in maize: A view from industry. FieldCrops Research 90: 19–34.

Cantarero MG, Cirilo AG, Andrade FH (1999) Night temper-ature at silking affects kernel set in maize. Crop Science39: 703–710.

Carcova J, Otegui ME (2001) Ear temperature and pollina-tion timing effects on maize kernel set. Crop Science 41:1809–1815.

Castiglioni P, Warner D, Bensen RJ et al. (2008) BacterialRNA chaperones confer abiotic stress tolerance in plantsand improved grain yield in maize under water-limitedconditions. Plant Physiology 147: 446–455.

Collins NC, Tardieu F, Tuberosa R (2008) Quantitative traitloci and crop performance under abiotic stress: Where dowe stand? Plant Physiology 147: 469–486.

Commuri PD, Jones RD (2001) High temperatures duringendosperm cell division in maize: A genotypic compari-son under in vitro and field conditions. Crop Science 41:1122–1130.

Crafts-Brandner SJ, Salvucci ME (2002) Sensitivity of pho-tosynthesis in a C-4 plant, maize, to heat stress. PlantPhysiology 129: 1773–1780.

Dietrich JT, Kamınek M, Blevins DG et al. (1995) Changesin cytokinins and cytokinin oxidase activity in develop-ing kernels and the effects of exogenous cytokinin onkernel development. Plant Physiology Biochemistry 33:327–336.

Dupuis L, Dumas C (1990) Influence of temperature stresson in vitro fertilization and heat shock protein synthe-sis in maize (Zea mays L.) reproductive systems. PlantPhysiology 94: 665–670.

Duvick DN (2005) The contribution of breeding to yieldadvances in maize (Zea mays L.). Advances Agronomy86: 83–145.

Edmeades GO, Bolanos J, Hernandez M, Bello S (1993)Causes for silk delay in lowland tropical maize. CropScience 33: 1029–1035.

Edmeades GO (2009) Drought tolerance in maize: An emerg-ing reality. In: Global Status of Commercial Biotech/GMCrops: 2008, pp. 197–217. ISAAA Brief 39. ISAAA,Ithaca, NY.

Edwards GE, Baker NR (1993) Can CO2 assimilationin maize be predicted accurately from chlorophyll

fluorescence analysis? Photosynthesis Research 37:89–102.

Fonseca AE, Westgate ME (2005) Relationship between des-iccation and viability of maize pollen. Field Crops Re-search 94: 114–125.

Garg AK, Kim JK, Owens TG et al. (2002) Trehalose accu-mulation in rice plants confers high tolerance levels todifferent abiotic stresses. PNAS 99: 15898–15903.

Giroux MJ, Shaw J, Barry G et al. (1996) A single mutationthat increases maize seed weight. PNAS 93: 5824–5829.

Giuliani S, Sanguineti MC, Tuberosa R et al. (2005) Root-ABA1, a major constitutive QTL, affects maize root ar-chitecture and leaf ABA concentration at different waterregimes. Journal Experimental Botany 56: 3061–3070.

Hammer GL, Dong Z, McLean G et al. (2009) Can changes incanopy and/or root system architecture explain historicalmaize yield trends in the U.S. corn belt? Crop Science49: 299–312.

Hannah L, Tuschall D, Mans R (1980) Multiple forms ofmaize endosperm ADP-glucose pyrophosphorylase andtheir control by Shrunken-2 and Brittle-2. Genetics 95:961–970.

Hardacre AK, Eagles HA (1986) Comparative temperatureresponse for corn belt dent and corn belt dent X pool 5maize hybrids. Crop Science 26: 1009–1012.

Herrero MP, Johnson RR (1980) High temperature stress andpollen viability in maize. Crop Science 20: 796–800.

Hochholdinger F, Tuberosa R (2009) Genetic and genomicdissection of maize root development and architecture.Current Opinion in Plant Biology 12: 172–177.

Hunger K, Beckering CL, Wiegeshoff F et al. (2006) Cold-induced putative DEAD box RNA helicases CshA andCshB are essential for cold adaptation and interact withCold Shock Protein B in Bacillus subtilis. Journal Bac-teriology 188: 240–248.

Jones RJ, Schreiber BMN (1997) Role and function of cy-tokinin oxidases in plants. Plant Growth Regulation 23:122–134.

Jones RJ, Setter TL (2000) Hormonal regulation of earlykernel development. In: M Westgate and K Boote (eds)Physiology and Modeling Kernel Set in Maize, pp. 25–42.Special Publication 29. Crop Science Society of America,Madison, WI.

Jones RJ, Ouattar S, Crookston RK (1984) Thermal envi-ronment during endosperm cell division and grain fillingin maize: Effects on kernel growth and development invitro. Crop Science 24: 133–137.

Kishor P, Hong Z, Miao GH et al. (1995) Overexpressionof D-pyrroline-5-carboxylate synthetase increases pro-line production and confers osmotolerance in transgenicplants. Plant Physiology 108: 1387–1394.

Landi P, Giuliani S, Salvi S et al. (2010) Characterizationof root-yield-1.06, a major constitutive QTL for root andagronomic traits in maize across water regimes. JournalExperimental Botany 61: 3553–3562.

Lynch JP (2007a) Roots of the second green revolution.Turner review. Australian Journal of Botany 55: 493–512.




Lynch JP (2007b) Rhizoeconomics: The roots of shootgrowth limitations. Hortscience 42: 1107–1109.

Magnard J-L, Vergne P, Dumas C (1996) Complexityand genetic variability of heat-shock protein expressionin isolated maize microspores. Plant Physiology 111:1085–1096.

Morgan JM (1983) Osmoregulation as a selection criterionfor drought tolerance in wheat. Australian Journal Agri-cultural Research 34: 607–614.

Muchow RC, Sinclair TR, Bennett JM (1990) Temperatureand solar-radiation effects on potential maize yield acrosslocations. Agronomy Journal 82: 338–343.

Narusaka Y, Nakashima K, Shinwari ZK et al. (2003) Interac-tion between two cis-acting elements, ABRE and DRE, inABA-dependent expression of Arabidopsis rd29A genein response to dehydration and high-salinity stresses. ThePlant Journal 34: 137–148.

Nelson DE, Repetti PP, Adams TR et al. (2007) Plant nuclearfactor Y (NF-Y) B subunits confer drought toleranceand lead to improved corn yields on water-limited acres.PNAS 104: 16450–16455.

Nord EA, Lynch JP (2009) Plant phenology: A critical con-troller of soil resource acquisition. Journal ExperimentalBotany 60: 1927–1937.

Oberhuber W, Edwards GE (1993) Temperature dependenceof the linkage of quantum yield of photosystem II toCO2 fixation in C4 and C3 plants. Plant Physiology 101:507–512.

Pellegrineschi A, Reynolds M, Pacheco M et al. (2004)Stress-induced expression in wheat of the Arabidopsisthaliana DREB1A gene delays water stress symptomsunder greenhouse conditions. Genome 47: 493–500.

Postma JA, Jaramillo RE, Lynch JP (2008) Towards modelingthe function of root traits for enhancing water acquisitionby crops. In: LR Ahuja, VR Reddy, SA Saseendran, andQiang Yu (eds) Response of Crops to Limited Water: Un-derstanding and Modeling Water Stress Effects on PlantGrowth Processes, pp. 251–276. ASA, CSSA, SSSA,Madison, WI.

Rathinasabapathi B, McCue KF, Gage DA et al. (1994)Metabolic engineering of glycine betaine synthesis: Plantbetaine aldehyde dehydrogenases lacking typical transitpeptides are targeted to tobacco chloroplasts where theyconfer betaine aldehyde resistance. Planta 193: 155–162.

Rivero RM, Kojima M, Gepstein A et al. (2007) Delayedleaf senescence induces extreme drought tolerance in aflowering plant. PNAS 104: 19631–19636.

Romay MC, Mlavar RA, Campo L et al. (2010) Climatic andgenotypic effects for grain yield in maize under stressconditions. Crop Science 50: 51–58.

Romero C, Belles JM, Vaya JL et al. (1997) Expressionof the yeast trehalose-6-phosphate synthetase gene intransgenic tobacco plants: Pleiotropic phenotypes in-clude drought tolerance. Planta 201: 293–297.

Runge ECA (1968) Effect of rainfall and temperature interac-tions during the growing season on corn yield. AgronomyJournal 60: 503–507.

Saini HS, Westgate ME (2000) Reproductive developmentin grain crops during drought. Advances Agronomy 68:59–96.

Schussler JR, Westgate ME (1990a) Kernel set of maize atlow water potentials. I. Sensitivity to reduced assimi-late supply during early kernel growth. Crop Science 31:1189–1195.

Schussler JR, Westgate ME (1990b) Kernel set in maize atlow water potentials. II. Sensitivity to reduced assimilatesupply at pollination. Crop Science 31: 1196–1203.

Schussler JR, Westgate ME (1995) Assimilate flux deter-mines kernel set at low water potential in maize. CropScience 35: 1074–1080.

Schoper JB, Lambert RJ, Vasilas BL, Westgate ME (1987)Plant factors controlling seed set in maize. Plant Physi-ology 83: 121–125.

Setter TL, Flannigan BA, Melkonian J (2001) Loss of kernelset due to water deficit and shade in maize: Carbohydratesupplies, abscisic acid, and cytokinins. Crop Science 41:1530–1540.

Sheveleva E, Chmara W, Bohnert HJ et al. (1997) Increasedsalt and drought tolerance by D-ononitol production intransgenic Nicotiana tabacum L. Plant Physiology 115:1211–1219.

Sheveleva EV, Marquez S, Chmara W et al. (1998) Sorbitol-6-phosphate dehydrogenase expression in transgenic to-bacco. High amounts of sorbitol lead to necrotic lesions.Plant Physiology 117: 831–839.

Shou H, Bordallo P, Wang K (2004) Expression of the Nico-tiana protein kinase (NPK1) enhanced drought tolerancein transgenic maize. Journal Experimental Botany 55:1013–1019.

Sutton T (2009) Functional genomics and abiotic-stress tol-erance in cereals. In: A Eaglesham and RWF Hardy (eds)Adapting Agriculture to Climate Change, pp. 57–64.NABC Report 21. National Agricultural BiotechnologyCouncil, Ithaca, NY.

Taji T, Ohsumi C, Iuchi S et al. (2002) Important roles ofdrought- and cold-inducible genes for galactinal synthasein stress tolerance in Arabidopsis thaliana. Plant Journal29: 417–426.

Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protec-tion of transgenic tobacco by production of the osmolytemannitol. Science 259: 508–510.

Tebaldi C, Hayhoe K, Arblaster JM et al. (2006) Climaticchange, going to the extremes; An intercomparison ofmodel-simulated historical and future changes in extremeevents. Climatic Change 79: 185–211.

Tollenaar M, Wu J (1999) Yield improvement in temper-ate maize is attributable to greater stress tolerance. CropScience 39: 597–604.

Vanderauwera S, De Block M, Van de Steene N et al.(2007) Silencing of poly(ADP-ribose) polymerase inplants alters abiotic stress signal transduction. PNAS 104:15150–15155.

Vega CRC, Andrade FH, Sadras VO et al. (2001) Seednumber as a function of growth. A comparative study




in soybean, sunflower, and maize. Crop Science 41:748–754.

Wang Y, Beaith M, Chalifoux M et al. (2009) Shoot-specific down-regulation of protein farnesyl transferase(α-subunit) for yield protection against drought in canola.Molecular Plant 2: 191–200.

Westgate ME (1994) Water status and development of themaize endosperm and embryo during drought. Crop Sci-ence 34: 76–83.

Westgate ME, Boyer JS (1985) Osmotic adjustment and theinhibition of leaf, root, stem, and silk growth at low waterpotentials in maize. Planta 164: 540–549.

Westgate ME, Boyer JS (1986) Reproduction at low silkand pollen water potentials in maize. Crop Science 26:951–956.

Wilhelm EP, Mullen RE, Keeling PL et al. (1999) Heat stressduring grain filling in maize: Effects on kernel growth andmetabolism. Crop Science 39: 1733–1741.

Xiao B-Z, Chen X, Xiang C-B et al. (2009) Evaluation ofseven function-known candidate genes for their effectson improving drought resistance of transgenic rice underfield conditions. Molecular Plant 2: 73–83.

Xu D, Duan X, Wang B et al. (1996) Expression or a lateembryogenesis abundant protein gene, HVA1, from bar-ley confers tolerance to water-deficit and salt stress intransgenic rice. Plant Physiology 110: 249–257.

Yu L, Setter T (2003) Comparative transcriptional profilingof placenta and endosperm in developing maize kernels inresponse to water deficit. Plant Physiology 131: 568–582.

Zhu JM, Kaeppler SM, Lynch JP (2005) Mapping of QTLsfor lateral root branching and length in maize (Zea maysL.) under differential phosphorus supply. Theoretical andApplied Genetics 111: 688–695.

Zhu J, Brown KM, Lynch JP (2010) Root corticalaerenchyma improves the drought tolerance of maize(Zea mays L.). Plant Cell Environment 33: 740–749.

Zhu JM, Mickelson SM, Kaeppler SM et al. (2006) Detec-tion of quantitative trait loci for seminal root traits inmaize (Zea mays L.) seedlings grown under differen-tial phosphorus levels. Theoretical and Applied Genetics113: 1–10.

Zinselmeier C, Habben JE, Westgate ME et al. (2000) Carbo-hydrate metabolism in setting and aborting maize ovaries.In: ME Westgate and KJ Boote (eds) Physiology andModeling kernel Set in Maize, pp. 1–13. CSSA SpecialPublication No. 29. Crop Science Society of America,Madison, WI.

Zinselmeier C, Jeong BR, Boyer JS (1999) Starch and thecontrol of kernel number in maize at low water potentials.Plant Physiology 121: 25–36.

Zinselmeier C, Lauer MJ, Boyer JS (1995) Reversingdrought-induced losses in grain yield: Sucrose main-tains embryo growth in maize. Crop Science 35:1390–1400.

Zinselmeier C, Sun YJ, Helentjaris T et al. (2002). The useof gene expression profiling to dissect the stress sensi-tivity of reproductive development in maize. Field CropsResearch 75: 111–121.

crop adaptation to climate change (yadav/crop adaptation to climate change) || genetic adjustment to...

Documents