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Plant Science 229 (2014) 247–261

Contents lists available at ScienceDirect

Plant Science

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o grow or not to grow: A stressful decision for plants

udy Dolferus ∗

SIRO, Agriculture Flagship, GPO Box 1600, Canberra, ACT 2601, Australia

r t i c l e i n f o

rticle history:eceived 4 September 2014eceived in revised form 6 October 2014ccepted 9 October 2014vailable online 18 October 2014

eywords:biotic stresslant developmentenescenceormone regulation

a b s t r a c t

Progress in improving abiotic stress tolerance of crop plants using classic breeding and selectionapproaches has been slow. This has generally been blamed on the lack of reliable traits and pheno-typing methods for stress tolerance. In crops, abiotic stress tolerance is most often measured in terms ofyield-capacity under adverse weather conditions. “Yield” is a complex trait and is determined by growthand developmental processes which are controlled by environmental signals throughout the life cycle ofthe plant. The use of model systems has allowed us to gradually unravel how plants grow and develop,but our understanding of the flexibility and opportunistic nature of plant development and its capacityto adapt growth to environmental cues is still evolving. There is genetic variability for the capacity tomaintain yield and productivity under abiotic stress conditions in crop plants such as cereals. Techno-logical progress in various domains has made it increasingly possible to mine that genetic variability and

erealsrop yield

develop a better understanding about the basic mechanism of plant growth and abiotic stress tolerance.The aim of this paper is not to give a detailed account of all current research progress, but instead tohighlight some of the current research trends that may ultimately lead to strategies for stress-proofingcrop species. The focus will be on abiotic stresses that are most often associated with climate change(drought, heat and cold) and those crops that are most important for human nutrition, the cereals.

© 2014 Elsevier Ireland Ltd. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2481.1. Abiotic stresses: definition and impact on agriculture. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2481.2. Plant growth and the environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2481.3. Can we exploit plant adaptive capacity? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2481.4. The virtue of model plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2481.5. Are domesticated plants different? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249

2. Genetic approaches for improving abiotic stress tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2492.1. Field or controlled environment phenotyping? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2492.2. Avoidance and escape reactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2492.3. Constitutive versus inducible stress tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2502.4. QTL analysis in the genomics era . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2512.5. Next generation phenotyping methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251

3. Components of abiotic stress responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2523.1. The power of transcriptomics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2523.2. First things first: establishment of cellular protection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252
3.3. Taking care of metabolic adjustment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3.4. Do abiotic stress response pathways overlap? . . . . . . . . . . . . . . . . . . . . .3.5. Selection for tolerance to multiple abiotic stresses . . . . . . . . . . . . . . . .
3.6. Transgenic approaches for abiotic stress tolerance . . . . . . . . . . . . . . . .

∗ Tel.: +61 2 62465010.E-mail address: [email protected]

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248 R. Dolferus / Plant Science 229 (2014) 247–261

4. Coordination of growth responses to abiotic stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2544.1. Do plants have brains? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2544.2. Growth inhibition responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2554.3. Growth stimulation responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2554.4. An old legend born again: auxins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2554.5. Coordination of environmental responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257

5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258

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References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. Introduction

.1. Abiotic stresses: definition and impact on agriculture

Plants are immobile and depend on their environment forrowth and development. This environment is variable and chal-enges plants with abiotic stress situations throughout their lifeycle: light (quality and quantity), mineral nutrition (depletionnd toxicity, salinity), temperature (heat, cold) and water avail-bility (drought, flooding). Plant development is therefore flexiblend adjustable to the environment. During evolution, wild plantpecies have learned to adapt to their natural environment andhis has determined their geographical distribution. In agriculturalnvironments, crop productivity is usually well controlled by agro-omical practices, but crop losses due to extreme and unexpectedeather events are unavoidable. The prospect of having to meet

ood demands for a 34% increase of the global population by 2050s imminent [1]. Crop yields will need boosting, but the higherrequency and intensity of drought, heat and cold spells will alsoequire crops that are better able to maintain productivity underub-optimal conditions. The concept of “tolerance” and “sensitiv-ty” of plants to abiotic stress situations can be difficult to measure.n model plants like Arabidopsis, tolerance is often measured assurvival”. In crop species like cereals maintenance of “yield” andproductivity” is for economical reasons more important than “sur-ival”. The criteria to evaluate stress tolerance in crop plants mustherefore be based on a thorough understanding of the complex-ty of plant growth and developmental processes that ultimatelyorrelate with maintenance of productivity. Unfortunately, thisnowledge is still evolving.

Progress in cereal yield improvements has generally been slownd is starting to reach a plateau, falling short of the annualield increases required to meet 2050 food demands [2]. In ricend wheat it is estimated that the annual rate of yield increaseas so far been primarily achieved through improved manag-

ng practices (mechanization) rather than through breeding andenetic gain [3,4]. During the last decade significant progress haseen made in improving our understanding about plant physiol-gy and molecular biology and new technologies have placed usow in a better position to improve the efficiency of crop breed-

ng. Improved knowledge and advanced new technologies mayow provide us with an opportunity to improve the speed andfficiency of breeding to boost crop yield and abiotic stress toler-nce.

.2. Plant growth and the environment

Plants continuously adjust growth and development, grow-ng prolifically when conditions are optimal and slowing down,rresting and even reversing growth (e.g. abscission, senescence
nd cell death responses) under sub-optimal conditions – evenhen conditions are not life-threatening. This bidirectional growth
djustment mechanism is quite remarkable and poorly understood,ut it may hold the key for improving abiotic stress tolerance.

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Plant growth is a measure of environmental input and adap-tive capacity to a particular environment; some conditions canbe controlled by humans (irrigation, fertilization etc.), but othersare at the mercy of the weather. It is therefore not surpris-ing that crop productivity attributes (yield, quality) are stronglyinfluenced by environmental variability (gene–environment inter-actions, GxE). Consequently, the responsiveness of crop plantsto abiotic stresses is equally variable and is controlled by com-plex gene networks with epistatic interactions [5]. In the field,crop plants are continuously challenged by a combination ofstresses which are often typical for that environment. Breedingactivities are usually focused on specific target environments,but this approach tends to improve adaptive traits that are con-stitutively present and are relevant for that environment only.This approach may have resulted in the loss of genetic varia-tion from current breeding stock that would allow the plant tomaintain productivity under unexpected and/or more extremestress conditions. To identify germplasm that is better able tomaintain productivity under more challenging abiotic stress con-ditions, it will be necessary to increase the selection standards andidentify germplasm that is able to perform well under stress con-ditions.

1.3. Can we exploit plant adaptive capacity?

Plants in general (higher and lower plants) have a stagger-ing capacity to adapt to extreme environments and they canbe found in most ecosystems of the globe. Some grasses andflowering plants can be found on the Antarctic Peninsula [6], res-urrection plants are adapted to extremely hot and dry conditions[7,8], while seagrasses are land plants that have re-adapted tolife in a marine environment, surviving conditions of low light,high salt and anoxia in the sediment [9]. Adaptation of plantsto extreme environments requires complex morphological, devel-opmental and metabolic adaptations. Exploring the molecularmechanisms of drought tolerance in resurrection plants and salttolerance of halophytes has benefited our understanding aboutabiotic stress signalling and metabolic and developmental adapt-ion mechanisms [8,10]. Proof-of-concept transgenic approachescan be used to evaluate some of these adaptation mechanisms(e.g., cryo- and osmo-protectants) in crop species such as cere-als. However, this may be difficult to achieve if genes of an entiremetabolic pathway need to be transferred and it may also compro-mise important yield and quality traits. Important morphologicaland developmental components that contribute to abiotic stresstolerance simply cannot be transferred to cereals. Sourcing abioticstress tolerance traits from the available genetic variability in cropspecies, landraces and progenitor species may be a more desirableapproach.

1.4. The virtue of model plants

A small genome size has been an important criterion for theselection of model plants. The simple dicot Arabidopsis has been

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workhorse for advancing our understanding of various plantiological processes, including plant development and responseo various abiotic stresses. Comparative genomics is starting toeveal important differences between different model systems,uggesting that care is needed when extrapolating informationrom model systems to other plants. For example, some genes are

issing in Arabidopsis that are present in other plants [11], whilether genes have diverged and evolved different functions in otherlants. The control of flowering and flower development differsonsiderably between eudicots (Arabidopsis) and monocots (rice,rachypodium), even though the regulatory genes (e.g. MADS-ox genes) identified in Arabidopsis are also present in monocots12–14]. In addition, it has been shown in plants that many of theroteins with completely unknown function (POFs; proteins withbscure features) are species-specific and have no homologues inther species [15,16]. In recent times, sequencing technology hasecome faster and cheaper, which has made it possible to sequence

arger plant genomes. In addition to the rice genome, the genomeequences of four other cultivated grasses (maize, sorghum, barleynd wheat; www.gramene.org) and one wild grass (Brachypodium;ww.brachypodium.org) are now available, providing a wealth

f information for comparative genomics studies into the evo-ution of these genomes (synteny, gene loss/conservation, geneivergence). This unstoppable progress in sequencing technolo-ies and genomics will ultimately reduce the reliance on modelystems.

.5. Are domesticated plants different?

Domestication has turned wild ancestor varieties into culti-ated crops that have a different architecture and look vastlyifferent from their progenitor species (e.g., rice: Fig. 1). Selec-ion for desirable traits has affected many plant developmentalrocesses, including yield-related traits (seed size and number),eed shattering, seed dormancy, photoperiod and flowering time,alatability and overall shape and body architecture [17,18]. Com-arative genomics is slowly revealing the effect of domesticationt the DNA level [19]. Comparison of the wild rice (Oryza rufipogon)nd cultivated rice (O. sativa japonica) genome sequences revealsignificant gene loss in the cultivated species [20]. A comparisonetween domesticated and wild tomato revealed genes that under-ent positive selection and many genes that showed shifts in gene

xpression levels [21]. Some gene deletions, mutations and vari-tion in gene expression may have directly or indirectly affectedbiotic stress tolerance. In beans, two DREB2 loci (dehydration-esponsive element binding transcription factor) shared high levelsf sequence diversity in one bean locus but no variation in thether, suggesting that domestication may have affected one ofhese genes [22]. Wild ancestor plants and landraces are often

ore tolerant to abiotic stresses and this genetic variability coulde re-introduced in domesticated crops. This process has startedor cereals such as rice [23] and maize [24] using wide crossesetween progenitors and interbreeding relatives. In bread wheat,he reconstruction of synthetic hexaploids from the respective wildncestors aims to achieve a similar goal [25]. This process cane complicated by the lack of molecular markers for precisionreeding and the possible introduction of undesirable traits. Theseroblems will be discussed in more detail in the following section.omparative genomics could also be used to compare adaptationf crop species to abiotic stresses in different environments ando compare genetic variability in stress tolerance [26]. The differ-
nce in growth responses to environmental conditions can alsoeside in more subtle changes in gene functions (e.g., base pairubstitutions). Identifying those differences will take additionalffort.
29 (2014) 247–261 249

2. Genetic approaches for improving abiotic stresstolerance

2.1. Field or controlled environment phenotyping?

Controlled environments allow control over occurrence andtiming of a stress during plant development, as well as its dura-tion and severity. It is also possible to investigate the effect of asingle abiotic stress at a time. This is a significant advantage overfield studies, where environmental conditions are typically variableand unpredictable. However, field environments remain difficult tosimulate in growth chambers, even though technology is improving[27]. Air humidity, variation of light quantity and quality through-out the day (blue and red light enrichments at sunrise and sunset,respectively) control important plant physiological processes, yetare often ignored in controlled environments. Additionally, heatload caused by light bulbs can sometimes cause heat stress prob-lems [28,29] and soil drought and frost events are extremely hardto simulate in controlled environments. In the field, environmentalchanges that cause stress in plants most often occur over severalhours (in the case of heat during the day or frosts overnight) or evenover several days (in the case of drought). These gradual changesare difficult to replicate in controlled environments and stressesare often imposed abruptly, causing a shock situation by not allow-ing the plant to gradually adapt to the stress. Additionally, growingplants in pots that are too small affects root development, whichin the case of drought stress affects the severity and the speedwith which the stress is imposed [30,31]. Despite these issues, con-trolled environments are the only tool that allows the comparisonbetween different stress responses independently and when usedwith due care and reasonable attention, they can help to analysestress responses in terms of sensitivity of different plant develop-mental stages and effect of treatment duration and severity. Thisis very important for designing phenotyping methods and to makesure that lines with different flowering times are stressed at thesame developmental stage when comparing different lines. Com-munication with breeders and farmers can identify germplasm thatperforms better/worse in field stress conditions and this materialcan then provide an excellent benchmark to establish “realistic”stress treatment conditions that give identical rankings in growthchambers. It is equally important to replicate controlled environ-ment results under field conditions.

2.2. Avoidance and escape reactions

Selecting germplasm that is tolerant to abiotic stress under fieldconditions is compromised by escape or avoidance responses. Inwheat, the damage caused by terminal drought can be alleviatedby escaping drought through alteration of flowering time [32,33].This is particularly troublesome when screening large populationsthat segregate for flowering time genes. Flowering time is impor-tant for optimizing grain yield in wheat, as flowering too earlycan result in cold and frost damage and late flowering can resultin poor yields due to drought and heat stress [34,35]. Manip-ulating flowering time can also have adverse effects on yield;early-maturing varieties have less chance to accumulate biomasscompared to late maturing varieties, which indirectly affects grainyield in wheat [36]. Plants can also avoid stress damage by adaptingmetabolic activity and growth rate. Accelerated growth requiresfaster metabolism and mobilization of resources, while slowingdown metabolism and growth saves vital resources for passive sur-vival of abiotic stress conditions. Plants can use any of these tactics
for survival in a particular environment. In rice, ethylene responsetranscription factors (ERF) play an important role in floodingtolerance [37,38]. The ERF genes SNORKEL1 and 2 are impor-tant in deep-water rice varieties, where elongation growth and
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ig. 1. Effect of domestication in rice. Oryza rufipogon (top panel) is considered to bend overall appearance between the two lines are very obvious.

utgrowing rising water levels (escape response) is important foronger-term survival and grain production. In contrast, anotherRF-family member, SUBMERGENCE-1A (SUB1A), is important inice varieties that have to survive occasional short-term submer-ence and flooding by transiently keeping growth and metabolicctivity quiescent. Analysis of the molecular basis indicates thathe plant hormone ethylene plays an important role in regulatinglongation growth under stress conditions. The example of flood-ng tolerance in rice illustrates the importance of regulating plantrowth rate and metabolic activity under stress conditions. Avoid-nce and escape reactions generally provide protection againstbiotic stress through adjustment of growth rate and developmen-al processes. Understanding the molecular basis of these processess important for understanding abiotic stress tolerance.

.3. Constitutive versus inducible stress tolerance

Selection for yield-related traits in field environments hasominated crop breeding. Traits such as growth vigour, biomassccumulation, harvest index (reproductive biomass), stem

ncestor of cultivated rice (Oryza sativa; bottom panel). The changes in development

carbohydrate levels, tiller number, plant height, water use andtranspiration efficiency, carbon isotope discrimination and rootdepth are important in cereal breeding. These traits, togetherwith improved management practises, have improved vegetativegrowth of cereal crops, resulting in higher yield and productivity[32,33,39–41]. Interestingly, for Australian wheat the yield gainwas found to be proportionally higher in the driest years comparedto the better years even though those traits were not specificallytargeting drought conditions [4]. This illustrates that yield-basedtraits that boost vegetative growth, biomass accumulation andwater use efficiency generally benefit plant growth and resilienceand contribute to higher yields under abiotic stress conditions[3–5,41,42]. However, unexpected and more extreme abiotic stressconditions still result in massive yield penalties, indicating thatgrowth vigour and biomass accumulation does not necessarilyresult in a better capacity to maintain that yield potential when
growth conditions during reproductive development are notfavourable [5]. It is clear that an additional tolerance mechanism isneeded to convert or maintain the yield potential generated duringthe vegetative stage to successful reproductive development and

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rain productivity. Sensitivity of crops to various abiotic stressesre usually associated with phenotypes that are indicative ofrowth arrest, generally including leaf senescence or cell death,evere tissue necrosis (e.g., frosts and salinity), stomatal closurend arrest of photosynthesis [5]. At the reproductive stage, pollenterility and abortion of grain development are similar growthepression phenotypes that cause major yield losses in cereals.nder shorter-duration or unexpected stress periods, survival of

he plant is often not compromised as growth repression savesesources for later growth when conditions have returned toormal [43]. Even when this occurs, yield can never be recoveredecause it is too late in the growing season and previously estab-

ished biomass and productivity has been lost. In many crops,rowth repression can be an exaggeration or an overly sensitiveesponse to stress conditions. There may therefore be an opportu-ity for increasing the threshold level at which growth repressionakes place in response to stresses, in order to maintain growthnd productivity for as long as possible. Interestingly, the twoooding tolerance mechanisms described earlier for rice (Section.2: growth acceleration versus metabolic quiescence) may beore widely applicable for other abiotic stresses and the molecular

nderstanding of flooding tolerance may stimulate research onther abiotic stresses. An intriguing question is whether avoidancend escape strategies should also be seen as part of the plant’sverall strategy to tolerate abiotic stresses.

To identify crops that maintain growth and yield potentialnder adverse growth conditions it is necessary to complementonstitutively expressed yield traits with traits that are inducednd specifically expressed under stress conditions. Identifyingore stress-induced traits will have a positive effect for breed-

ng stress-tolerant crops, but also for improving our understandingf the underlying physiological and molecular mechanism. Undertress conditions, plants require mechanisms to protect theirellular machinery, metabolic adaptations and their capacity toustain growth and development (see Section 3). Selection fortress-inducible traits is more difficult to achieve, considering thenpredictability of field conditions and interference of avoidancend escape reactions. Field plots can be selected to target certainbiotic stresses (drought, heat, frost) or can be artificially modifiedo create stress conditions (irrigated, rain-fed, rainout shelter plotso compare water stress conditions) [44]. However, controlled envi-onments offer significant advantages if precision-phenotyping isequired (see Section 2.1). Leaf senescence is a stress-induced phe-otype and has received a lot of attention as a stress-inducedrait. Selecting for delayed foliar senescence (stay-green) and

aintenance of stomatal conductance, transpiration and photo-ynthesis during stress conditions are relatively easy phenotypeso score [45]. Significant improvements in drought tolerance haveesulted from proof-of-concept transgenic approaches manipulat-ng cytokinin levels, confirming that this trait contributes to stressolerance [46]. Leaf rolling is another distinctive and easy to scoreeat and drought-induced phenotype. Reduction in leaf area pre-ents transpiration and water loss and genetic variation for leafolling is available in wheat and rice. However, leaf rolling does notlways correlate with drought tolerance, suggesting that it coulde an escape rather than tolerance mechanism [47,48]. Osmoticdjustment is an inducible drought adaptation mechanism thataintains leaf water potential through the synthesis of osmotically

ctive substances [44,49,50]. Osmotic adjustment delays leaf senes-ence and leaf rolling, maintains stomatal conductance and turgorressure, thereby sustaining growth under drought conditions [51].espite its importance, osmotic adjustment has so far remained a
ifficult trait to phenotype [52]. Many abiotic stresses cause pollenterility and loss of fertility and grain yield in cereals [53,54]. Ahenotyping method for cold and drought-induced pollen steril-
ty was established using controlled environments [55,56] and the

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plant hormone abscisic acid (ABA) was shown to play a role instress-induced pollen abortion [53,57,58]. Stress-inducible traitsare less likely to have negative effects on productivity of cropsunder non-stress conditions. While yield traits that improve veg-etative plant growth and development contribute to building up ahigher yield potential, stress-inducible traits are essential to sustainthat higher yield potential under adverse environmental conditionsto maintain growth and reproductive development.

2.4. QTL analysis in the genomics era

Identifying genetic variation for abiotic stress tolerance incrops requires the tedious and laborious process of establish-ing linkage maps using DNA-based molecular markers: restrictionfragment length polymorphism (RFLP), amplified fragment lengthpolymorphism (AFLP), random amplification of polymorphic DNA(RAPD), cleaved amplified polymorphic sequences (CAPS) and sim-ple sequence repeat (SSR, microsatellite) markers. In the lastdecade, the shift to high-throughput technologies such as diversityarrays (DArT; [59]) and single nucleotide polymorphism markers(SNP; [60]) has made the construction of high density genomicmaps easier. The identification of SNP markers was boosted by theavailability of the genome sequence for many crop species. 160,000SNPs were identified in the non-repetitive genome fraction of 20different rice varieties [61]. The availability of annotated genomesequences and accurate high density SNP maps makes it easier toidentify candidate genes within quantitative trait loci (QTL) [61,62]and the lowering in sequencing costs has made it possible to carryout genotyping by sequencing (GBS), which further facilitates fine-mapping QTL [63]. Genome-wide association studies (GWAS [64])also benefit from high density SNP maps and can be used for map-ping abiotic stress tolerance loci. In wheat, the development ofmulti-parent advanced inter-cross populations (MAGIC) providesa powerful tool for mapping and fine-mapping QTL [65].

Abiotic stress tolerance is typically controlled by a largenumber of QTL with epistatic interactions and low phenotypiccontribution and heritability. A comprehensive overview of QTLfor various abiotic stress-related traits can be accessed at theGramene and Plant Stress websites (archive.gramene.org/qtl/;www.plantstress.com/files/qtls for resistance.htm). Abiotic stressQTL mapping and genomic selection (GS) has so far not led tomarkers for routine use in marker-assisted selection (MAS) for abi-otic stress tolerance [41,66,67]. With the bottleneck of genotypingremoved, mapping of abiotic stress tolerance loci will depend onthe availability of reliable traits for phenotyping. The case of salin-ity tolerance in rice is a good example that QTL analysis can leadto identification of candidate genes provided that reliable pheno-typing methods are available [68].

2.5. Next generation phenotyping methods

Considering the difficulties involved in direct selection for abi-otic stress tolerance in field or controlled environments, shiftingfrom “observable” to molecular or secondary traits that are highlycorrelated with abiotic stress tolerance, may improve reliability ofphenotyping procedures [69]. Our understanding about the physi-ological and molecular basis of stress responses has improved andtechnological progress in the last decade has provided opportuni-ties for high-throughput phenotyping. Metabolomics is a promisingtechnology that can now be used at a scale that is compatiblewith population screening and mQTL mapping. This technologywas used to identify genes controlling several metabolites and
quality-related traits [70–72], but can also be used to map mQTLfor metabolite changes associated with abiotic stresses [73,74].Measuring diagnostic metabolites can be informative about thephysiological state of plant tissues in response to drought, heat
http://archive.gramene.org/qtl/

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nd cold and metabolomics can be used to quantitatively andualitatively evaluate components of cellular protection. Hor-one measurements can be used as indicators of developmental

esponses in sensitive and tolerant germplasm (senescence orrowth). Proteomics can also be used for phenotyping abiotictress responses, but protein expression profiling can be techni-ally more challenging (e.g., resolution limits of two-dimensionallectrophoresis and detection limits of mass spectrometry) and isarder to adapt for high throughput screening [75]. The devel-pment in recent years of various digital imaging technologiesas added even more opportunities for phenotyping [67,76]. Non-estructive imaging can measure canopy properties that contributeo biomass accumulation, as well as stress-related traits (photo-ynthesis, transpiration and leaf senescence). This technology cane applied for high-throughput screening under field or controllednvironments [77–79]. New generation phenotyping technologiesre powerful but require some knowledge about the molecular andhysiological basis of abiotic stress phenotypes and the questionso be addressed.

. Components of abiotic stress responses

.1. The power of transcriptomics

While GxE interactions are considered problematic and some-hing to avoid in plant breeding, molecular biologists have usedifferential gene expression of stress-treated versus unstressedlant material as a standard method to study abiotic stressesponses. In the recent decade, large-scale transcriptome analysessing microarrays and more recently new generation sequencingechnologies (RNA-seq) have proven to be a powerful tool for iden-ifying genes and cellular processes that are affected by abiotictresses [80]. A massive amount of transcriptome information forifferent stresses and plant species is currently available in publicatabases.

Transcriptome information is starting to reveal how plantsespond to various abiotic stresses, but the full potential is stillnexplored [81]. Currently, about 40% of the proteins encoded by aukaryotic genome have an unknown function [82]. It is estimatedhat between 18 and 38% of the eukaryotic proteome consists ofroteins without any defined domain or motif [15]. Interestingly,hen comparing the Arabidopsis and rice proteins with totallynknown features (POFs) nearly half were found to be species-pecific and had no homolog in the other genome [16]. Obviously,dentifying the function of these proteins will require species-pecific studies and this will be a major challenge. Finding thexact physiological function for members of large gene familiese.g., transcription factors) can also be a complicated and time-onsuming process. In model plants such as Arabidopsis and rice,nsertion mutagenesis using T-DNA and transposons can be used todentify gene functions and support the gene annotation process.n rice, about 60.49% of the nuclear genes have been tagged with-DNA or Tos17 transposon insertions [83], but the functional char-cterization of these insertion mutants remains a major effort. Inddition, the function of some genes for which the insertion mutanthenotype is lethal cannot be investigated. Another limitation isene redundancy and lack of a clear phenotype for some mutations.ver-expression and RNAi technology can also be used to reveal

he function of candidate genes in plants that can be transformed.ranscriptome analysis needs support from other technologies topeed up the identification of unknown gene functions. A systems
iology approach combining transcriptomics with proteomics andetabolomics can help this process [84,85]. It is also important
o realize that transcriptomics focuses on differentially expressedenes, while some genes that play an important role in the early

29 (2014) 247–261

stress signal perception and transduction events, or those trigg-ering early developmental responses, are likely to be present allthe time and simply require activation by upstream signals (e.g.,phosphorylation). Identifying those genes will require more funda-mental approaches, ideally using model systems in the first place(e.g., using mutagenesis approaches).

3.2. First things first: establishment of cellular protection

Bacteria, yeast and animals have a general cellular stressresponse mechanism that protects essential macromolecules (DNA,proteins and lipids) against oxidative stress and removes damagedcells using a cell death response. The conservation of this responsein different life forms suggests that it is an ancient protection mech-anism against general stress situations. The minimal cellular stressresponse proteome consists of 44 proteins with known function,including molecular chaperones (e.g. heat shock proteins), vari-ous enzymes that repair DNA damage and proteins that protectagainst oxidative stress and reactive oxygen species (ROS), such assuperoxide dismutase and glutathione antioxidant defence path-way proteins [86].

Plants also activate a cellular protection mechanism in responseto various stresses. Little is known about macromolecule protec-tion in plants, but chaperone proteins (e.g. heat shock proteins) areinduced by all abiotic stresses and their importance is illustrated bythe fact that an Escherichia coli gene encoding a cold shock proteinthat functions as RNA chaperone can significantly improve toler-ance to multiple stresses (cold, drought, heat) in transgenic rice andmaize [87]. The transformation of light into chemical energy dur-ing photosynthesis and the mitochondrial electron transport chainproduce damaging free radicals [88]. Regulation of intracellularredox homeostasis has been shown to control important metabolicpathways such as photosynthesis [89,90] and is also important forregulating root and leaf developmental processes [91,92]. Superox-ide, hydrogen peroxide and hydroxyl radical production is inducedin response to abiotic and biotic stresses and results in activationof genes encoding ROS-detoxifying enzymes [93,94]. Active oxygenspecies such as hydrogen peroxide are generally considered as localand systemic signals in response to various stress situations [95,96].This indicates that plants may have turned this early stress defencemechanism into a systemic warning signal to protect different plantparts. Some oxidative stress-related genes are expressed in cellsassociated with the vascular bundles [97], which is compatiblewith a systemic signalling function of ROS [98–100]. Resistanceto the ROS-generating herbicide paraquat in Conyza bonariensis iscorrelated with a highly expressed constitutive ROS detoxificationsystem and cross-tolerance to environmental oxidants [101,102].Paraquat resistance in wheat and barley has been correlated withtolerance to water stress and paraquat treatment has been evalu-ated as a screening system for abiotic stress tolerance [103,104].Overexpression of peroxidase, catalase, superoxide reductase andsuperoxide dismutase in transgenic plants has resulted in improvedtolerance to cold, drought, salinity and heat stress [105–108],while an ascorbate deficient mutant in Arabidopsis caused a stress-sensitive phenotype [109]. Cellular protection in plants may alsofunction as an intracellular and systemic signal to regulate devel-opmental processes. As a stress defence mechanism it may beessential for all other aspects of the stress response to functionand it could therefore act as an “enabling” mechanism that needsto be activated before other aspects of stress responses (biotic andabiotic) can be established (Fig. 2).

3.3. Taking care of metabolic adjustment

Changes in plant growth and development under abiotic stressconditions must be associated with metabolic activity to provide

R. Dolferus / Plant Science 2

Fig. 2. Proposed components of abiotic stress responses in plants. Early responses toabiotic stress are likely to be general stress responses: cellular protection of macro-molecules and oxidative stress, metabolic adjustments and hormonal changes thatlead to developmental responses. Genetic variation in crop species can lead to dif-ferent responses in reaction to certain threshold levels of abiotic stresses. Somegermplasm will initiate a senescence response and stop growth, with negative yieldconsequences. Other germplasm is more resilient and will maintain growth andproductivity as much as possible. The latter phenotype will require successful inter-action between the different early responses to establish stress-specific responses.Genetic variation can occur at different levels of the response pathway. QTL (starswith letter “Q”) in different parts of the general stress response will affect responseto different abiotic stresses. QTL in the stress-specific responses are predicted toonly affect response to a particular stress. Targeting the genetic variation in thegte

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eneral stress response could be more successful, but may require additional QTL inhe stress-specific responses. QTL for stress-specific responses may have negativeffects for other stresses.

he energy required to establish the response. Firstly, the alteredellular environment requires changes in the cellular machin-ry to be put in place; adaptations of translation initiation androtein folding are commonly observed in stress-induced trans-riptomes [110,111]. Then, specially adapted metabolic proteinsre induced early in the stress response (Fig. 2). Many abiotictresses shut down photosynthesis, while photosynthates are a cru-ial source of energy. Sugars are transported from source to sinkissues via the phloem and are important signals for growth andevelopment, as well as response to various abiotic stresses. Sugarignalling and metabolism are therefore tightly linked to growthesponses [112]. ABA regulates stomatal conductance and photo-ynthetic activity, causing vegetative growth retardation. This haseen shown to contribute to vegetative stage abiotic stress tol-rance, but this growth repression also has a negative effect oneproductive processes [113]. Abiotic stresses repress the sucroseleaving enzyme cell wall invertase in anthers, preventing hex-se supply for pollen development and causing pollen sterility.BA accumulation was shown to directly or indirectly repress cellall invertase expression. Tolerant wheat and rice germplasm dis-layed different anther ABA homeostasis, maintaining lower ABA

evels than sensitive lines in response to cold and drought stress55–57,113]. Sugars and ABA are known to regulate ethylene andenescence responses [114]. Sugars are an important growth sig-al in plants and are therefore tightly connected with the decisiono grow or repress growth and respond to abiotic stress (Fig. 2).he glycolytic enzyme hexokinase (HXK) is a cellular sugar sen-or that cross-talks to several phytohormones [115]. Other cellular
omponents involved in regulation of metabolism in plants showome similarity to yeast. The mitogen-activated protein kinaseMAPK) [116,117] and the salt overly sensitive (SOS) pathwaysespond to osmotic stresses such as drought, cold and salt stress
29 (2014) 247–261 253

and are tightly integrated with signalling pathways for sugars,essential nutrients (nitrogen) and various hormones [118–120].The yeast SnRK (sucrose non-fermenting related kinase) relatedprotein kinases KIN10 and KIN11 play a central role in coordinatingsugar, stress and developmental signals with metabolic pathways,activating gene expression via bZIP transcription factors [121,122].The general control non-repressible related protein kinase (GCN-2) phosphorylates translation initiation factor 2 (eIF2�) and is ableto sense free amino acid levels, respond to osmotic stresses andcontrol protein synthesis [123,124]. Both SnRK1 and GCN-2 regu-late nitrate reductase and nitrogen metabolism [120,121]. Furtherresearch is required to establish how this complex metabolic reg-ulation mechanism is controlled by environmental stimuli. Theconservation of the kinases that regulate fundamental metabolicpathways between plants, yeast and animals illustrates their evo-lutionary importance.

3.4. Do abiotic stress response pathways overlap?

It has been demonstrated that treatment with one abiotic stresscan provide “cross-tolerance” or “hardening” to other stresses,including biotic stresses [125,126]. Pre-treatment of plants withthe stress hormone ABA has a similar effect [127–129]. Thisalready suggests that there must be some functional overlap inthe signalling and response pathways of abiotic stresses. Osmoticstresses (drought, cold, salinity, heat) involve ABA and are thereforeexpected to share common components. Furthermore, transcrip-tome analyses have confirmed that early macromolecule andoxidative stress protection is recruited by most stresses and is ageneral stress response (Fig. 2). Some developmental and metabolicresponses (e.g., growth adaptation, leaf senescence, pollen fertil-ity, induction of osmo-protectants by drought, cold and salinity)are also shared by different stresses. Communication between sinkand source tissues is especially important under abiotic stress con-ditions when growth can be limited by available resources. To fullyunderstand the impact of abiotic stresses on plant growth it isessential to further unravel the relationships between metabolismand developmental processes.

Due to gene redundancy, different gene copies encoding pro-teins with the same function can be activated under differentstresses, suggesting that overlap between different stresses couldbe larger at the protein level than at the transcript level. In eco-nomical terms, it seems logical that plants will share the responseto the initial threat and mount stress-specific responses once thegeneral response has created the environment to make this possi-ble (Fig. 2). A shared initial stress response may not require manygenes and some may have so far remained undetected in differen-tial gene expression studies. Regulation at the protein level, suchas targeted protein degradation using the ubiquitin proteasome, iscommonly used by plant hormones to regulate downstream devel-opmental signalling [130]. It is therefore possible that a rather small– but critically important – part of the overlap between differentabiotic stress responses has so far escaped detection.

3.5. Selection for tolerance to multiple abiotic stresses

Genetic diversity for abiotic stress tolerance is more likelyto occur in the early response mechanism than in the stress-specific responses that depend on the initial response (Fig. 2). Thedecision to continue growth or induce senescence and growtharrest is taken in this early response mechanism and it is animportant factor for determining productivity and abiotic stress
tolerance in crops. Selection for adaptation to specific environ-ments and productivity traits has affected many developmentalproperties and may also have modified the early response mecha-nism to stress. Selection against seed dormancy may have affected

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omeostasis of hormones that play a role in stress tolerance (ABA,A). Adaptation to seasonal conditions and different environments

n cereals has modified important growth processes such as dura-ion of photosynthesis, adaptation to day-length and altered ratef leaf senescence, which may also have changed the interactionetween plant hormones (ethylene, cytokinins). The stay-greenrait has therefore been thought of as a potential domesticationrait [45,131]. Analysis of stay-green QTL (e.g., sorghum) could leado positional cloning and identification of new genes involved inhis process [45,132].

In nature, frequent exposure to a combination of stresses mayave selected a shared genetic adaptation mechanism to thosetresses. This may be the case for heat and drought stress whichften occur at the same time in field conditions [126,133]. It there-ore makes sense to select germplasm that is tolerant to more thanne abiotic stress [126], especially since different abiotic stressesponses may already share a common initial response mech-nism (Fig. 2). Germplasm that establishes the initial responseuccessfully may also be better able to establish a stress-specificesponse (Fig. 2). However, selecting germplasm that is tolerant toore than one stress using the combination of those stresses may

e difficult to achieve because of quantitative and qualitative differ-nces in tolerance to the combination of stresses and the difficultyo choose physiologically relevant selection conditions for the com-ination of stresses. We are currently using a step-wise selectionrocedure to first identify wheat lines that are tolerant to multiplebiotic stresses individually (drought, heat, shading and cold). QTLapping using this tolerant germplasm can also be used to iden-

ify overlapping general stress-response QTL, as well as QTL thatre specific for different stresses. Obtaining high levels of abiotictress tolerance may ultimately require combining both generaltress response and stress-specific QTL. However, for some traits itay be difficult to obtain tolerance to a combination of stresses;

ome traits for drought (stomata closed to prevent water loss) andeat stress (open stomata to reduce leaf temperature) are mutuallyxclusive [126].

.6. Transgenic approaches for abiotic stress tolerance

It is common practice in molecular biology to use proof-of-oncept transgenic approaches (over-expression, RNAi) to evaluateandidate genes for their effect on abiotic stress tolerance. Manyenes have indeed been shown to improve abiotic stress tol-rance ([134]; see Plant Stress website for a comprehensiveisting: www.plantstress.com/files/abiotic-stress gene.htm). Thesenclude transcription and regulatory factors, osmo-protectants,ormone and oxidative stress-related genes, molecular chaper-nes, transporters and various metabolic genes. Abiotic stressolerance for most of these genes was evaluated under controllednvironment or glasshouse conditions, using model systems suchs Arabidopsis or tobacco and some were also evaluated in cerealsrice, wheat, barley, maize). Relatively few transgenic lines haveo far made any impact for improving field abiotic stress toler-nce [135]. Potential explanations are that the field environments much harsher, transgenes only partially improve the abiotictress response or they improve response to one stress and not aombination of stresses. Differences in evaluation criteria for abi-tic stress tolerance may also be a contributing factor; in modellants tolerance is usually measured as survival under vegetativetage stresses, while in crops maintenance of productivity duringeproductive stage stresses is important [136,137]. The choice ofromoter to drive transgene expression is also important. Strong
onstitutive promoters lead to ectopic expression of a transgene,otentially causing adverse secondary effects on crop productiv-
ty. CBF/DREB transcription factors can improve osmotic stressolerance but result in stunted growth when using constitutive

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promoters [138]; plants look normal when a strong drought-inducible promoter is used that expresses the transgene only whenrequired [139]. The quantitative and qualitative properties of thepromoter driving a transgene may be particularly critical in the caseof transcription factors, hormone metabolic and signal transductiongenes. Using Arabidopsis as a model system it may be extremely dif-ficult or impossible to fully evaluate and predict potential adverseeffects in crop species [139]. In the case of multigene families itis often difficult to find out which gene to use for transforma-tion. For instance, only a few aquaporin gene family members areaffected by stress and lead to improvement of drought tolerance intransgenic plants [140]. For large transcription factor families, trialand error approaches can identify which gene has a positive effecton stress tolerance [141]. Some transgenic approaches may resultin morphologically different plants where stress phenotypes aresimply delayed (e.g., smaller leaf area reduce transpiration underdrought), giving transgenics an unfair advantage [142]. Manipu-lation of cytokinin levels using a stress-induced promoter led todelayed senescence and improved drought tolerance in rice underglasshouse conditions [143]. It is possible that these transgeniclines may also perform well under field drought conditions, consid-ering the field experience with stay-green plants. Interestingly,transgenic rice and maize plants expressing an E. coli cold shockprotein that acts as RNA chaperone in cellular protection resultedin improved tolerance to multiple stresses (cold, drought and heat)in field experiments [88], suggesting that focusing on the manipu-lation of the top of the stress signalling cascade using general stressresponsive genes may yield positive results.

4. Coordination of growth responses to abiotic stress

4.1. Do plants have brains?

How are the early responses to abiotic stresses orchestrated bysignals from the environment? Higher animals are mobile and reactto stress by escaping environmental challenges. The brain processesenvironmental signals via the central nervous system and regulatesthis mobility and escape reaction. The flexibility of plant develop-ment in response to environmental change indicates that they havean efficient systemic signalling mechanism that coordinates andorchestrates the response to adverse environmental conditions.The plant vascular system bears some resemblance to an animalcentral nervous system, sparking some speculation that plants havea cellular communication mechanism similar to animals [144]. Spe-cific proteins known to play a role as neurotransmitters in animals(e.g., glutamate receptors, 14-3-3 proteins) are also encoded inplant genomes but they acquired different functions when plantsevolved into multicellular organisms. The vascular system plays animportant role in coordinating growth and development betweenthe different plant parts [145], but the signalling mechanism isvastly different to that of animals. Plants have evolved their ownsystemic signals to drive growth and development (Fig. 2). Beingphotosynthetic organisms, they use photosynthates and the capac-ity to produce sugars as a resource signal for growth. They alsoadapted reactive oxygen species as a signal for abiotic stress. Plantshave evolved their own hormone signals, which are totally unlikeanimal hormones, to signal developmental and growth responses.An emerging theme in plant biology is the observation that manygenes involved in hormone synthesis and signalling, e.g. thoseinvolved in ABA synthesis and signalling [58,146], are expressedin vascular parenchyma cells. This allows rapid signal perception
and distribution via the vascular system, similar to a nervous sys-tem but at a slower pace. Environmental signals can therefore besensed in any plant part and quickly spread throughout the plant,suggesting that plants have essentially obviated the need for a
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entral nervous system. Despite its importance, the signal trans-itting function of the vascular system still needs to be unravelled

147]. Understanding of how the signals (hormones, ROS, metabo-ites) themselves work is gradually emerging. Auxins can beransported all over the plant using directional efflux carriersnd long-distance transporters and tissue-specific response mech-nisms make it possible to mount different auxin responsesn different plant parts [148]. These different plant parts arere-programmed to react differently to plant hormone signals,xplaining how environmental signals can have different but coor-inated responses. Hormonal signals therefore form an important

ink between the environment and developmental processes. Plantvolution and global diversity is testimony that plants have evolvedfficient systems to manage and adapt to environmental chal-enges.

.2. Growth inhibition responses

The key to understanding abiotic stress tolerance residesn understanding the plant’s capacity to accelerate/maintain orepress growth. Interaction between plant hormones must playn important role in this phenomenon. Most plant hormones play

role in development and have been implicated in abiotic stressesponses. A lot of progress has been made in recent years in under-tanding their function. Plant hormones can be growth-retardingABA, ethylene, jasmonic acid) or growth-promoting (auxin, gib-erellic acid, cytokinin). Two recently discovered plant hormones,rassinosteroids [149] and strigolactones [150] act in conjunctionith auxins and can be classified as growth promoting hor-ones, while salicylic acid functions in plant defence responses to

athogens [151]. The stress hormone ABA is implicated in stomatallosure and regulation of plant water balance, which impairs photo-ynthesis and restricts growth [113]. ABA levels are up-regulatedn response to osmotic stresses (drought, cold, salinity) and heattress. Higher ABA levels improve stress tolerance at the vegeta-ive level, but there is a compromise at the reproductive level. QTLnalysis in maize indicated that lines with higher root ABA lev-ls had lower grain yield [152] and our own work demonstratedhat lower ABA levels in stressed anthers was correlated with bet-er cold and drought tolerance, as well as maintenance of antherink strength in rice [58]. The ABA signalling pathway interactsith other hormones and sugar signalling via the SnRK network

98,123]. ABA’s restriction of photosynthesis and photosynthatellocation to sink tissues may help in shorter periods of abiotictress, but is destructive under longer term stress conditions suchs terminal drought. The opposing effect of ABA on vegetative andeproductive structures indicates that it is important to understandhe effect of abiotic stress during plant development. The success ofransgenic approaches for manipulation of abiotic stress toleranceill depend on carefully targeting the control of ABA homeostasis

o particular tissues and growth stages.Growth repression under abiotic stress conditions is associated

ith induction of leaf senescence (Fig. 3) or programmed cell deathesponses in tissues such as the anther tapetum [153,154]. Exter-al application and stress-induced accumulation of ABA results

n senescence, but the role of ABA in this process is still unclear.BA may interact with the oxidative stress response that pro-

ects against senescence [155], but may also cause senescenceia interaction with ethylene. The role of ethylene in inducingeaf senescence and inhibition of root elongation has been wellnvestigated. Antisense repression of ethylene biosynthesis inhibitsenescence, and the limitation of ethylene production has in many
ases resulted in improved abiotic stress tolerance [156]. Ethylenean induce the biosynthesis of the growth-promoting hormoneuxin in a tissue-specific manner [157]. The role of ethylene canherefore also be growth-promoting; low light (etiolation) and
29 (2014) 247–261 255

shading conditions cause elongation growth in shading-sensitiveplants [158]. Ethylene is in a unique position to control plant devel-opmental processes: it can act as an inhibitor of growth, but also asa growth promoter (Fig. 4).

Jasmonic acid can also induce senescence. In Arabidopsis,jasmonate-induced senescence involves induction of the transcrip-tion factor WRKY57, which is repressed by the growth hormoneauxin [159]. In addition, jasmonate induces expression of ICE(inducer of CBF expression), thereby promoting freezing toler-ance in Arabidopsis [160]. Ethylene and jasmonate can regulateeach other’s homeostasis via feedback regulation, producing a finebalance between growth repression (jasmonic acid) and growthstimulation (ethylene).

4.3. Growth stimulation responses

The growth hormone group of cytokinins plays a role in con-trolling cell division. Cytokinins counteract the effect of ethylene,preventing senescence and stimulating sugar metabolism andsink strength. Over-expression of the cytokinin biosynthetic geneisopentenyl transferase has been used to produce plants thatshow delayed senescence (stay-green trait), increased biomassproduction and improved stress tolerance [45,131]. However, thestay-green trait is not always associated with increased yield andproductivity [131], suggesting that increased cytokinin levels ben-efit vegetative growth but not reproductive development.

Gibberellins (GA) play a crucial role in the promotion of plantelongation growth. In the absence of GA, elongation growth isrestrained by DELLA nuclear proteins. In the presence of GA, DELLAproteins bind to the GA-GID1 receptor complex, targeting it fordegradation by the ubiquitin-26S proteasome and thereby acti-vating GA signalling and elongation growth [161]. Some DELLAmutants are unable to bind the GA-GID1 complex, causing itto escape proteasome degradation. This suppresses elongationgrowth, causing a semi-dwarf phenotype. Other DELLA mutantsabolish its repression activity, resulting in a tall stature (slender);these mutants are also male sterile, suggesting that DELLA proteinsplay a role in pollen development [162]. Mutations in GA biosyn-thesis genes and DELLA proteins with a semi-dwarf phenotypeincrease yield in cereals and have formed the basis of the GreenRevolution [163]. However, some GA-insensitive dwarf mutantsin wheat (reduced height; Rht) also have reduced pollen viabil-ity, which has been associated with reduced tolerance to abioticstresses such as heat and drought [162,164]. Interestingly, thegrowth-stimulation of GA can be counteracted by environmen-tal stresses and hormones such as ethylene and auxins, whichaffect the growth restraining activity of DELLA proteins [165–167].In Arabidopsis, the CBF/DREB cold-inducible transcription factorsactivate cold acclimation and freezing tolerance. CBF1 was shownto induce DELLA gene expression and activate GA catabolic genes,causing growth repression [168,169]. Stress-induced accumula-tion of ABA antagonizes GA action by controlling DELLA activity[170]. In addition, DELLA proteins play a role in mounting a pro-tective response to oxidative stress [169,171]. The DELLA proteinsobviously form a hub of hormonal and environmental interactionsthat determine continuation or repression of growth in function ofenvironmental cues [159].

4.4. An old legend born again: auxins

Auxins were the first plant hormone to be discovered. Thegrowth-promoting properties of auxins have gained increasing
prominence in recent years because of their role in regulatingdevelopment and response to abiotic stress. Auxins are synthesizedin the shoot apical meristem and are transported to neighbouringtissues and over longer distances using efflux carriers and polar


Fig. 3. Effect of drought stress at the reproductive stage in wheat. Drought stress leads to extensive leaf senescence in wheat (top left). Re-watering results in the developmento pmenr respon

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f new freshly green tillers that will flower and produce grains, while grain develoight). The close-up pictures at the bottom show prolific initiation of new tillers in

ransporters respectively. Auxins stimulate root growth and otherissue-specific responses throughout the plant such as leaf andruit senescence [148]. In Arabidopsis this requires cross-talk withasmonic acid signalling and the transcription factor WRKY57161,172,173].

One of the oldest known effects of auxins is the control ofpical dominance and shoot branching (tillering in cereals). Cut-ing the main stem of a plant removes the apical meristemhere auxins are made, resulting in increased branching. The

ranching response involves interaction with strigolactone andequires adequate sugar supply to support axillary bud out-rowth [174,175]. It has been demonstrated that auxin treatmentmproves fertility in heat-stressed barley plants [176]. Auxinsave a role in stamen development and are actively synthesized

n the anther, controlling pollen development and anther dehis-ence [177]. Apical dominance may play an important role in
romoting reproductive development and grain yield in cereals.uxins are synthesized in the anthers towards maturity where
hey play a role in anther senescence [177,178]. At the startf reproductive development in cereals the shoot apex where

t in the older stressed tillers is either aborted or leads to spikes without grain (topse to re-watering after drought treatment.

auxins are synthesized changes into a flowering meristem. It thendevelops into a spike containing the reproductive organs. Thepresence of auxin biosynthesis in the floral organs at this stagemight signify that apical dominance is controlled by the reproduc-tive structures. This function may be essential to direct resourcesto the reproductive structures for seed production rather thaninvesting them in further vegetative growth. Abiotic stresses incereals cause pollen sterility in sensitive lines, resulting in increasedtillering after the stress period (Fig. 3). This may reflect the lossin apical dominance as a result of pollen sterility. An intrigu-ing aspect of auxins is that they regulate some aspects of plantdevelopment such as lateral root development synergistically withethylene and other hormones, while for some aspects both hor-mones act antagonistically [179]. Recent progress in understandingplant hormone action is illustrating the complexity of cross-talkbetween different plant hormones and the importance of con-
trolling hormone homeostasis. Understanding the intricacies ofthese interactions is important to unravel how genetic variabil-ity in the network can affect how plants adapt to environmentalchange.

R. Dolferus / Plant Science 229 (2014) 247–261 257

F ironmr s of gr

4

dprptpttlomtDpeasebtlainliarrlotgeas

ig. 4. Simplified schematic representation of the components involved in the envesponse pathway in Arabidopsis. The PIF and DELLA proteins are central regulator

.5. Coordination of environmental responses

Progress made in unravelling how plants react to low light con-itions provided a clue as to how environmental signals regulatelant growth. Phytochrome photoreceptors react to changes in theatio between red and far-red light and play an important role inhotomorphogenesis. Phytochromes respond to darkness (etiola-ion) and changes in the red to far-red light ratio, which warns thelant about competing vegetation (shade avoidance) [158]. Phy-ochromes control many growth processes from seed germinationo reproductive development and they are well known to modu-ate biotic and abiotic stress responses [180]. The activated formf phytochrome moves to the nucleus and forms a complex withembers of the basic helix-loop-helix (bHLH) transcription fac-

ors, the phytochrome interacting factors (PIF). PIFs interact withELLA proteins; in the absence of GA, DELLA proteins bind to PIFs,reventing them from regulating their target genes. In the pres-nce of GA, DELLA proteins are degraded, PIFs become functionalnd elongation growth is activated [161,181,182] (Fig. 4). PIF tran-cription factors also activate auxin biosynthesis and their ownxpression is controlled by the circadian clock; the ArabidopsisZIP transcription factor Hy5 (elongated hypocotyl) promotes pho-omorphogenesis by antagonizing PIF action and the RING-motif E3igase COP1 (constitutive morphogenic) inhibits Hy5. This pathwaylso influences CBF function and freezing tolerance [183]. PIFs formn combination with DELLA proteins a hub for the integration of sig-als from various hormones [182,184–186], day-length [183,187],

ight quality [158,183], as well as sugars [188] (Fig. 4). Light qual-ty is also important for the induction of CBF transcription factorsnd activation of cold and frost tolerance [189,190] and PIFs play aole in regulating expression of DREB transcription factors that areequired for drought responses [182,191]. Low red to far-red ratiosead to increased levels of ethylene [158], which affects the stabilityf the DELLA proteins [165] (Fig. 4). Induction of the ERF transcrip-ion factor SUB1A under flooding conditions prevents elongation
rowth by increasing DELLA levels, thereby inhibiting GA-mediatedlongation growth [37,38]. The PIF transcription factors also medi-te cross-talk with ROS signalling [192]. These findings demon-trate how different environmental stimuli converge into a single,
ental response module that controls plant growth, based on the shade avoidanceowth and environmental responses in plants.

complicated signalling hub that orchestrates plant growthresponses. This environmental response hub may explain why oneabiotic stress can improve the response to other stresses (Section3.4).

5. Conclusions

In the last decade important progress has been made usingmodel plants in understanding how plants grow and develop andhow they respond to changes in the environment. This know-howis still fragmentary and needs to be extended to crop plants. Inimportant crop species such as cereals, it is important to maintainproductivity under abiotic stress conditions during the reproduc-tive stage. Some crop plants appear to overreact and switch togrowth arrest too quickly, even when survival is not immediatelyunder threat. One way of improving stress tolerance and grain pro-ductivity in cereals would be to increase the threshold level atwhich plants switch from promotion to arrest of growth. At thevegetative stage, the stay-green trait has achieved this by selectingfor delayed senescence. Maybe an equivalent of the stay-green traitis required to protect the reproductive stage and grain formationin cereals. Seed production itself is a stress survival mechanism;seed can survive prolonged stress conditions in dehydrated stateand this guarantees the plant’s next generation. This potential mayhave been lost from crop plants, but genetic diversity to reintro-duce this trait may still be available in breeding lines, landracesor wild progenitor species. This material can also be used to fur-ther improve our understanding of the hormonal interactions thatcontrol growth.

A lesson could be learned from flooding tolerance research,which showed that both growth arrest and acceleration can be ben-eficial – depending on the circumstances. This response requiresethylene and ERF transcription factors. The molecular basis of howflooding tolerance interacts with the environmental response hub
can serve as a guideline for other abiotic stresses. Response toshading also shares some of the hub components used by flood-ing stress. Importantly, the example of flooding stress indicatesthat avoidance and/or escape reactions should not necessarily be

2 ience 2

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rotrtdtniirothroRtiSi(ontsnsuhgaf

raci

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DCfrTn

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reated as different or independent from true tolerance responses.he common denominator is “growth regulation”. It is crucial thate learn to understand how plants regulate growth in function of

nvironmental restraints; this may lead to strategies to manipulatehe threshold levels to switch from growth arrest to maintenancef growth. Crop plants such as cereals, combined with current tech-ologies, can help us to reach that level of understanding.

Having a single regulatory hub to integrate all environmentalesponses and regulate plant growth and development makes a lotf sense, but a lot of questions still need to be answered. We needo get a better understanding about systemic signalling and theelationship between vegetative and reproductive growth. Duringhe stage of flowering and seed production, a plant behaves quiteifferently from a plant during vegetative growth. Even thoughhere is a shared response system to the environment, growth sig-als still need to be relayed to different plant parts and the effect

n different plant parts can be interpreted very differently. Fornstance, nitrogen application can stimulate vegetative growth andepress reproductive development. In cereals, grain yield dependsn successful interaction between both vegetative and reproduc-ive growth. While management, agronomy and breeding practicesave focused a lot on the vegetative establishment phase of cereals,elatively little is known about the control of reproductive devel-pment and its interaction with the environment. The use of Greenevolution genes in cereals has shown that reducing stem elonga-ion growth using semi-dwarf genes benefits grain yield, but theres a trade-off in terms of abiotic stress tolerance and pollen fertility.ome semi-dwarf mutations affect the function of DELLA proteinsn the central hub controlling growth and abiotic stress responsesFig. 4). This raises the question whether high yield and high abi-tic stress tolerance are compatible – or not. There is a strongeed to fully understand the function of the central environmen-al response hub (e.g., role of PIF family members, identification oftill unknown components), but the use of model systems only mayot allow us to achieve this and genetic variation in crop specieshould be included in these studies. Analysing this genetic variationsing new generation genotyping and phenotyping technologiesas vastly improved and identification of candidate stress toleranceenes is made easier using genomics. Proof-of-function transgenicpproaches may also lead to identification of genes that can be usedor stress-proofing cereals.

The technological revolution of the last decade has providedenewed hope for improving abiotic stress tolerance in crops suchs cereals, but it is clear that this effort will increasingly requirelose interaction between plant scientists of different disciplines,ncluding bioinformaticians and engineers.

cknowledgements

R.D. is supported by grants from the Grains Research andevelopment Corporation (GRDC, grants CSP00130, CSP00143 andSP00175). The author thanks Jane Edlington and Holly Staniford

or their help in preparing the manuscript. The number of citedeferences in this review paper has been limited by journal policy.he author apologizes to those authors whose publications wereot cited in this paper.

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