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Genetic Engineering for Modern Agriculture:

Challenges and Perspectives

Ron Mittler 1,2and Eduardo Blumwald 3

Department of Biochemistry and Molecular Biology,University of Nevada,Reno,Nevada 557;email:ronm@unr.edu

Department of Plant Sciences,Hebrew University of Jerusalem,Givat Ram,Jerusalem 91904,Israel

Department of Plant Sciences,University of California,Davis,California,95616-5270;email:eblumwald@ucdavis.edu

Annu.Rev.Plant Biol.2010.61:443–62

First published online as a Review in Advance on January 29,2010

The Annual Review of Plant Biology is online at plant.annualreviews.org

This article’s doi:

10.1146/annurev-arplant-042809-112116Copyright c

1543-5008/10/0602-0443$20.00

Key Words

abiotic stress,climate change,ﬁeld conditions,global warming,stress combination,stress tolerance,transgenic crops

Abstract

Abiotic stress conditions such as drought,heat,or salinity cause exten-sive losses to agricultural production worldwide.Progress in generating transgenic crops with enhanced tolerance to abiotic stresses has never-theless been slow.The complex ﬁeld environment with its heterogenic conditions,abiotic stress combinations,and global climatic changes are but a few of the challenges facing modern agriculture.A combination of approaches will likely be needed to signiﬁcantly improve the abiotic stress tolerance of crops in the ﬁeld.These will include mechanistic understanding and subsequent utilization of stress response and stress acclimation networks,with careful attention to ﬁeld growth conditions,extensive testing in the laboratory,greenhouse,and the ﬁeld;the use of innovative approaches that take into consideration the genetic back-ground and physiology of different crops;the use of enzymes and pro-teins from other organisms;and the integration of QTL mapping and other genetic and breeding tools.

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B i o l . 2010.61:443-462. D o w n l o a d e d f r o m a r j o u r n a l s .a n n u a l r e v i e w s .o r g b y U n i v e r s i t y o f T o r o n t o o n 07/15/10. F o r p e r s o n a l u s e o n l y .

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Further

ANNUAL REVIEWS

Contents

INTRODUCTION (444)

CHALLENGES IN MODERN AGRICUL TURE:CLIMATIC CHANGES AND ABIOTIC

STRESS ..........................444Climate Change and Global

Warming.......................444Climate Change Effects on Plant Growth and Development. (445)

THE FIELD ENVIRONMENT ,STRESS COMBINATION,AND PERSPECTIVES FOR STUDYING OF ABIOTIC

STRESS (446)

Field Conditions and Their

Relevance to Laboratory Studies of Abiotic Stress ................446Abiotic Stress Combinations.. (448)

CURRENT ACHIEVEMENTS IN ABIOTIC STRESS RESEARCH AND THEIR RELEVANCE

TO AGRICUL TURE .............451Regulatory Networks ..............451Sensing of Stress...................451Retrograde and Systemic

Signaling.......................452Epigenetic Control ................452Small RNAs.......................453QTL Analysis and Breeding........453Strategies for T ransgene

Expression......................454FUTURE DIRECTIONS IN

ABIOTIC STRESS RESEARCH ..454Novel Sources of T ransgenes.......454Overcoming Genetic

Programming...................

455

INTRODUCTION

Current and predicted climatic conditions,such as prolonged drought and heat episodes,pose a serious challenge for agricultural production worldwide,affecting plant growth and yield,and causing annual losses estimated at billions

of dollars (17,82).T ransgenic crops provide a promising avenue to reduce yield losses,im-prove growth,and provide a secure food supply for a growing world population (67,68).The acclimation of plants to abiotic stress conditions is a complex and coordinated response involv-ing hundreds of genes.These responses are also affected by interactions between different envi-ronmental factors and the developmental stage of the plant and could result in shortened life cycle,reduced or aborted seed production,or accelerated senescence.Here we review some of the critical challenges facing modern agri-culture,discuss different considerations for the development of crops with enhanced tolerance to ﬁeld conditions,and review recent achieve-ments in the study of abiotic stress.

CHALLENGES IN MODERN AGRICULTURE:CLIMATIC

CHANGES AND ABIOTIC STRESS Climate Change and Global Warming

Climate change and global warming are gener-ating rapid changes in temperature that are not matched by any global temperature increase of the past 50million years (55,60).Atmospheric CO 2concentrations increased signiﬁcantly in the past two centuries,rising from about 270μmol.mol −1in 1750to current concentra-tions larger than 385μmol.mol −1(55,65).This increase in atmospheric CO 2has been accom-panied by a coincident increase in the even more potent forcing gases methane,ozone,and ni-trous oxide such that combined ambient green-house gas concentrations are now expected to exceed concentrations of 550μmol.mol −1by 2050(18,101).The increase in greenhouse gases contributes to the greenhouse effect,lead-ing to global warming,and average annual mean warming increases of 3◦–5◦C in the next 50–100years have been projected (55).Although models differ considerably in their projections of local climate changes,they tend to agree in their predictions of increased frequencies of heatwaves,tropical cyclones,ﬂoods,and prolonged drought episodes (12).Agricultural

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regions of our planet are likely to be differ-entially affected by climate change.Average surface temperatures in the Northern Hemi-sphere,for example,have been estimated to rise between 2–3◦C by 2050and by as much as 6.5◦C by the end of the century (139).Because of the increased temperatures,projections for the western United States include earlier snowmelt,leading to reduced ice and decreased water stor-age in the spring.Climate models tend to sim-plify observed crop responses to climate change variables at both plot and ﬁeld levels,reducing the levels of conﬁdence in regional and global projections (134).Even though climate mod-els vary in their predictions on the intensity of the changes in temperature,precipitation,and other variables affecting global climate,there is a general consensus supporting the notion that changes in atmospheric CO 2concentra-tions,increase in ambient temperatures,and regional changes in annual precipitations will signiﬁcantly inﬂuence future agricultural pro-duction.

Climate Change Effects on Plant Growth and Development

The increase in atmospheric CO 2concentra-tions will stimulate photosynthesis and possibly lead to increased plant productivity and yields (55,97,134).Under optimal growth condi-tions,rising CO 2concentrations will increase net photosynthetic carbon assimilation in C3plants with a concomitant increase in yield be-cause Rubisco is not CO 2saturated at current atmospheric CO 2concentrations and because CO 2inhibits the oxygenation reactions and photorespiration (69).On the other hand,in C4plants the high concentration of CO 2inside the bundle sheath would prevent a signiﬁcant in-crease in photosynthetic activity.Nevertheless,at elevated CO 2concentrations the water sta-tus of C4plants under drought conditions was improved,resulting in greater photosynthesis and biomass accumulation (66).Recent evi-dence from FACE (free-air concentration en-richment)experiments (3)have provided clear evidence that carbon gains are greater in C3

Free-air

concentration

enrichment (FACE):experimentally enriching the atmosphere-enveloping portions of a ﬁeld with controlled amounts of carbon dioxide without using chambers or walls

plants grown in high CO 2concentrations.In crop FACE experiments,different CO 2condi-tions are imposed on crops growing in large ﬁelds under well-managed farm conditions and as close as possible to ﬁeld growing condi-tions.FACE experiments have established that C4photosynthesis is not directly stimulated by higher CO 2concentrations (66).

Both greenhouse and FACE experiments aimed at assessing the effects of elevated at-mospheric CO 2on evapotranspiration (ET)demonstrated a decrease in stomatal conduc-tance (g s )in potato,rice,wheat,and soybean,with a consistent decrease in ET ranging from 5%to 20%,depending on species and loca-tion (66).The CO 2-induced reduction in ET would improve water use efﬁciency of most crops,contributing to a better tolerance to wa-ter deﬁcit.However,a decrease in ET would increase leaf temperatures,thereby possibly re-ducing photosynthesis (120).Climate change factors,such as drought and increased temper-atures,projected for the near future may of-ten limit and even decrease any yield increase brought about by high atmospheric CO 2con-centrations.Brief periods of high temperature of a few days above those permissive for the for-mation of reproductive organs and the develop-ment of sinks such as seeds and fruits can have serious yield detriments.For example,a short episode of high temperature during anthesis can greatly reduce grain production in cereals (135,143).Because carbon supply increases in plants growing at elevated CO 2,it could be possible to utilize the increased carbon acquisition to sustain an increased sink development (increase in fruit or seed).Nonetheless,a recent analysis of the protein content in food crops showed that at elevated CO 2concentrations there is a 10%–15%reduction in grain protein con-tent (129),due to the nitrogen acquisition gap at elevated CO 2(4;excluding legumes).The possibility of partitioning a greater portion of the photosynthate into carbon-rich metabolites associated with stress tolerance has been dis-cussed (4).Thus,carbon-rich osmolytes,such as pinnitol,mannitol,trehalose,etc.,could con-tribute to the stabilization of protein structures

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ROS:reactive oxygen species

during water deﬁcit and the scavenging of reac-tive oxygen species (ROS)during stress (14,81).Nevertheless,more research would be needed to overcome intracellular transport constraints and attain proper compartmentation (i.e.,cy-tosol versus chloroplast)of the osomolytes (7,108).Although experiments performed in controlled environmental conditions indicated an effect of elevated CO 2concentrations on ﬂowering of both short-day and long-day species,FACE experiments suggested that CO 2concentrations have little or no effect on ﬂow-ering time in either C4or C3species (30,122;see,however,19).

THE FIELD ENVIRONMENT ,STRESS COMBINATION,AND PERSPECTIVES FOR STUDYING OF ABIOTIC STRESS

Field Conditions and Their Relevance to Laboratory Studies of Abiotic Stress

The main abiotic stresses that affect plants in the ﬁeld are being extensively studied (20,25,85).They include drought,salinity,heat,cold,chilling,freezing,nutrient,high light intensity,ozone and anaerobic stresses (e.g.,2,10,22,51,88,138).Nevertheless,ﬁeld conditions are un-like the controlled conditions used in the lab-oratory.For example,within any given ﬁeld,large ﬂuctuations in drought,salinity,extremes of temperature,or anaerobic conditions can oc-cur (44,103).As a consequence,a large de-gree of heterogeneity between the stress levels that impact different plants in the same ﬁeld can be present.This heterogeneity,in turn,can affect plant performance and yield.Abiotic stress-induced nonuniform ﬂowering in differ-ing parts of the ﬁeld can,for example,cause signiﬁcant reductions in yield (145).

In addition to heterogeneity in stressful conditions in differing parts of a given ﬁeld,the simultaneous occurrence of different abi-otic stresses should also be addressed (82;see below).Abiotic stresses such as drought and salinity,salinity and heat,and distinct combina-tions of drought and temperature,or high light

intensity are common to many agricultural ar-eas around the globe and could affect plant pro-ductivity.It was recently shown that the re-sponse of plants to a combination of drought and heat stress is unique and cannot be di-rectly extrapolated from the response of plants to drought or heat stress applied individually (,106,107,126).Similar ﬁndings were also reported for a combination of heat and high light intensity (49),and heat and salinity (61).Because different abiotic stresses are most likely to occur simultaneously under ﬁeld conditions,a greater attempt must be made to mimic these conditions in laboratory studies (82).It is ex-pected that a large number of distinct stress combinations will occur under ﬁeld conditions in different areas of the world,and it is likely that the same principles reported with drought and heat (,106,107,126),heat and high light intensity (49),and heat and salinity (61)will ap-ply to the co-occurrence of these stresses as well (see below).

The timing of the abiotic stress event with respect to the developmental stage of the plant should also be addressed (118).Although plants can differ in their sensitivity to various abiotic stresses during different developmental stages including germination,vegetative growth,re-productive cycle,and senescence,from a strictly agronomic point of view there appears to be only one main consideration:How would this interaction between stress and development af-fect overall yield?Germinating seedlings,for example,can be rapidly replaced by the farmer if damaged by an abiotic stress event,but a fully mature ﬁeld ready to ﬂower,or in the midst of its reproductive cycle,cannot.Most crops are highly sensitive to abiotic stresses dur-ing ﬂowering,with devastating effects on yield (11,54,113).In contrast,most laboratory stud-ies,especially those performed with Arabidop-sis ,do not address the effects of abiotic stress on seed productivity.As indicated above,stress events could also cause poststress premature ﬂowering in a ﬁeld,signiﬁcantly reducing pro-ductivity and yield (145).The interactions be-tween abiotic stress events and plant productiv-ity are perhaps the most critical for agricultural

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productivity and should be taken into con-sideration when conducting abiotic stress experiments.

A generalized strategy used by plants to cope with water deﬁcit is drought escape (73),where drought-stressed plants complete their life cy-cle through rapid growth and early ﬂowering,resulting in low plant productivity and infe-rior seed yields (145).Studies have demon-strated the occurrence of earlier ﬂowering and early maturity of crop plants during the past 50years and crop phenological events have ad-vanced at rates ranging from 0.8to 2.5days per decade depending on location (30,38,77).Although increased atmospheric CO 2concen-trations would not likely affect ﬂowering time in either C3or C4plants (122),studies have shown that season length has increased with warmer winter and spring temperatures (30).Thus,the increase in atmospheric temperature during this century will extend the growing season of many different crops and inﬂuence plant phenology.The extension of the grain-ﬁlling period could improve yields,and this improvement would be dependent on nutri-ent acquisition from the soil,efﬁcient mobi-lization of nutrients from the sources to the sinks,and slow rates of leaf senescence.Never-theless,two separate aspects of climate change (increased ambient temperature,and frequent drought episodes)could act antagonistically on yield during an extended growing season due to stress-induced leaf senescence.Thus,ef-forts toward developing transgenic plants with decreased stress-induced leaf abscission rates could render varieties able to tolerate dryer and extended growth periods.There is some experi-mental support to this notion:It has been shown that the cytokinin-induced delay of senescence in transgenic plants expressing IPT (isopen-tenyl transferase;a critical step in cytokinin pro-duction)under the control of a maturation-and stress-induced promoter resulted in increased drought tolerance,yield,and growth (104,105).

All stress events are typically followed by re-covery,although only a few studies have focused on the molecular,biochemical,or metabolic IPT:isopentenyl transferase

events that accompany recovery from stress (21).Moreover,when laboratory experiments on abiotic stress responses in plants included recovery,they mostly mimicked a single stress event followed by a single recovery period,with very few exceptions (75).In contrast,in the ﬁeld multiple cycles of stress and recovery typically occur over the growth period of the plant (21,39,99),and the acclimation to these stresses and relief cycles could be very different from the acclimation to a single stress event such as that studied in the laboratory.It could,for ex-ample,involve epigenetic changes and/or hor-monal memory,situations that are unlike those provided by a single stress scenario.

Another key difference between laboratory studies and ﬁeld conditions is the intensity and duration of the stress.In the ﬁeld drought con-ditions are generated gradually during a period of several days and plants do not experience a sudden water stress.Thus,artiﬁcial soil mix-tures containing a high content of peat moss,vermiculite,or high organic matter should be avoided because they cannot reproduce natu-ral soil drying conditions.Similarly,results ob-tained in laboratory experiments where plants are grown under hydroponic conditions should be corroborated,at least,with results of green-house experiments that attempt to reproduce ﬁeld conditions.Conditions of water deﬁciency similar to those occurring in the ﬁeld can be mimicked in the laboratory by growing plants under limited daily amounts of water rather than by withholding water altogether (e.g.,104).The root:shoot ratio has been shown to be an important determinant in the ability of plants to respond to environmental stress in general and to salt and drought in particular (85),and in the ﬁeld roots play critical roles in the plant strategy for stress avoidance (78,85).Labora-tory experiments should utilize large pots in order to facilitate root growth and a relative high root:shoot ratio and small pots should be avoided.A similar principle can be applied to all other abiotic stresses studied in the laboratory including heat,cold,and anaerobic stresses.It is mostly unknown at present whether the typ-ical standards used to study abiotic stress in the

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MS:Murashige and Skoog medium QTL:quantitative trait loci

TILLING:targeting induced local lesions in genomes

laboratory will elicit plant responses similar to those seen under ﬁeld conditions.

An additional consideration that is mostly neglected by abiotic stress studies in the labo-ratory is the relationship between abiotic stress and plant nutrition.For example,improved ni-trogen use efﬁciency,which represents nitro-gen uptake efﬁciency and nitrogen utilization efﬁciency,can correlate with improved drought tolerance.In addition,the potassium content of the soil can determine the degree of salinity stress affecting the plant (117,149).As a con-sequence,researchers who use K +-rich growth medium,such as MS (Murashige and Skoog)(86),together with salinity stress are subjecting the plants to a much lower degree of salt toxicity than those using an MS-based growth medium with controlled levels of K +and other nutri-ents (121).A distinction should also be made between soil salinity that is mostly used in lab-oratory studies (i.e.,NaCl)and soil sodicity that occurs in large areas of our globe (98,102).The high sodium nature of sodicity can come in the form of many salts including chlorides,sul-fates,carbonates,and bicarbonates of calcium magnesium,sodium,potassium,and high lev-els of boron and/or selenium,and have a high pH value.Plants developed by genetic engi-neering to tolerate salinity (i.e.,NaCl)under controlled growth conditions in the laboratory might therefore not be suitable for tolerating sodicity in the ﬁeld.Because the nutrient con-tent and/or pH of the soil or media can have a dramatic effect on the degree and mode of ac-tion of the abiotic stress applied,these param-eters should be taken into consideration when studying the abiotic stress response of plants under laboratory conditions (149).

Plant biologists have long acknowledged the importance of breeding for tolerance to abiotic stresses and stress combination (e.g.,50).The genetic characterization of segregating popula-tions of various crop species facilitated the iden-tiﬁcation of QTLs (quantitative trait loci)asso-ciated with root growth (154),early ﬂowering (130),drought (36,133),etc.Even so,few of these QTLs were successfully used for breed-ing programs.The most important limitation

of stress-related QTLs is that they are depen-dent on the environmental conditions to which they were characterized (high G ×E interac-tion)(28).Other constraints are that the differ-ent QTLs associated with stress-related traits (water use efﬁciency,osmotic potential,etc.)can explain only a low percentage of the vari-ation of the phenotype and that the effects of a favorable allele could not be transferable due to epistatic interactions (93).The challenge is to identify QTLs of major effect that are inde-pendent of the particular genetic background and clone the genes in the QTL.Functional analysis of the genes can be signiﬁcantly aided through the application of reverse genetics ap-proaches such as RNA interference (RNAi)and by screening TILLING libraries (76)in order to characterize the individual gene function(s).Emphasis should be given to forward genet-ics studies where the identiﬁed genes can be expressed in genotypes that have been already selected for their adaptation to stressful envi-ronmental conditions.

In light of the complex nature of the ﬁeld environment as described above,and the inter-actions between abiotic stress and plant devel-opment,a better attempt should be made to reproduce ﬁeld conditions in the laboratory.In addition,genetically modiﬁed plants should be tested under experimental conditions that rep-resent the various combinations of restrictive conditions that occur in the ﬁeld environment (82).

Abiotic Stress Combinations

Plant acclimation to a particular abiotic stress condition requires a response tailored to the precise environmental condition that the plant encounters (20,25,87,136).Although some overlap is expected,biochemical,physiological,and molecular events triggered by a speciﬁc en-vironmental stress condition would mostly dif-fer from those activated by a different set of abiotic parameters (24,32,40,106,107).In ad-dition to the differences that exist between the acclimation of plants to various abiotic condi-tions,different stresses,when combined,might

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actually require antagonistic responses (82,131,151).For example,during heat stress,plants increase their stomatal conductance in order to cool their leaves by transpiration.However,if the heat stress occurred simultaneously with drought,plants would not be able to open their stomata and their leaf temperature would be 2◦–5◦C higher (106,107).Salinity or heavy metal stress might pose a similar problem when com-bined with heat stress because enhanced tran-spiration could result in enhanced uptake of salt or heavy metals (61,142).High light intensity could prove problematic to plants subjected to drought or cold stress (47).Under these con-ditions the dark reactions are inhibited owing to the low temperature or insufﬁcient availabil-ity of CO 2,and the high photosynthetic energy absorbed by the plant,owing to the high light intensities,enhances oxygen reduction and thus ROS production (81,84).On the other hand,some stress combinations might have beneﬁcial effects on plants,when compared to each of the individual stresses applied separately.Drought stress,for example,would cause a reduction in stomatal conductance,thereby enhancing the tolerance of plants to ozone stress (70,90).Be-cause energy and resources are required for the process of plant acclimation,nutrient depri-vation could pose a serious problem to plants attempting to cope with stress (78,140).Like-wise,limited availability of key micronutrients such as iron,copper,zinc,or manganese,re-quired for the function of different detoxifying enzymes such as copper/zinc,iron,and man-ganese superoxide dismutases,or certain per-oxidases (94,100)could result in an enhanced oxidative stress in plants subjected to diverse abiotic stresses (81).The acclimation of plants to a combination of different abiotic stresses would,therefore,require a well-tailored re-sponse customized to each of the individual stress conditions involved,as well as to the need to adjust for some of the antagonistic or syner-gistic aspects of stress combination (82).

Drought and heat stress represent an excel-lent example of two distinct abiotic stress condi-tions that occur in the ﬁeld simultaneously (50,82,83,95,115).This combination was found to have a signiﬁcantly higher detrimental effect on the growth and productivity of maize,bar-ley,sorghum,and different grasses and plants than if each of the several stresses was applied individually (1,29,37,50,58,115,116,150).A comparison of all major U.S.weather disasters between 1980and 2004indicates that a combi-nation of drought and heat stress caused an ex-cess of $120billion in damages.In contrast,over the same period,drought not accompanied by heat stress caused some $20billion in damages (82).Physiological characterization of plants subjected to simultaneous drought and heat stress revealed that the stress combination has several unique aspects combining high respira-tion with low photosynthesis,low stomatal con-ductance,and high leaf temperature (106,107).Drought and heat stress combination was found to involve the conversion of malate to pyruvate generating NADPH and CO 2,which is possi-bly recycled into the Calvin–Benson cycle and thereby alleviates the effects of stress on pho-tosynthesis ().The source of malate for this reaction is starch breakdown that,coupled with energy production in the mitochondria,might play an important role in plant metabolism dur-ing a combined drought and heat stress (,107).T ranscriptome proﬁling studies of plants subjected to drought and heat combination sup-port the physiological and metabolic analysis of this stress combination and suggest that it re-quires a unique acclimation response involving over 770transcripts,not altered by drought or heat stress (107).Similar changes in metabolite and protein accumulation were also found,with several unique metabolites and at least 53dif-ferent proteins accumulating speciﬁcally during the stress combination (,107).In addition,at least one plant gene,cytosolic ascorbate per-oxidase 1(Apx1),was found to be speciﬁcally required for the tolerance of Arabidopsis plants to drought and heat stress combination ().A recent study that examined the response of sun-ﬂower plants to a combination of heat and high light intensity stress supported the results ob-tained during the exposure of Arabidopsis plants to a drought and heat combination and iden-tiﬁed a large number of genes that speciﬁcally

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responded to the stress combination (49).In ad-dition,the activity of different antioxidative en-zymes was found to be particularly effected by a combination of drought and temperature stress (61).

The extent of damage caused to agriculture by stress combination underscores the need to develop crops with enhanced tolerance to a combination of abiotic stresses (82).Draw-ing upon the limited physiological,molecular,and metabolic studies performed with plants si-multaneously subjected to two distinct abiotic stresses,it is not sufﬁcient to study each of the individual stresses separately (49,61,,106,107).The particular stress combination should be handled as a new state of abiotic stress in plants that requires a new type of acclimation response (82).

Figure 1summarizes many of the com-binations of environmental conditions that could have a signiﬁcant effect on

agricultural

Drought Salinity Heat Chilling Freezing Ozone Pathogen

Nutrient High CO 2High light

D r o u g h t

S a l i n i t y

H e a t

C h i l l i n g

F r e e z i n g

O z o n e

P a t h o g e n

U V

N u t r i e n t

H i g h C O 2

H i g h l i g h t

Figure 1

The stress matrix.Different combinations of potential environmental stresses that can affect crops in the ﬁeld are shown in the form of a matrix.The matrix is color coded to indicate stress combinations that were studied with a range of crops and their overall effect on plant growth and yield.References for the individual studies are given in the text (adapted from Reference 82).

production (the “stress matrix”).Stress interac-tions that have a deleterious effect on crop pro-ductivity include drought and heat,salinity and heat,ozone and salinity,ozone and heat,nutri-ent stress and drought,nutrient stress and salin-ity,UV and heat,UV and drought,and high light intensity combined with heat,drought,or chilling (29,41,47,48,50,58,78,100,114,115,116,137,140,141,142).Environmental interactions that do not have a deleterious ef-fect on yield and could actually have a beneﬁ-cial impact on the effects of each other include drought and ozone,ozone and UV ,and high CO 2combined with drought,ozone,or high light (4,18,90,124,144).Perhaps the most studied interactions presented in Figure 1are those of different abiotic stresses with pests or pathogens (i.e.,biotic stress).In some instances,it was reported that a particular abiotic stress condition enhanced the tolerance of plants to pathogen attack (16,92,110,114).However,in most cases prolonged exposure of plants to abi-otic stress conditions,such as drought or salin-ity,resulted in weakening of plant defenses and enhanced susceptibility to pests or pathogens (5,6,46,114,147).In contrast to the biotic-abiotic axis,most of the abiotic stress combi-nations presented in Figure 1have received little attention.The experience of farmers and breeders should be used as a valuable guide and resource to plant biologists trying to address a speciﬁc stress combination that is pertinent to their crop of interest or region.In addi-tion,different plants or crops speciﬁcally de-veloped by individual breeding programs might have varying degrees of sensitivity to distinct abiotic stress combinations.Major U.S.crops,including corn and soybean,are especially vul-nerable to a combination of drought and heat stress during their reproductive cycle.In con-trast,trees and a range of crops from northern hemispheres such as Sweden or Canada are rou-tinely subjected to a combination of cold stress and high light intensity (82).The global cli-matic changes causing increased CO 2,ozone,and UV stresses together with high average temperatures are also becoming major factors in stress combination research (4,18).Although

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the effects of elevated concentrations of CO 2are considered beneﬁcial for crop resistance to abiotic stresses,when nutrients are not limited,care should be taken when assessing these ef-fects in diverse areas of our globe and with dif-ferent crops (4,18).

CURRENT ACHIEVEMENTS IN ABIOTIC STRESS RESEARCH AND THEIR RELEVANCE TO AGRICULTURE

The central dogma of abiotic stress research in plants is to study how plants sense and ac-climate to abiotic stress conditions,and then use this knowledge to develop plants and crops with enhanced tolerance to abiotic stresses.The development of new methodologies has been a major driving force in this research:For exam-ple,microarray technology have driven much of the research into transcriptional networks during abiotic stress,whole-genome sequenc-ing and chromatin immunoprecipitation have driven research into epigenetic control of gene expression during stress,and metabolic proﬁl-ing has driven research into metabolic networks and their role in stress tolerance.

Despite this enormous research endeavor,the roles of very few genes in enhancing abi-otic stress tolerance have thus far been demon-strated under ﬁeld conditions.Moreover,these genes were identiﬁed through extensive screen-ing of transgenic lines in the laboratory and in the ﬁeld using a pipeline approach by various biotech companies ().Still unclear is whether massive screening of transgenic lines is superior to the central dogma approach in the develop-ment of future crops.Perhaps a comprehen-sive understanding of the plant acclimation pro-cess would be needed before efﬁcient molecular tools to enhance crop tolerance to abiotic stress could be designed.Of course,such understand-ing should take into account many of the ﬁeld conditions described above.Several promising avenues of research have been described in re-cent years.These include gene networks and upstream regulators of abiotic stress,the role of retrograde signaling and the balancing of stress

Pipeline:large-scale analysis of hundreds of genes expressed in transgenic plants and tested for tolerance to abiotic stress

and energy signaling,epigenetic control of gene expression during stress,and metabolomics and systems biology approaches.

Regulatory Networks

T ranscriptional regulatory networks and up-stream regulators in response to abiotic stress have been classiﬁed into regulons.These in-clude the CBF/DREB regulon that is mainly in-volved in cold stress responses,is controlled by ICE1/HOS1and SIZ1,and involves Zat10and Zat12;the AREB/ABF regulon that is mainly involved in ABA,drought,and salinity re-sponses is controlled by Snf1-related protein kinases and has a cross talk interaction with the CBF/DREB regulon via CBF4/DREB1D;the NAC/ZF-HD regulon that is ABA-independent and is involved in drought and salinity re-sponses;the MYC/MYB regulon that is ABA-dependent and could be activated by different abiotic stresses;and additional networks such as the HSF and WRKY that have a broad function in many biotic and abiotic stresses (23,26,40,87,112,123).

A network of upstream regulatory genes controls the transcriptional regulatory net-works and includes different proteins that integrate calcium signaling with protein phos-phorylation to decode particularlized stress signals and activate acclimation responses (e.g.,57,72,91,132,123,152).This network includes histidine kinases (HKs);receptor-like kinases;mitogen-activated protein kinases (MAPK cascades);calcium-dependent protein kinases (CDPKs);and different calcium chan-nels,pumps,and calcium binding proteins such as calmodulin (CaM)and calcineurin B-like proteins (CBLs).Unfortunately,the link between stress perception and the extensive networks of calcium,ROS,and protein phos-phorylation signaling is largely unknown and only a few new studies have begun to unravel it (see below).

Sensing of Stress

Sensing of abiotic stresses could be mediated via different routes.The sensor molecule could

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SnRK1:SNF1-related kinase

be physically affected by the stress,for example,as a membrane protein the receptor could be af-fected by changes in membrane ﬂuidity/rigidity or separation of the membrane from the cell wall.In contrast,the sensor could be activated by indirect changes in plant metabolism that result from stress such as metabolic changes,accumulation of ROS,release of ATP ,or reduced energy levels (e.g.,9,35,84,111,117,127).It was recently shown that energy depletion in Arabidopsis during abiotic stress is directly linked to the activation of abiotic stress responses via SnRK1(SNF1-related kinase 1;8).This upstream regulator triggers extensive transcriptional changes involving over 600genes and contributes to the restoration of cellular homeostasis and cellular survival (8).The large number of transcripts involved in the various metabolic and other acclimation responses controlled by SnRK1demonstrates that this protein functions as a key regulator of abiotic stress responses in plants.Another putative stress receptor that appears to function at a high level along the osmotic stress response signaling pathway is ATHK1.It was recently proposed that this plasma membrane histidine kinase functions through a phosphorelay mechanism together with ARR3/ARR4and/or ARR8/ARR9to activate ABA-dependent and ABA-independent responses involved in osmotic stress and seed desiccation tolerance,and controls the expression of about 400target genes (146).Another protein that was recently shown to function as an upstream regulator of salinity responses in Medicago truncatula is a novel leucine-rich repeat receptor kinase (Srlk ;31).However,RNAi or TILLING mutants in Srlk failed to suppress root growth in response to salinity stress and had lower expression of salinity response transcripts.These ﬁndings indicate that Srlk is involved in sensing of salinity stress and reveal an interesting mode for salinity adaptation in Medicago .

Retrograde and Systemic Signaling

Retrograde signaling from the chloroplast or mitochondria to the nucleus has also been

proposed to mediate abiotic stress perception (96).Many abiotic stress conditions will inﬂu-ence chloroplast or mitochondria metabolism and could generate signals such as overreduc-tion of the electron transport chain,enhanced accumulation of ROS,or altered redox poten-tial that will,in turn,trigger nuclear gene ex-pression and acclimation responses.Signaling from the chloroplast to the nuclei was recently shown to be mediated by Gun1and Abi4and to regulate a large number of nuclear transcripts (63).This pathway was also shown to be im-portant for heat stress acclimation and could be involved in sensing of other stresses (80).Retro-grade signaling could also mediate the response to high light intensity stress (96,109).Using a luciferase reporter gene fused to the promoter of the ascorbate peroxidase 2(Apx2)gene,it was previously reported that a local high light inten-sity stress can trigger a plant-wide systemic ac-climation response (59).This systemic response was recently shown to enhance the tolerance to oxidative stress and to involve the zinc ﬁnger protein Zat10(109).Rapid systemic responses to such abiotic stress conditions as heat,cold,salinity,and high light intensity were recently reported to be mediated by an auto-propagating wave of ROS that travels at a rate of ∼8.4cm min −1and is dependent on the presence of the respiratory burst oxidase RbohD gene (79).The rapid rates of systemic signals detected with lu-ciferase imaging suggest that many of the re-sponses to abiotic stresses might occur at a much faster rate than previously thought.It is therefore possible that many of the GeneChip ®studies for abiotic stress,present for example in GENEVESTIGATOR (45),lack key early time points from their analysis and these should be taken into consideration when designing future studies.

Epigenetic Control

A very exciting area in abiotic stress research has emerged in recent years focusing on epi-genetic factors that mediate responses to and memory of different abiotic stresses (25,52,56).Chromatin immunoprecipitation of DNA

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cross-linked to modiﬁed histones coupled with next-generation sequencing technology,as well as shotgun bisulﬁte sequencing,has opened the way for genome-wide analyses of changes in epigenome state.Stable or heritable DNA methylation and histone modiﬁcations can therefore be linked with abiotic stresses and show how plants use these mechanisms for long-term memory.Of particular interest to the characterization of abiotic stress under ﬁeld conditions is the control of ﬂowering time dur-ing abiotic stress.Mutations in some of the genes involved in epigenetic processes during stress were shown to cause changes in ﬂower-ing times (25).For example,late ﬂowering of the freezing-sensitive Arabidopsis mutant hos15was shown to result from deacetylation of the ﬂowering genes SOC and FT (153).The ﬂow-ering repressor FLC (a MADS-box protein)is epigenetically repressed during vernalization,allowing the acquisition of the competence to ﬂower after exposure to prolonged low temper-atures (33).This process was shown to involve numerous proteins with potential to alter chro-matin remodeling including VIN3,FCA,and FPA (25).In addition,it was recently shown that VIN3is also responsive to hypoxic conditions,suggesting that other abiotic stresses might af-fect ﬂowering time via modiﬁcations of this pathway (15).Because transition from the vege-tative to the reproductive stage in plants is heav-ily controlled by epigenetic mechanisms,more studies are needed to examine how these mech-anisms are altered by differing abiotic stresses.Such understanding could lead to better control of stress-induced early ﬂowering under ﬁeld growth conditions.

Small RNAs

In addition to chromatin remodeling,and par-tially responsible for some types for transcrip-tional suppression,the involvement of small RNAs in abiotic stress responses has received increased attention recently (71,125).Small RNAs belong to at least two groups:microR-NAs (miRNAs)and endogeneous small inter-fering RNAs (siRNAs).miRNAs and siRNAs

siRNAs:small interfering RNAs RISC:RNA-induced silencing complex RITS:RNA-induced transcriptional signaling

can cause posttranscriptional gene silencing via RISC (RNA-induced silencing complex)-mediated degradation of mRNA in the cy-tosol.In addition,siRNA can suppress gene expression by altering chromatin properties in the nuclei via RITS (RNA-induced transcrip-tional signaling;125).The involvement of small RNAs in suppressing protein translation dur-ing stress has also been proposed (125).Small RNAs such as miR398,393,395,and 399,as well as siRNAs such as SRO5-P5CDH and ATGB2,were shown to control gene expression during abiotic stresses including cold,nutri-ent,dehydration,salinity,and oxidative stresses (71,125).Small RNAs were also implicated in the control of ﬂowering time.For example,overexpression of miR159and 319causes de-layed ﬂowering,and overexpression of miR172,which targets an AP2transcription factor,re-sults in early ﬂowering (125).A key question,of course,is how the expression of small RNAs is regulated during abiotic stress.Unraveling the mode of small RNA expression during abi-otic stress will allow better control of gene ex-pression during stress and the improvement of crop stress tolerance.However,this task is dif-ﬁcult because of the large number of potential small RNAs that exist in the genome of differ-ent plants.

QTL Analysis and Breeding

QTL analysis and traditional breeding have proven to be useful for the identiﬁcation of genes responsible for biotic and abiotic stress tolerance in crops (27,128).Thus,genes re-sponsible for salinity tolerance were identiﬁed in wheat and rice;genes responsible for boron and aluminum toxicity were identiﬁed in wheat,sorghum,and barley;and genes responsible for tolerance to anaerobic stress were identi-ﬁed in rice (128).How the availability of next-generation sequencing and advanced metabolic proﬁling will impact this ﬁeld and facilitate the cloning of more genes responsible for tolerance to abiotic stresses will be an interesting avenue to explore (62).The ability of these tools to cosequence or coscreen a large number of F2

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or recombinant inbred lines coupled with sta-tistical linkage analysis could open the way for a very rapid and new type of marker-assisted mapping at the genome or metabolome level.

Strategies for Transgene Expression

Strategies for the use of selected genes to improve tolerance to abiotic stresses in crops include gain-and loss-of-function approaches that target single genes at various levels.These genes could be enzymes,proteins,or regu-latory genes such as transcription factors or MAPK.Tissue-speciﬁc,constitutive,or stress-inducible promoters have been used to express the selected genes in order to achieve maximum efﬁciency in stress protection with as few as possible negative effects on growth and pro-ductivity.Balancing energy requirements with acclimation appears to be a major challenge,and the identiﬁcation of functional homologs of SnRK1(8)in a range of crops could be a major breakthrough for this research.A better understanding of gene networks and regulons controlling individual stress and metabolic networks is required in order to truly balance energy,acclimation,and growth under stress conditions and during recovery.Such under-standing will likely be achieved in the near future through system-level studies of stress re-sponses in a variety of crops and model plants.A better understanding of ﬁeld conditions,agricultural needs,classical plant physiology,as well as the attitude and objectives of agricul-tural business interests should be a major focus for plant molecular biologists in studying basic mechanisms of abiotic stress tolerance.

FUTURE DIRECTIONS IN ABIOTIC STRESS RESEARCH

Various strategies can be used to enhance the tolerance of plants to abiotic stress by genetic engineering.As described above,detailed un-derstanding of the response of plants to abi-otic stress is a prerequisite to the identiﬁcation and use of upstream regulators to activate a bal-anced acclimation response that will enhance

the tolerance of plants to different stresses.The activation of this response could be facilitated during normal stress episodes in the ﬁeld via the use of abiotic stress-response promoters,or triggered prior to the stress event using differ-ent chemicals combined with chemical-speciﬁc inducible promoters,a strategy similar to the priming used to alleviate biotic stresses (13).However,even if all of the plant’s acclimation responses are activated,the plant might not be able to survive or produce sufﬁcient yield under the abiotic stress because of natural limitations of the speciﬁc cultivar or plant and its genetic programming.

Novel Sources of Transgenes

One strategy that might enable plants to resist otherwise lethal abiotic stresses is to introduce genes from stress-adapted species such as desert and halotolerant plants,or organisms such as freezing-tolerant ﬁsh.The use of these special-ized proteins,enzymes,or channels might give the crop plant the necessary additive advantage and enable it to resist far greater stress con-ditions than the nonmodiﬁed parental plant is able to.The large number of plant genome se-quencing projects in progress,as well as the se-quencing projects of other organisms from ex-treme environments,and even metagenomics projects,could well provide a rich source of genes for the manipulation of crop tolerance to abiotic stresses.A potentially interesting source of genes to enhance abiotic stress tolerance in crops may come from genes of unknown func-tion,which account for 20%–40%of each new genome sequenced (42,53).The majority of genes with unknown function were found to be species speciﬁc,suggesting that they could encode for stress adaptive mechanisms that are unique to different plants and other organisms (42,43).A test of 42ROS-response genes with unknown function in transgenic plants deter-mined that most of these genes could enhance the tolerance of plants to oxidative stress and demonstrated that Arabidopsis plants could con-tain Arabidopsis -and/or Brassica -speciﬁc path-ways for tolerance to oxidative stress (74).Thus

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genes of unknown function could be a promis-ing source of unique mechanisms for abiotic stress tolerance.Overcoming Genetic Programming A key consideration with respect to abiotic stress tolerance of annual crop plants is their genetic programming to undergo early ﬂower-ing and accelerated senescence in response to stress.Although this tendency is ideal for sur-vival in nature,it can have devastating effects on crop productivity.Overcoming this genetic programming by expression of a gene medi-ating cytokinin biosynthesis under the control of a drought stress-inducible promoter was re-cently shown to result in a dramatic increase in plant productivity under drought stress con-ditions (104,105).Elucidating and controlling the epigenetic mechanisms that regulate the transition from vegetative to reproductive phases and early ﬂowering during stress could

have similarly positive effects on plant pro-

ductivity under stress.Because programmed

cell death (PCD)is thought to be activated

by different abiotic conditions and enhanced ROS accumulation,as part of the genetic pro-gramming of annual plants,suppressing abiotic stress-induced PCD could also result in a simi-lar enhancement of yield under stress (34,148).Although suppressing senescence and PCD during stress might seem counterproductive,annual plants might have mechanisms to resist far greater stresses than previously thought,but they either do not activate these mechanisms,or use them only for the short period needed to generate seeds during stress-induced early

ﬂowering and senescence.

SUMMARY POINTS

1.A better attempt should be made to reproduce ﬁeld conditions in the laboratory,and

genetically modiﬁed plants should be tested under experimental conditions that represent

the different combinations of restrictive conditions in the ﬁeld environment.

2.Stress combination should be handled as a new state of abiotic stress in plants that requires

a new type of acclimation response.

3.The interactions between abiotic stress events and plant productivity are perhaps the most

critical for agricultural production and should be considered when developing transgenic

crops with superior ﬁeld performance.

4.Severe yield losses can be caused by climate change resulting in brief periods of temper-ature of a few days above the limits associated with the formation of reproductive organs

and the development of sinks such as seeds and fruits.

FUTURE ISSUES

1.Omics tools should be used to study abiotic stress response in the ﬁeld with elite cultivars as model plants.

2.Researchers should learn how to regulate ﬂowering time and control stress-induced early ﬂowering.

3.Identiﬁcation of key upstream regulators/sensors of stress acclimation and their use in enhancing abiotic stress tolerance is an important area of research.

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5.We should attempt to overcome the genetic programming of annual crops and suppress stress-induced facilitated life cycle and early senescence.

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462Mittler ·Blumwald A n n u . R e v . P l a n t B i o l . 2010.61:443-462. D o w n l o a d e d f r o m a r j o u r n a l s .a n n u a l r e v i e w s .o r g

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Annual Review of Plant Biology Volume 61,2010

Contents

A Wandering Pathway in Plant Biology:From Wildﬂowers to

Phototropins to Bacterial Virulence

Winslow R.Briggs p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1Structure and Function of Plant Photoreceptors

Andreas M¨o glich,Xiaojing Y ang,Rebecca A.Ayers,and Keith Moffat p p p p p p p p p p p p p p p p p p p p p 21

Auxin Biosynthesis and Its Role in Plant Development

Yunde Zhao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 49

Computational Morphodynamics:A Modeling Framework to

Understand Plant Growth

Vijay Chickarmane,Adrienne H.K.Roeder,Paul T .T arr,Alexandre Cunha,

Cory T obin,and Elliot M.Meyerowitz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 65

Female Gametophyte Development in Flowering Plants

Wei-Cai Y ang,Dong-Qiao Shi,and Y an-Hong Chen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p

Doomed Lovers:Mechanisms of Isolation and Incompatibility in Plants

Kirsten Bomblies p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 109

Chloroplast RNA Metabolism

David B.Stern,Michel Goldschmidt-Clermont,and Maureen R.Hanson p p p p p p p p p p p p p p 125

Protein T ransport into Chloroplasts

Hsou-min Li and Chi-Chou Chiu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157The Regulation of Gene Expression Required for C 4Photosynthesis

Julian M.Hibberd and Sarah Covshoff p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 181Starch:Its Metabolism,Evolution,and Biotechnological Modiﬁcation

in Plants

Samuel C.Zeeman,Jens Kossmann,and Alison M.Smith p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209Improving Photosynthetic Efﬁciency for Greater Yield

Xin-Guang Zhu,Stephen P .Long,and Donald R.Ort p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 235Hemicelluloses

Henrik Vibe Scheller and Peter Ulvskov p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263Diversiﬁcation of P450Genes During Land Plant Evolution

Masaharu Mizutani and Daisaku Ohta p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 291v A n n u . R e v . P l a n t B i o l . 2010.61:443-462. D o w n l o a d e d f r o m a r j o u r n a l s .a n n u a l r e v i e w s .o r g

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Evolution in Action:Plants Resistant to Herbicides Stephen B.Powles and Qin Yu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317Insights from the Comparison of Plant Genome Sequences Andrew H.Paterson,Michael Freeling,Haibao T ang,and Xiyin Wang p p p p p p p p p p p p p p p p 349High-Throughput Characterization of Plant Gene Functions by Using Gain-of-Function T echnology Youichi Kondou,Mieko Higuchi,and Minami Matsui p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 373Histone Methylation in Higher Plants Chunyan Liu,Falong Lu,Xia Cui,and Xiaofeng Cao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 395Genetic and Molecular Basis of Rice Yield Yongzhong Xing and Qifa Zhang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 421Genetic Engineering for Modern Agriculture:Challenges and Perspectives Ron Mittler and Eduardo Blumwald p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 443Metabolomics for Functional Genomics,Systems Biology,and Biotechnology Kazuki Saito and Fumio Matsuda p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 463Quantitation in Mass-Spectrometry-Based Proteomics Waltraud X.Schulze and Bj¨o rn Usadel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 491Metal Hyperaccumulation in Plants Ute Kr¨a mer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 517Arsenic as a Food Chain Contaminant:Mechanisms of Plant Uptake and Metabolism and Mitigation Strategies Fang-Jie Zhao,Steve P .McGrath,and Andrew A.Meharg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 535Guard Cell Signal T ransduction Network:Advances in Understanding

Abscisic Acid,CO 2,and Ca 2+Signaling

T ae-Houn Kim,Maik B¨o hmer,Honghong Hu,Noriyuki Nishimura,

and Julian I.Schroeder p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561The Language of Calcium Signaling

Antony N.Dodd,J¨o rg Kudla,and Dale Sanders p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 593Mitogen-Activated Protein Kinase Signaling in Plants

Maria Cristina Suarez Rodriguez,Morten Petersen,and John Mundy p p p p p p p p p p p p p p p p p 621Abscisic Acid:Emergence of a Core Signaling Network

Sean R.Cutler,Pedro L.Rodriguez,Ruth R.Finkelstein,and Suzanne R.Abrams p p p p 651Brassinosteroid Signal T ransduction from Receptor Kinases to

T ranscription Factors

T ae-Wuk Kim and Zhi-Y ong Wang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 681vi Contents A n n u . R e v . P l a n t B i o l . 2010.61:443-462. D o w n l o a d e d f r o m a r j o u r n a l s .a n n u a l r e v i e w s .o r g

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Directional Gravity Sensing in Gravitropism

Miyo T erao Morita p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 705Indexes

Cumulative Index of Contributing Authors,Volumes 51–61p p p p p p p p p p p p p p p p p p p p p p p p p p p 721Cumulative Index of Chapter Titles,Volumes 51–61p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 726Errata

An online log of corrections to Annual Review of Plant Biology articles may be found at http://plant.annualreviews.org

Contents vii A n n u . R e v . P l a n t B i o l . 2010.61:443-462. D o w n l o a d e d f r o m a r j o u r n a l s .a n n u a l r e v i e w s .o r g b

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