Shair H.Wani*，Vinay Kumar*，Varsha Shriram，Saroj Kumar SahDivision of Genetis an Plant Breeing，F(xiàn)aulty of Agriulture WADURA，Sher-e-Kashmir University of Agriultural Sienes an Tehnology，Kashmir 191121，IniaDepartment of Biotehnology，Moern College of Arts，Siene an Commere，S.P.Pune University，Ganeshkhin，Pune 411016，IniaDepartment of Botany，Prof.Ramkrishna More College，S.P.Pune University，Akuri，Pune 411044，IniaDepartment of Biohemistry，Moleular Biology，Entomology an Plant Pathology，Mississippi State University，MS 39762，USA

?

Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants

Shabir H.Wania，*，Vinay Kumarb，*，Varsha Shriramc，Saroj Kumar SahdaDivision of Genetics and Plant Breeding，F(xiàn)aculty of Agriculture WADURA，Sher-e-Kashmir University of Agricultural Sciences and Technology，Kashmir 191121，India
bDepartment of Biotechnology，Modern College of Arts，Science and Commerce，S.P.Pune University，Ganeshkhind，Pune 411016，India
cDepartment of Botany，Prof.Ramkrishna More College，S.P.Pune University，Akurdi，Pune 411044，India
dDepartment of Biochemistry，Molecular Biology，Entomology and Plant Pathology，Mississippi State University，MS 39762，USA

A R T I C L E I N F OA B S T R A C T

Article history：

Received in revised form

15 January 2016

Accepted 15 March 2016

Available online 1 April 2016

Phytohormones

Abiotic stress

Metabolic engineering

Plant stresses

Abiotic stresses including drought，salinity，heat，cold，flooding，and ultraviolet radiation causes crop losses worldwide.In recent times，preventing these crop losses and producing more food and feed to meet the demands of ever-increasing human populations have gained unprecedented importance.However，the proportion of agricultural lands facing multiple abiotic stresses is expected only to rise under a changing global climate fueled by anthropogenic activities.Identifying the mechanisms developed and deployed by plants to counteract abiotic stresses and maintain their growth and survival under harsh conditions thus holds great significance.Recent investigations have shown that phytohormones，including the classical auxins，cytokinins，ethylene，and gibberellins，and newer members including brassinosteroids，jasmonates，and strigolactones may prove to be important metabolic engineering targets for producing abiotic stress-tolerant crop plants.In this review，we summarize and critically assess the roles that phytohormones play in plant growth and development and abiotic stress tolerance，besides their engineering for conferring abiotic stress tolerance in transgenic crops.We also describe recent successes in identifying the roles of phytohormones under stressful conditions.We conclude by describing the recent progress and future prospects including limitations and challenges of phytohormone engineering for inducing abiotic stress tolerance in crop plants.

?2016 Crop Science Society of China and Institute of Crop Science，CAAS.Production and hosting by Elsevier B.V.This is an open access article under the CC BY-NC-ND license

（http://creativecommons.org/licenses/by-nc-nd/4.0/）.

1.Introduction

The human population is rapidly increasing and needs a substantial increase in agricultural productivity worldwide. However，various biotic and abiotic stresses are major factors limiting crop productivity［1］.To feed the world population，productivity must be increased by 70%for an additional 2.3 billion people by 2050［2］.The mechanisms underlying environmental stress response and tolerance in plants are different and more complex than animals［3］.Identifying the principles by which plants respond to various environmental stresses is one of the critical aspects for plant biotechnologists.Amongst various abiotic stresses，drought，salinity，and extreme temperatures are most widespread and significant［4］.Because of the complexity of stress tolerance traits，conventional breeding techniques have met with limited success.They demand effectiveadvancestofeedthegrowingworldwidefooddemand. In this direction，novel and potent approaches should be devised.Engineering of phytohormones could be a method of choice to produce climate-resilient crops with high yields.

Phytohormones are molecules produced in very low concentrations but able to regulate a variety of cellular processes in plants.They work as chemical messengers to communicate cellular activities in higher plants［5］.Phytohormones play key roles and coordinate various signal transduction pathways during abiotic-stress response.They regulate external as well as internal stimuli［6］.Some phytohormones，such as ABA，have been identified as stress hormones.ABA plays critical roles in plant development: maintenance of seed dormancy，inhibition of germination，growth regulation，stomatal closure，fruit abscission，besides mediating abiotic and biotic stress responses［7］.Phytohormone engineering could be a perfect platform for biotechnologists to improve cropsnutritionally and economically.In this review，we present an overview of the phytohormones and their roles in plant growth，development，and abiotic stress response，in addition to their metabolic engineering to confer abiotic stress tolerance in crop plants to increase food quantity and quality. We discuss recent successes and future prospects.

2.Abiotic stresses：Challenging the changing world

Investigating how abiotic stresses affect plant growth and development at the physiological，biochemical，and molecular levels is critical to increasing the productivity of crops，because stresses cause widespread crop losses throughout the world［6］.Environmental factors imposing stress on plants，including drought，salinity，heat，chilling，freezing，ozone，pathogens，and UV radiation are the major environmental cues that limit crop productivity.The period and development of stress，stages of the plant，and biotic and abiotic factors may influence the stress response［8］.Some crops may be affected at an early stage，but recover and finally survive.Susceptibility or resistance to stresses may differ markedly among species or genotypes of crops.Among these stress conditions，drought is perhaps the most severe stress，responsible for decreased agricultural production worldwide. It affects plants in many ways:plant growth，membrane integrity，pigment content，osmotic adjustments，water relations，and photosynthetic activity［9，10］.As rightly pointed out by Postel［11］，water will be the oil of the 21st century.Many rivers around the globes are drying daily；most have no water to discharge to the sea［11］.After drought，salinity is the second major stress reducing crop productivity.Various plant hormones have shown positive plant-protective functionsagainst abiotic stresses and attempts have been made to assign specific hormone（s）for specific stresses as well as combinations of stresses，as some hormones have shown multiple stress-resistance functions.

3.Importance of studying plant stresses in combination

Previously，to study abiotic stress conditions，generally specific stress conditions were investigated，including drought，salinity，or heat，and the diverse molecular aspects of plant acclimation were analyzed.However，conditions differ in the natural environments.In nature，crops face different stresses or combinations of stresses found in the environment.The majority of molecular studies are conducted under controlled conditions in the laboratory or greenhouse and do not reflect the actual conditions that occur in the field.In the laboratory or greenhouse，conditions are controlled so that one stress is imposed，but in natural conditions there are many environmental stresses that are applied in combination. Therefore，the experiments conducted for evaluating effects of a combination of stress factors rather than an individual stress may prove advantageous.Drought and heat stress in combination caused losses of$200 billion in the USA（readers are encouraged to refer to the excellent review of Suzuki et al.［12］）.

4.Phytohormones：Key mediators of plant responses to abiotic stresses

Plants must regulate their growth and development to respond to various internal and external stimuli［13］.Phytohormones，a diversegroupofsignalingmoleculesfoundinsmallquantitiesin cells，mediate these responses.Their pivotal roles in promoting plant acclimatization to ever-changing environments by mediating growth，development，source/sink transitions，and nutrient allocation have been well established［14］. Although plant response to abiotic stresses depends on various factors，phytohormones are considered the most important endogenous substances for modulating physiological and molecular responses，a critical requirement for plant survival as sessile organisms［14］.Phytohormones act either at their site of synthesis or elsewhere in plants following their transport［15］.Phytohormones are of key importance in plant development and plastic growth.They include auxin （IAA），cytokinins（CKs），abscisic acid（ABA），ethylene（ET），gibberellins（GAs），salicylic acid（SA），brassinosteroids（BRs），and jasmonates（JAs）.The strigolactone（SL）are relatively new phytohormones.Fig.1 shows the chemical structures of major phytohormones.

4.1.Abscisic acid（ABA），the abiotic stress hormone

Abscisic acid（ABA）owes its name to its role in abscission of plant leaves and is perhaps the most studied phytohormone for its response and distinct role in plant adaptation to abiotic stresses，and is accordingly termed a“stress hormone.”It is an isoprenoid plant hormone produced in the plastidal 2-C methyl-D-erythritol-4-phosphate pathway.ABA plays an influential during several plant physiological processes and developmental stages including seed dormancy and development，stomatal opening，embryo morphogenesis，and synthesis of storage proteins and lipids［16］.

ABA is considered an essential messenger in the adaptive response of plants to abiotic stress and its role in stress tolerance has received much attention.In response to environmental stresses，endogenous ABA levels increase rapidly，activating specific signaling pathways and modifying gene expression levels［17］.Nemhauser et al.［18］have reported that ABA transcriptionally regulates up to 10%of protein-encoding genes.ABA also acts as an internal signal enabling plants to survive under adverse environmental conditions［19］.

Under water-deficit conditions，ABA plays a vital role in providingplantstheabilitytosignaltotheirshootsthattheyare experiencing stressful conditions around the roots，eventually resulting in water-saving antitranspirant activity，notably stomatal closure and reduced leaf expansion［20］.ABA is also involved in robust root growth and other architectural modifications under drought stress［21］and nitrogen deficiency［22］. ABA regulates the expression of numerous stress-responsive genes and in the synthesis of LEA proteins，dehydrins，and other protective proteins［23，24］.ABA upregulates the processes involved in cell turgor maintenance and synthesis of osmoprotectants and antioxidant enzymes conferring desiccation tolerance［25］.Zhang et al.［26］reported a proportional increase in ABA concentration upon exposure of plants to salinity.

4.2.Auxins（IAA） Although auxin has been studied for over 100 years，its biosynthesis，transport，and signaling pathways are still not clear［27］.However，some interconnecting pathways have been proposed so far for biosynthesis of auxin in plants，including four tryptophan（Trp）-dependent and one Trp-independent pathway［28］.IAA（indole-3-acetic acid）is one of the most multi-functional phytohormones and is vital not only for plant growth and development but also for governing and/or coordinating plant growth under stress conditions［29］.The presence of an auxin biosynthesis，signaling，and transport apparatus in single-celled green algae is clear evidence of the evolutionary role played by auxin during the adaptation of plants to diverse land environments［30］.Though there has been a recent upsurge in our understanding of auxin regulation of plant growth and development，its role as a regulator of stress response is still little understood［29］.

Interestingly，there is growing evidence that IAA plays an integral part in plant adaptation to salinity stress［14，31］.It increasesrootandshootgrowthofplantsgrowingundersalinity or heavy metal stresses［32，33］.Salinity reduced IAA levels in maize plants，but salicylic acid application effectively increased them［34］，indicating that hormonal balance and crosstalk are critical to signal perception，transduction，and mediation of stressresponse［14］.Auxinstimulatesthetranscriptionofalarge numberofgenescalledprimaryauxinresponsegenes，andthese genes have been identified and characterized in several plant species including rice，Arabidopsis，and soybean［35］.Auxin is regarded as an influential constituent of defense responses via regulation of numerous genes and mediation of crosstalkbetween abiotic and biotic stress responses［36］.However，identification of novel genes involved in stress responses may prove to be a vital target for engineering abiotic stress tolerance in principal crops.

Fig.1-Major classes of phytohormones involved in abiotic stress response and tolerance in plants.

4.3.Cytokinins（CKs） CKs play influential roles in many plant growth and developmental processes and are considered as master regulators during plant growth and development［37，38］.Alteration of endogenous levels of CKs in response to stress indicates their involvement in abiotic stress［17］，including drought［37］and salinity［38］.Mutants and transgenic cells/tissues with altered activity of cytokinin metabolic enzymes or perception machinery points toward their crucial involvement in several crop traits including productivity and increased stress tolerance［39］.

Although plant responses to CKs have been evaluated most often via their external application，stressful conditions are also known to enhance their endogenous levels via uptake and enhanced biosynthesis［40］.In contrast to the ABA inhibition of seed germination，they also release seeds from dormancy［36］.CKs are often considered ABA antagonists［41］.In water-stressed plants，decreased CK content and accumulation of ABA lead to an increased ABA/CK ratio. The reduced CK levels enhance apical dominance，which，together with the ABA regulation of stomatal aperture，aids in adaptation to drought stress［17］.

4.4.Ethylene（ET）

ET，a gaseous phytohormone，is involved in several phases of plant growth and development，notably fruit ripening，flower senescence，and leaf and petal abscission，besides being an essential regulator ofstress responses［42，43］.It isbiosynthesized from methionine via S-adenosyl-L-methionine（AdoMet）and the cyclic non-protein amino acid ACC.ACC synthase convert AdoMet to ACC，while ACC oxidase catalyzes the conversion of ACC to ethylene.

Abiotic stresses including low temperature and salinity alter endogenous ET levels in plants.Enhanced tolerance was accordingly achieved with higher ET concentrations［44］.ET also plays a major role in the defense response of plants to heat stress［45］.Environmental stress induces ET accumulation which increases plant survival chances under these adverse conditions［42］.ET has been proposed to function via modulation of gene expression considered as the effectors of ethylene signal［46］.

ET in combination with other phytohormones such as JA and SA often acts cooperatively.These are considered the main players involved in regulating plant defense against pests and pathogens［6］.The biosynthesis，transport，and accumulation of these hormones trigger a cascade of signaling pathways involved in plant defense［47］.As concluded by Yin et al.［48］，ET and ABA seem to act synergistically or antagonistically to control plant growth and development.

4.5.Gibberellins（GAs）

The gibberellins（GAs）are a large group of tetracyclic diterpenoid carboxylic acids，but only a few of them function asgrowthhormonesinhigher plants，predominantformsbeing GA1and GA4［49］.The GAs show positive effects on seed germination，leaf expansion，stem elongation，flower and trichome initiation，and flower and fruit development［50］. They are essential for plants throughout their life cycle for growth-stimulatory functions.They also promote developmental phase transitions［51］.Interestingly，there is increasing evidence for their vital roles in abiotic stress response and adaptation［51］.Recently，experiments have been performed to investigate the role of GAs in osmotic stress response in Arabidopsis thaliana seedlings［52，53］.GAs are known to interact with all other phytohormones in numerousdevelopmental and stimulus-response processes［54］.The interactions between GAand ET include both negative and positive mutual regulation depending on the tissue and signaling context［54］.

4.6.Brassinosteroids（BRs） Brassinosteroids（BRs）comprise a relatively new group of polyhydroxy steroidal plant hormones with strong growth and development-promoting potential.They were first isolated and characterized in pollen of the rape plant（Brassica napus）. More than 70 BRs have been isolated from plants.However，brassinolide，28-homobrassinolide，and 24-epibrassinolide constitute the three most bioactive BRs and are widely used in physiologicalandexperimental studies［55］.Theyarepresentin almost every part of plants including pollen，flower buds，fruits，seeds，vascular cambium，leaves，shoots，and roots［56］.They play a critical role in numerous developmental processes such as stem and root growth，floral initiation，and development of flowers and fruits［56］.

However，recent findings suggest stress-impact mitigating roles of BRs and associated compounds in various plants subjected to various abiotic stresses.These abiotic stresses are high temperature［57］，chilling［58］，soil salinity［59］，light ［60］，drought［61］，flooding［62］，metals/metalloids［63］，and organic pollutants［64］.Recent research has shown tremendous potential of BRs and associated compounds in the modulation of components of antioxidant defense system in-response-to and to counteract the abiotic stress-induced oxidative burst，reviewed byVardhini and Anjum［65］. However，there is tremendous scope for further research focused on the sites，pathways，and enzymology of their biosynthesis，source-sink relationships，developmental and stress physiology，their interactions with microorganisms，fungi，and animals，and the realization of their powerful applications［14］.

4.7.Jasmonates（JAs）

The cyclopentanone phytohormones derived from the metabolism of membrane fatty acids including primarily methyl jasmonate（MeJA）and its free acid jasmonic acid（JA）are collectively called jasmonates（JAs）and are widespread in the plant kingdom.These multifunctional compounds are involved in crucial processes associated with plant development and survival including reproductive processes，flowering，fruiting，senescence，secondary metabolism，and direct and indirect defenseresponses［66，67］.JAisthemostabundant，best known，and best characterized of the JAs.In addition to developmental functions of plants，JA activates plant defense responses to pathogenic attack as well as environmental stresses including drought，salinity，and low temperature［68，69］.JAs are vital signaling molecules induced by various environmental stresses including salinity［68］，drought［69，70］，and UV irradiation［71］. They have great potential to mitigate an array of threatening environmentalstresses［72］.TheexogenousapplicationofMeJA effectively reduced salinity stress symptoms in soybean seedlings［73］.Remarkably，endogenous levels of JA increased in rice roots under salinity stress and reported to counteract the deleterious effects of salinity stress［74］.JAs applications alleviate heavy metal stress in plants by activating the antioxidant machinery［75］.MeJA confers tolerance in A. thaliana plants against Cu and Cd stress via accumulation of phytochelatins［76］.

4.8.Salicylic acid（SA） Salicylic acid（SA）is a naturally occurring phenolic compound involved in the regulation of pathogenesis-associated protein expression［77］.In addition to defense responses，it plays a vital role in the regulation of plant growth，ripening and development，as well as responses to abiotic stresses［78，79］.The synthesis of SA occurs via two pathways:the isochorismate（IC）andthephenylalanineammonia-lyase（PAL）pathway.Ofthese，the major pathway is the IC pathway in Nicotiana benthamiana ［80］and tomato［81］.

An interesting and noteworthy general belief is that low concentrations of SA enhance the antioxidant capacity of plants，but high concentrations of SA cause cell death or susceptibility to abiotic stresses［82］.Most genes that respond positively to acute SA treatment are associated with stress and signaling pathways that eventually led to cell death.SA consists of genes encoding chaperones，heat shock proteins，antioxidants，and genes involved in the biosynthesis of secondary metabolites，such as sinapyl alcohol dehydrogenase，cinnamyl alcohol dehydrogenase，and cytochrome P450 ［82］.

SA is involved in plant response to abiotic stresses such as drought［83］，salinity［34，84］，chilling［85］，and heat［86］.SA along with ABA is involved in the regulation of drought response［77］.Drought stress induced a five-fold increase in the endogenous levels of SA in Phillyrea angustifolia［87］.The SA content in barley roots was increased approximately twofold by water deficit［88］.The SA-inducible genes PR1 and PR2（pathogenesis-related genes）are induced by drought stress［83］.However，the detailed molecular mechanisms of SA's roles in abiotic stress tolerance remain largely unknown and more comprehensive investigations are needed in this direction.

4.9.Strigolactones（SL）

Strigolactones（SLs）constitutes a small class of carotenoidderived compounds，first characterized more than 45 years ago as seed germination stimulants in root parasitic plants such as Striga，Orobanche，and Phelipanche species［89，90］. Several types of SLs can be synthesized by single plant species，whereas mixtures of different types and quantities of SL molecules are produced in intraspecific varieties［89，91］. Although they are produced and exuded in small amounts primarily in roots，other plant parts can also synthesize them ［92］.A comparative study involving wild-type and mutant Arabidopsis plants indicates their role in the development of root system architecture［93］.Application of GR24，a synthetic and biologically active SL［94，95］，repressed lateral root formation in wild-type seedlings and SL-synthesis mutants （max3 and max4）but not in the strigolactone-response mutant （max2），suggesting the MAX2-dependent negative effect of strigolactone on lateral root formation［93，96］.Apparently，SLs are involved in plant responses to environmental stimuli from their early evolution.In higher plants，they participate in both shoot and root architecture in response to nutritionalconditions［97］.SLs also act as signaling molecules for plant interactions with microbes.They stimulate nodulationin the legume-rhizobium interaction process［98，99］.Overall，it can be concluded that SLs constitute an important group of signaling molecules and are key regulators of plants'developmental adaptations to changing environmental conditions. They have the potential to be used in agriculture for various purposes including as inducers of suicidal seed germination of parasitic plants［100］.

5.Crosstalk between phytohormones signaling

Environmental stresses require plants to perceive and react to these signals in a highly coordinated and interactive manner. Plants being sessile organisms need to maintain plasticity in growth and ability to adapt to harsh changing environmental conditions，and this adaptation is mediated by elaborate signaling networks.Signal transduction cascades that interact with the baseline pathways transduced by phytohormones get triggered by the perception of abiotic stresses［101］. The fluctuations of stress-responsive hormones help alter cellular dynamics and thus play a central role in coordinately regulating growth responses under stress conditions［102］. The convergence points among hormone signal transduction cascades are considered crosstalk，and together they form a signaling network［101］.In this way，hormones seemingly interact by activating either a common second messenger or a phosphorylation cascade.In the last few decades，insights into the biosynthetic and core signaling components of major phytohormones including ABA，IAA，BRs，GAs，JA，and ET have been revealed［103］.However，owing to the extreme complexity of responses to different stress thresholds，lack of knowledge about tissue-specific stress response，and inadequate understanding of genetic plasticity and its adaptability to environments，the mechanistic basis of abiotic stress tolerance remains largely unclear and confusing［102］.Consequently，all these factors collectively contribute to more confusion than resolution［104］.Still，perturbed phytohormone fluxes and the subsequent signal transduction cascade have been revealed as one of the primary stress responses evolved by plants.

Various plant hormones interact together for signal defense networking to fine-tune the defense against environmental challenges.Among them，SA，JA，and ABA hold particular importance and are regarded as key players in the regulation of signaling pathways.In recent years，deciphering the interactions between phytohormones and their coordinated roles in counteracting abiotic stresses has gained new attention. Experimentalfindingsunequivocallyshowthattheinteractions among phytohormones are the rule rather than the exception in integrating diverse input signals and readjusting growth and acquiring stress tolerance in plants［102］.The presence of multiple and frequent redundant signaling intermediates for each hormone hints at their apparent roles in such crosstalk. Understanding the crosstalk between phytohormonal and defense signaling pathwaysis thus important，as it may reveal new potential targets for the development of host resistance mechanisms and phytohormones［105］.

We now discuss stomatal closure as a rapid response to water deficit conditions and phytohormonal crosstalk in its regulation.Stomatal closure is regulated by a complex network of signaling pathways，and as a short-term response is triggered primarily by ABA.ABA controls long-term growth responses via the regulation of gene expression that favors maintenance of root growth，which optimizes water uptake ［26］.However，following the rules of drought stress response，ABA apparently interacts with other plant hormones and signaling molecules such as JA and nitric oxide（NO）to stimulate stomatal closure，whereas its regulation of gene expression includes the induction of genes associated with response to ethylene，cytokinin，or auxin［101］.It has been proposed by the authors that stress-induced JA production interacts with ABA-mediated stomatal closure by stimulating the influx of extracellular Ca2+and/or by activating H2O2/NO signaling［101］.In contrast，Desikan et al.［106］provided evidence that stomatal closure by ethylene is regulated via its signal transduction pathway，which both stimulates production and requires H2O2synthesis.This crosstalk also involves JA，whose biosynthesis is induced by stress conditions including herbivory［107］，whereas many JA-associated signaling genes are regulated by drought stress［108］.JA interacts with ABA-regulated stomatal closure by increasing Ca2+influx，which ultimately stimulates calcium-dependent protein kinase（CDPK）production and the resulting signal cascade［101］.A 10-min treatment with either ABA or MeJA resulted in a reduction of stomatal aperture in turgid and excised leaves of Arabidopsis［109］.The authors postulated that both ABA and MeJA interact in guard cells and induce the formation of reactive oxygen species and NO and that both are present at reduced concentrations in MeJA-insensitive plants.In another experiment，Kim et al.［110］found that drought stress induced a 19-fold increase in MeJA levels and a 2-fold increase in ABA levels，which was associated with severe yield loss due mainly to poor seed set.This phenotype was mimicked by concentrations of MeJA in young panicles of rice through the ubiquitous expression of AtJMT transgenically，which also led to a dramatic reduction in grain yield and a substantial increase inABA，suggestingcrosstalk betweenMeJA and ABA biosynthesis［110］.Similarly，long-term physiological responses to abiotic stress conditions are caused and influencedbyalteredABA-mediatedgeneregulationoftranscription factors（TFs）that bind to ABA-responsive elements（ABREs）on ABA-regulated genes.Notably，phosphorylation cascades like those signaling stomatal closure also lead to changes in ABA-regulated TFs.For instance，the ABA-responsive TFsABF1 andABF4areactivatedupontheirphosphorylationby ABA-inducible kinases CPK4 or CPK11［111］，as reviewed by Harrison et al［101］.

On a similar line，preferential upregulation of JA pathway genes under salinity stress in barley plants has been reported ［112］.Although the precise role of JA in drought and salinity remains unknown；it could be implicated as a molecule signaling cell death［102］.Nishiyama et al.［38］，studying gene expression，concluded that exogenous ABA treatment strongly downregulated isopentenyltransferase（IPT），a key cytokinin biosynthetic pathway gene，but upregulated genes encoding cytokinin oxidases and dehydrogenases.Further，in addition to its well-documented role in controlling plantgrowth and development in close associations with auxins and BRs［113］，GA is also involved in cross-talk of hormonal interactions in signaling environmental inputs［114，115］. Various recent reports make it clear that interplay between environmentally activated ABA，ET，GA，and CK signals is crucial in determining plant stress responses［3，116，117］.

There is evidence that some phytohormones also counteract adverse conditions.For example，a signal peptide system coupled with JA is reported to be involved in wound-induced salt-stress adaptation in tomato［118］，indicating cross-tolerance signaling.The possible roles of phytohormones in abiotic stress tolerance and crosstalk between phytohormone signaling are illustrated in Fig.2.

6.Recent attempts at deciphering the role of phytohormones in abiotic stress tolerance

6.1.Hormones help in pollen development under cold stress

Abiotic stress can affect any developmental stages，but the reproductive stage is perhaps most critical.If stresses are applied at the reproductive stage，it may damage the whole plant and ultimately reduce the crop yield.Further，among the various reproductive stages，pollen development is crucial and is affected by abiotic stresses such as drought，cold，and heat，leading to reduced crop yield［119］.In pollen development，pollen meiosis is the stage most sensitive to cold，which causes pollen sterility and also reduces anther dehiscence，pollen load to the stigma，pollen germination，and pollen tube growth［120，121］.Hormones such as GA and ABA are considered major signals for cold-induced pollen sterility and an understanding of molecular mechanism of pollen development under stress and non-stress conditions can be beneficial for hybrid seed production by producing novel sterile plants. In rice，Zhang and co-workers［122］developed a hybrid seed production line in the form of a new photoperiod-sensitive genetic male sterile line by using transcription regulation of pollen development；for details，see review by Sharma［123］.

Fig.2-The possible roles of phytohormones in abiotic stress tolerance and crosstalk between phytohormone signaling

6.2.Hormonal balance under cold stress

Kolaksazov et al.［124］reported that stress phytohormones such as ABA，JA，and SA triggerphosphoprotein cascade pathways，leading to expression of genes associated with cold stress tolerance.They reported high contents of JA in the three different populations at a controlled temperature of 22°C，with a 10-fold reduction in sensitive plants but no change intolerant plants at 4°C.

6.3.Salicylic acid increases germination，seedling growth，and enzymes activity

Gharib and Hegazi［125］showed that SA stimulated various growth aspects of bean seedlings，was responsible for biosynthesis of growth-promoting and-inhibiting substances，and reduced the adverse effect of cold stress in common bean.They conducted an experiment on six common bean varieties with optimal temperature 25°C and chilling stress at 15°C.They found that germination and seedling growth of the six varieties were slowed under chilling stress.Seeds treated with SA showed increased germination germination rate compared to untreated（control）seedsundercontrolaswellaschillingstress.

6.4.Hormone responsive protein mediated stress responses

In plant stress response，phytohormones play a vital role，and some proteins can be used for communication.Bhaskar et al. ［126］reported that C1-（cysteine rich protein family）domaincontaining proteins play a part in plant hormone-mediated stress responses.Authors identified 72 other proteins in Arabidopsis that contained all three unique signature domains.Transgenic lines also showed differential regulation of many abiotic stress-responsive distinct genes，indicating theinvolvement of C1-clan protein family in hormone-mediated stress remediation.

6.5.Putative auxin efflux carrier involved in the drought stress response and drought tolerance

Auxin acts as a necessary signal in reaction to abiotic stresses. Zhang et al.［127］identified a putative auxin efflux carrier gene（OsPIN3t）in rice that acts in polar auxin transport involved in the drought response in rice.They also found that knockdown of the OsPIN3t gene leads to crown root abnormalities in the seedling stage and that its overexpression increased drought tolerance.Under 20%polyethylene glycol stress，GUS activity significantly increased under NAA treatment.The study showed that OsPIN3t is involved in auxin transport and the drought stress response in plants.

6.6.Phytohormones alleviate high-temperature stress

Owing to high temperatures，crop productivity is decreasing in many parts of the world.Chhabra et al.［128］performed an experimenttotesttheeffectofvarioushormonalconcentrations on heat-stress effects and observed that both growth-promoting and growth-retarding hormones mitigated heat-stress effects. They also reported that the most effective concentration of kinetin was 100 μmol L-1followed by 50 μmol L-1and that soaking seeds in ABA delayed 50%seedling mortality by 1 h and 50 min at 0.5 and 1.0 μmol L-1concentrations.

7.Engineeringphytohormonesforproducing abiotic-stress tolerant crop plants

7.1.Engineering techniques Genetic engineering has opened new avenues for introducing abiotic stress tolerance in numerous economically important crop species.Recent success has made genetic engineering approaches as one of the most potent solutions for improving crop productivity under challenging environments.The success of transgenic research，however，depends largely on effective plant transformation methods for stable integration and functional expression of foreign genes in the plant genome.Since initial reports in tobacco［129，130］，rapid developments in transformation technology have resulted in the genetic modification of large number of plant species ［131］.

Two general approaches are available for transferring gene（s）to plants:one vector-mediated，by a biological vector such as Agrobacterium，and the other direct gene transfer approach，whereDNAisintroducedintocellsbyphysical，chemical，oreven electrical means.Direct or nonbiological gene transfer methods include particle bombardment，DNA uptake into protoplasts in the presence of polyvalent cations，protoplast fusion with bacterial spheroplasts and with liposomes containing foreign DNA（lipofection），electrotransfection，polymer-based transfection（polyfection），silicon carbide fiber-mediated DNA uptake，injection-based methods（micro-and macro-injection），wave and beam-mediated transformation，desiccation-based transformation，andexogenousDNAapplicationandimbibition［131，132］.The use of biolistics or particle bombardment is by far the most widely used direct gene transfer method.

Withitsever-increasinghostrange，Agrobacteriumtumefaciens has become the clear method of choice for gene transfer to all of the main crop plants.This soil bacterium possesses the natural ability to deliver a distinct part of its plasmid DNA（transfer or T-DNA）into the nuclear genome of its host plant.This condition has arisen also partly because although direct gene transfer methodsareusefulforstabletransformationaswellastransient expression，there are still some problems:alow frequency of stabletransformation，unwanted genetic rearrangements due to the high copy number of genes，and the long period required to regenerate whole transgenic plants.In Agrobacterium，bacterial genes can be successfully replaced with gene（s）of interest，and interestingly，this replacement does not affect the transformation process or frequency［133，134］.

For efficient transformation and subsequent regeneration，Agrobacterium-mediated methods are dependent on several factors.They are the choice of explant，the hormonal composition of the medium used，nutritional supplements，culture conditions before and during inoculation，duration of co-cultivation，virulence of the Agrobacterium strain，and concentration and composition of the bacteriostatic agent used. The length of selection and concentration of the antibiotic selection marker are also important.Other important factors are the plantcultivar and various conditions of tissue culture，including a robust system of plant regeneration［135］.However，throughextensiveefforts，remarkableprogresshasbeen achievedduringthelast2-3decadesinplantgeneticengineering. Optimized protocols have been developed for the Agrobacteriummediated genetic transformation of a broad range of crop plants including monocots，previously considered to lie outside the Agrobacterium host range.Recently，success has been achieved in developing inplanta transformation methods.However，inspired by the complex patent landscape of Agrobacterium technology and in search of a perfect（open source）platform for plant biotechnology，Broothaerts et al.［136］have identified three non-Agrobacterium species:Rhizobium sp.NGR234，Sinorhizobium meliloti，and Mesorhizobium loti as being capable of successful genetic transformation of different plant species.A recent addition to this list of biological vectors for genetic transformation of plants is virus-based vectors.

7.2.Metabolic engineering of phytohormones for conferring abiotic stress tolerance on crop plants Considering that phytohormones are key regulators of plant growth and development as well as mediators of the response to environmental stress［24］，hormone metabolism and signaling processes are excellent targets of manipulation to obtain enhanced abiotic stress tolerance.However，maintenance of hormonal balance to minimize possible adverse effects on growth and development is critical［15，137］.

Among various phytohormones，ABA is perhaps the most sought-after hormone for engineering abiotic stress tolerance in crop plants owing to its identity as a stress hormone and its vast array of functions under environmental stress conditions，particularly drought.As a result，many of the key ABA biosynthetic pathway enzymes have been investigated transgenically for improved abiotic stress tolerance［138］.Park et al.［139］reported enhanced osmotic stress tolerance by overexpressing an ABA-responsive stress-related gene in Arabidopsis.C-repeat binding factor（CBF）and/or dehydration-responsive elementbinding（DREB）genes have been manipulated to confer improved droughttolerance.Forexample，overexpressionofCBF1/ DREB1B from Arabidopsis improved tolerance to water-deficit stress in tomato［140］.Likewise，Al-Abed et al.［141］found expressionofCBF/DREBgenesunderstress-induciblepromoters in transgenic plants that do not express detectable levels of these genes under non-stress conditions，minimizing growthretardationandotheradverseeffects.Lietal.［142］overexpressed theMoCosulfurasegeneinsoybean，resultinginhigherbiomass production and yield with overall enhanced drought tolerance attributed to higher ABA accumulation，reduced water loss through smaller openings of stomata，and induced antioxidant enzymatic machinery.

Table 1-List of attempts made at engineering phytohormones for enhanced abiotic stress tolerance of plants.

However，on some occasions，overexpression of gene（s）involved in ABA biosynthesis or catabolic pathways resulted in increased drought tolerance，but led to impaired growth due to pleiotropic effects even with the use of inducible promoters［143］.To offset these unwanted growth anomalies，Zhang et al.［122］overexpressed CRK45，a stress-inducible kinase involved in ABA signaling，and the resulting transgenics showed enhanced drought tolerance but with tighter control of ABA levels and signaling，indicating the role of CRK45 in fine-tuning of ABA levels.Similarly，IPT was expressed under the control of stress-inducible promoters to avoid pleiotropic effects，leading to increased CK content，antioxidant scavenging，and better root growth with overall improved grain yield under drought conditions in Agrostis stolonifera［144，145］.

Recently，transgenic poplars were produced via overexpression of the Arabidopsis YUCCA6 gene（a member of the YUCCA family of flavinmonooxygenase-like proteins），which is involved in tryptophan-dependent IAA biosynthesis pathway and known to respond to environmental cues，under the control of the stress-inducible SWPA2 promoter［27］.The transgenic lines displayed auxin-overproduction morphological phenotypes，including rapid shoot growth and retarded main root development with increased root hair formation. Also，SY plants had higher levels of free IAA and early auxin response gene transcripts.The transgenic lines showed tolerance to drought stress，associated with reduced levels of reactive oxygen species［27］.The rice mutant CONSTITUTIVELY WILTED1 was deficient in the YUCCA homolog［146］，and an activation tagline of YUCCA7 in Arabidopsis showed enhanced drought tolerance［147］.Drought tolerance by overexpression of AtYUC6 in potato was also observed in 4-month-old potted plantsingreenhousesbymonitoringrecoveryafterwithholding water for 18 days［148］.

Sakamoto et al.［149］modified GA levels by overexpression of OsGA2ox1，a gene encoding GA2-oxidase.Interestingly，when the actin promoter constitutively expressed the gene，transgenic rice showed severe dwarfism but failed to set grain，given that GA is involved in both shoot elongation and reproductive development.In contrast，OsGA2ox1 ectopic expression at the site of bioactive GA synthesis in shoots under the control of the promoter of a GA biosynthesis gene，OsGA3ox2（D18），resulted in a semi-dwarf phenotype showing normal flowering and grain development. Attemptsatengineering phytohormones for enhanced abiotic stress tolerance of plants are listed in Table 1.

Given that biosynthetic pathways and convergence points for crosstalk are still not clear，there is further scope to increase our understanding in this regard and to identify novel genes encoding phytohormone metabolisms to be targeted for engineering abiotic stress tolerance in crop plants.Recent findings have opened various avenues for targeting phytohormones for genetic engineering to conferring abiotic stress tolerance on important crop species.

8.Conclusion and future outlook

Overall，phytohormone engineering represents an important platformforabioticstresstolerance，providingnewopportunities to maintain sustainable crop production to feed the world under changing environmental conditions.It has a major application in plant stress tolerance and adaptation to a variety of stresses，owing to the involvement of multiple stress responsive genes. During the past few years，with the rapid development of genomictechnology，muchresearchhasbeenperformedtowards understanding of plant abiotic stress response.Still many challenges are lying ahead to uncover and understand the complexity hidden in stress signal-transduction pathways.For example，to acquire wide-ranging understanding of plant responses to abiotic stress in coming years，more extensive work should be performed at the genetic level of the biosynthetic pathway of hormones such as IAA.Research to date indicates that phytohormone engineering has been initiated.The roles of plant hormones in responses to fluctuating environments have been demonstrated，and hormones play a primary role in determining plant stress responses.In this review，we have summarized the role of phytohormones，crosstalk among hormones，the importance of studying plant stresses in combination，and engineering techniques and strategiesfor developing stress tolerance in plants.In a wide range of stresses，plant hormones are involved directly or indirectly，and it is clear that plant hormones play roles in plant defense and plantenvironment interactions.

In conclusion，although phytohormone engineering is promising for plant biologists，there is still a long way to go before the technology can reach its full potential.Among the greatest challenges that remain to be addressed is the development of stable phytohormone-engineered crops that produce main staple foods such as rice，wheat，and corn. Towards this goal，study should be focused on a combination of stress responses such as those in field environments，because different stresses are most likely to occur simultaneously under field conditions.

R E F E R E N C E S

［1］S.H.Wani，S.K.Sah，Biotechnology and abiotic stress tolerance in rice，J.Rice Res.2（2014），e105 http://dx.doi.org/ 10.4172/jrr.1000e105.

［2］D.Tilman，C.Balzer，J.Hill，B.L.Belfort，Global food demand and the sustainable intensification of agriculture，Proc.Natl. Acad.Sci.U.S.A.108（2011）20260-20264.

［3］F.Qin，S.Kazuo，Y.S.Kazuo，Achievements and challenges in understanding plant abiotic stress responses and tolerance，Plant Cell Physiol.52（2011）1569-1582.

［4］S.H.Wani，N.B.Singh，A.Haribhushan，J.A.Mir，Compatible solute engineering in plants for abiotic stress tolerance-the role of glycine betaine，Curr.Genomics 14 （2013）157-165.

［5］U.Vob，A.Bishopp，E.Farcot，M.J.Bennett，Modelling hormonal response and development，Trends Plant Sci.19 （2014）311-319.

［6］K.Kazan，Diverse roles of jasmonates and ethylene in abiotic stress tolerance，Trends Plant Sci.20（2015）219-229.

［7］X.J.Li，M.F.Yang，H.Chen，L.Q.Qu，F(xiàn).Chen，S.H.Shen，Abscisic acid pretreatment enhances salt tolerance of rice seedlings:proteomic evidence，BBA-Proteins Proteomics 1804（2010）929-940.

［8］U.Feller，I.I.Vaseva，Extreme climate events:impacts of drought and high temperature on physiological processes in agronomically important plants，F(xiàn)ront.Environ.Sci.39 （2014）1-17.

［9］G.S.Sanghera，S.H.Wani，W.Hussain，N.B.Singh，Engineering cold stress tolerance in crop plants，Curr. Genomics 14（2011）30-43.

［10］M.R.Pathak，J.A.da Silva Teixeira，S.H.Wani，Polyamines in response to abiotic stress tolerance through transgenic approaches，GM Crops Food 5（2014）87-96.

［11］S.L.Postel，F(xiàn)or our thirsty world，efficiency or else，Science 313（2006）1046-1047.

［12］N.Suzuki，R.M.Rivero，V.Shulaev，E.Blumwald，R.Mittler，Abiotic and biotic stress combinations，New Phytol.203 （2014）32-43.

［13］H.Wolters，G.Jurgens，Survival of the flexible:hormonal growth control and adaptation in plant development，Nat. Rev.Genet.10（2009）305-317.

［14］S.Fahad，S.Hussain，A.Bano，S.Saud，S.Hassan，D.Shan，F(xiàn).A.Khan，F(xiàn).Khan，Y.T.Chen，C.Wu，M.A.Tabassum，M.X. Chun，M.Afzal，A.Jan，M.T.Jan，J.L.Huang，Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses:consequences for changing environment，Environ.Sci.Pollut.Res.22（2015）4907-4921.

［15］Z.Peleg，E.Blumwald，Hormone balance and abiotic stress toleranceincropplants，Curr.Opin.PlantBiol.14（2011）290-295.

［16］N.Sreenivasulu，V.Radchuk，A.Alawady，L.Borisjuk，D. Weier，N.Staroske，J.Fuchs，O.Miersch，M.Strickert，B. Usadel，U.Wobus，B.Grimm，H.Weber，W.Weschke，De-regulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8，Plant J. 64（2010）589-603.

［17］J.A.O'Brien，E.Benkova，Cytokinin cross-talking during biotic and abiotic stress responses，F(xiàn)ront.Plant Sci.4（2013）451，http://dx.doi.org/10.3389/fpls.2013.00451.

［18］J.L.Nemhauser，F(xiàn).Hong，J.Chory，Different plant hormones regulate similar processes through largely non overlapping transcriptional responses，Cell 126（2006）467-475.

［19］B.C.Keskin，A.T.Sarikaya，B.Yuksel，A.R.Memon，Abscisic acid regulated gene expression in bread wheat，Aust.J.Crop. Sci.4（2010）617-625.

［20］S.Wilkinson，G.R.Kudoyarova，D.S.Veselov，T.N.Arkhipova，W.J.Davies，Plant hormone interactions:innovative targets for crop breeding and management，J.Exp.Bot.63（2012）3499-3509.

［21］S.Giuliani，M.C.Sanguineti，R.Tuberosa，M.Bellotti，S.Salvi，P.Landi，Root-ABA1 a major constitutive QTL affects maize root architecture and leaf ABA concentration at different water regimes，J.Exp.Bot.56（2005）3061-3070.

［22］S.Zhang，J.Hu，Y.Zhang，X.J.Xie，A.Knapp，Seed priming with brassinolide improves lucerne（Medicago sativa L.）seed germination and seedling growth in relation to physiological changes under salinity stress，Aust.J.Agric.Res.58（2007）811-815.

［23］P.E.Verslues，M.Agarwal，S.Katiyar-Agarwal，J.Zhu，J.K. Zhu，Methods and concepts in quantifying resistance to drought，salt and freezing，abiotic stresses that affect plant water status，Plant J.45（2006）523-539.

［24］N.Sreenivasulu，V.T.Harshavardhan，G.Govind，C.Seiler，A. Kohli，Contrapuntal role of ABA:does it mediate stress tolerance or plant growth retardation under long-term drought stress？Gene 506（2012）265-273.

［25］M.Chaves，J.P.Manuela，J.S.Maroco，Pereira，Understanding plant responses to drought-from genes to the whole plant，F(xiàn)unct.Plant Biol.30（2003）239-264.

［26］J.Zhang，W.Jia，J.Yang，A.M.Ismail，Role of ABA in integrating plant responses to drought and salt stresses，F(xiàn)ield Crops Res.97（2006）111-119.

［27］Q.Ke，Z.Wang，C.Y.Ji，J.C.Jeong，H.S.Lee，H.Li，B.Xu，X. Deng，S.S.Kwak，Transgenic poplar expressing Arabidopsis YUCCA6 exhibits auxin-overproduction phenotypes and increased tolerance to abiotic stress，Plant Physiol.Biochem. 94（2015）19-27.

［28］Y.Mano，K.Nemoto，The pathway of auxin biosynthesis in plants，J.Exp.Bot.63（2012）2853-2872.

［29］K.Kazan，Auxin and the integration of environmental signals into plant root development，Ann.Bot.112（2013）1655-1665.

［30］I.De Smet，U.Voss，S.Lau，M.Wilson，N.Shao，R.E.Timme，R.Swarup，I.Kerr，C.Hodgman，R.Bock，M.Bennet，G. Jurgens，T.Beeckman，Unraveling the evolution of auxin signaling，Plant Physiol.155（2010）209-221.

［31］N.Iqbal，S.Umar，N.A.Khan，M.I.R.Khan，A new perspective of phytohormones in salinity tolerance:regulation of proline metabolism，Environ.Exp.Bot.100（2014）34-42.

［32］X.F.Sheng，J.J.Xia，Improvement of rape（Brassica napus）plant growth and cadmium uptake by cadmium-resistant bacteria，Chemosphere 64（2006）1036-1042.

［33］D.Egamberdieva，Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat，Acta Physiol.Plant.31（2009）861-864.

［34］S.Fahad，A.Bano，Effect of salicylic acid on physiological and biochemical characterization of maize grown in saline area，Pak.J.Bot.44（2012）1433-1438.

［35］M.G.Javid，A.Sorooshzadeh，F(xiàn).Moradi，S.A.M.M.Sanavy，I. Allahdadi，The role of phytohormones in alleviating salt stress in crop plants，Aust.J.Crop.Sci.5（2011）726-734.

［36］S.Fahad，S.Hussain，A.Matloob，F(xiàn).A.Khan，A.Khaliq，S. Saud，S.Hassan，D.Shan，F(xiàn).Khan，N.Ullah，M.Faiq，M.R. Khan，A.K.Tareen，A.Khan，A.Ullah，N.Ullah，J.L.Huang，Phytohormones and plant responses to salinity stress:a review，Plant Growth Regul.75（2015）391-404.

［37］N.Y.Kang，C.Cho，N.Y.Kim，J.Kim，Cytokininreceptor-dependent and receptor-independent path ways in the dehydration response of Arabidopsis thaliana，J.Plant Physiol.169（2012）1382-1391.

［38］R.Nishiyama，Y.Watanabe，Y.Fujita，L.D.Tien，M.Kojima，T.Werner，R.Vankova，K.Yamaguchi-Shinozaki，K. Shinozaki，T.Kakimoto，H.Sakakibara，T.Schmuelling，P.T. Lam-Son，Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought，salt and abscisic acid responses，and abscisic acid biosynthesis，Plant Cell 23 （2011）2169-2183.

［39］D.Zalabák，H.Pospí?ilová，M.?mehilová，K.Mrízová，I. Frébort，P.Galuszka，Genetic engineering of cytokinin metabolism:prospective way to improve agricultural traits of crop plants，Biotechnol.Adv.31（2013）97-117.

［40］J.Pospí?ilová，Interaction of cytokinins and abscisic acid during regulation of stomatal opening in bean leaves，Photosynthetica 41（2003）49-56.

［41］J.Pospí?ilová，Participation of phytohormones in the stomatal regulation of gas exchange during water stress，Biol.Plant.46（2003）491-506.

［42］E.Gamalero，B.R.Glick，Ethylene and abiotic stress tolerance in plants，in:P.Ahmed，M.N.V.Prasad（Eds.），Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change，Springer，New York 2012，pp.395-412.

［43］S.C.Groen，N.K.Whiteman，The evolution of ethylene signaling in plant chemical ecology，J.Chem.Ecol.40（2014）700-716.

［44］Y.Shi，S.Tian，L.Hou，X.Huang，X.Zhang，H.Guo，S.Yang，Ethylene signaling negatively regulates freezing toleranceby repressing expression of CBF and Type-A ARR genes in Arabidopsis，Plant Cell 24（2012）2578-2595.

［45］J.Larkindale，D.J.Hall，M.R.Knight，E.Vierling，Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermo-tolerance，Plant Physiol.138（2005）882-897.

［46］I.Klay，J.Pirrello，l.Riahi，A.Bernadac，A.Cherif，M. Bouzayen，S.Bouzid，Ethylene response factor Sl-ERF.B.3 is responsive to abiotic stresses and mediates salt and cold stress response regulation in tomato，Sci.World J.2014 （2014）167681，http://dx.doi.org/10.1155/2014/167681.

［47］M.A.Matilla-Vazquez，A.J.Matilla，Ethylene:Role in plants under environmental stress，in:P.Ahmad，M.R.Wani（Eds.），Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment，vol.2，Springer Science+Business Media，New York 2014，pp.189-222.

［48］C.C.Yin，B.Ma，D.P.Collinge，B.J.Pogson，S.J.He，Q.Xiong，J.S. Zhang，Ethylene responses in rice roots and coleoptiles are differentially regulated by a carotenoid isomerase-mediated abscisic acid pathway，Plant Cell 27（2015）1061-1081.

［49］V.M.Sponsel，P.Hedden，Gibberellin，biosynthesis and inactivation，in:P.J.Davies（Ed.），Plant Hormones Biosynthesis，Signal Transduction，Action！Springer，Dordrecht 2004，pp.63-94.

［50］S.Yamaguchi，Gibberellin metabolism and its regulation，Annu.Rev.Plant Physiol.59（2008）225-251.

［51］E.H.Colebrook，S.G.Thomas，A.L.Phillips，P.Hedden，The role of gibberellin signaling in plant responses to abiotic stress，J.Exp.Biol.217（2014）67-75.

［52］A.Skirycz，H.Claeys，S.De Bodt，A.Oikawa，S.Shinoda，M. Andriankaja，K.Maleux，N.B.Eloy，F(xiàn).Coppens，S.D.Yoo，K. Saito，D.Inze，Pause-and-stop:the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest，Plant Cell 23（2011）1876-1888.

［53］H.Claeys，A.Skirycz，K.Maleux，D.Inze，DELLA signaling mediates stress-induced cell differentiation in Arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity，Plant Physiol.159（2012）739-747.

［54］V.Munteanu，V.Gordeev，R.Martea，M.Duca，Effect of gibberellin cross talk with other phytohormones on cellular growth and mitosis to endoreduplication transition，Int.J. Adv.Res.Biol.Sci.1（6）（2014）136-153.

［55］B.V.Vardhini，S.Anuradha，S.S.R.Rao，Brassinosteroids:a great potential to improve crop productivity，Indian J.Plant Physiol.11（2006）1-12.

［56］A.Bajguz，S.Hayat，Effects of brassinosteroids on the plant responses to environmental stresses，Plant Physiol. Biochem.47（2009）1-8.

［57］A.Janeczko，J.Oklestkova，E.Pociecha，J.Koscielniak，M. Mirek，Physiological effects and transport of 24-epibrassinolide in heat-stressed barley，Acta Physiol.Plant. 33（2011）1249-1259.

［58］X.H.Wang，C.Shu，H.Y.Li，X.Q.Hu，Y.X.Wang，Effectsof0.01% brassinolide solution application on yield of rice and its resistance to autumn low-temperature damage，Acta Agric. Jiangxi 26（2014）36-38（in Chinese with English abstract）.

［59］S.Abbas，H.H.Latif，E.A.Elsherbiny，Effect of 24-epibrassinolide on the physiological and genetic changes on two varieties of pepper under salt stress conditions，Pak.J. Bot.45（2013）1273-1284.

［60］L.V.Kurepin，S.H.Joo，S.K.Kim，R.P.Pharis，T.G.Back，Interaction of brassinosteroids with light quality and plant hormones in regulating shoot growth of young sunflower and Arabidopsis seedlings，J.Plant Growth Regul.31（2012）156-164.

［61］B.Mahesh，B.Parshavaneni，B.Ramakrishna，S.S.R.Rao，Effect of brassinosteroids on germination and seedling growth of radish（Raphanus sativus L.）under PEG-6000 induced water stress，Am.J.Plant Sci.4（2013）2305-2313.

［62］J.Q.Liang，Y.Liang，Effects of plant growth substances on water-logging resistance of oilseed rape seedling，J. Southwest China Norm.Univ.（Nat.Sci.Ed.）34（2009）58-62 （in Chinese with English abstract）.

［63］A.Bajguz，An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress，Environ.Exp.Bot.68 （2010）175-179.

［64］G.J.Ahammed，S.P.Choudhary，S.Chen，X.Xia，K.Shi，Y. Zhou，J.Yu，Role of brassinosteroids in alleviation of phenanthrene-cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato，J. Exp.Bot.64（2013）199-213.

［65］B.V.Vardhini，N.A.Anjum，Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system，F(xiàn)ront.Environ. Sci.2（2015）1-16.

［66］H.S.Seo，J.T.Song，J.J.Cheong，Y.H.Lee，Y.H.Lee，I.Hwang，J.S.Lee，D.C.Yang，Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate regulated plant responses，Proc. Natl.Acad.Sci.U.S.A.98（2001）4788-4793.

［67］S.Fahad，L.Nie，Y.Chen，C.Wu，D.Xiong，S.Saud，L. Hongyan，K.Cui，J.Huang，Crop plant hormones and environmental stress，Sustain.Agric.Rev.15（2015）371-400.

［68］L.Pauwels，D.Inze，A.Goossens，Jasmonate-inducible gene: whatdoesitmean？Trends Plant Sci.14（2009）87-91，http:// dx.doi.org/10.1016/j.tplants.2008.11.005.

［69］J.S.Seo，J.Joo，M.J.Kim，Y.K.Kim，B.H.Nahm，S.I.Song，J.J. Cheong，J.S.Lee，J.K.Kim，Y.D.Choi，OsbHLH148，a basic helix-loop-helix protein，interacts with OsJAZ proteins in a jas monate signaling pathway leading to drought tolerance in rice，Plant J.65（2011）907-921.

［70］H.Du，H.B.Liu，L.Z.Xiong，Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice，F(xiàn)ront.Plant Sci.4（2013）397，http://dx.doi.org/10.3389/ fpls.2013.00397.

［71］P.V.Demkura，G.Abdala，I.T.Baldwin，C.L.Ballare，Jasmonate-dependent and-independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense，Plant Physiol.152 （2010）1084-1095.

［72］T.A.Dar，M.Uddin，M.M.A.Khan，K.R.Hakeem，H.Jaleel，Jasmonates counter plant stress:a review，Environ.Exp.Bot. 115（2015）49-57.

［73］J.Y.Yoon，M.Hamayun，S.K.Lee，I.J.Lee，Methyl jasmonate alleviated salinity stress in soybean，J.Crop.Sci.Biotechnol. 12（2009）63-68.

［74］Y.Wang，S.Mopper，K.H.Hasentein，Effects of salinity on endogenous ABA，IAA，JA，and SA in Iris hexagona，J.Chem. Ecol.27（2001）327-342.

［75］Z.Yan，J.Chen，X.Li，Methyl jasmonate as modulator of Cd toxicity in Capsicum frutescens var.fasciculatum seedlings，Ecotoxicol.Environ.Saf.98（2013）203-209.

［76］W.Maksymiec，M.Wojcik，Z.Krupa，Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate，Chemosphere 66（2007）421-427.

［77］K.Miura，Y.Tada，Regulation of water，salinity，and cold stress responses by salicylic acid，F(xiàn)ront.Plant Sci.5（2014）4，http://dx.doi.org/10.3389/fpls.2014.00004.

［78］V.M.Rivas-San，J.Plasencia，Salicylic acid beyond defense: its role in plant growth and development，J.Exp.Bot.62 （2011）3321-3338.

［79］M.Hara，J.Furukawa，A.Sato，T.Mizoguchi，K.Miura，Abiotic stress and role of salicylic acid in plants，in:A.Parvaiz，M.N.V.Prasad（Eds.），Abiotic Stress Responses in Plants，Springer，New York 2012，pp.235-251.

［80］S.R.Uppalapati，Y.Ishiga，T.Wangdi，B.N.Kunkel，A.Anand，K.S.Mysore，C.L.Bender，The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv tomato DC3000，Mol.Plant-Microbe Interact.20（2007）955-965.

［81］J.Catinot，A.Buchala，E.Abou-Mansour，J.P.Métraux，Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana，F(xiàn)EBS Lett.582（2008）473-478.

［82］S.S.Jumali，I.M.Said，I.Ismail，Z.Zainal，Genes induced by high concentration of salicylic acid in Mitragyna speciosa，Aust.J.Crop.Sci.5（2011）296-303.

［83］K.Miura，H.Okamoto，E.Okuma，H.Shiba，H.Kamada，P.M. Hasegawa，Y.Murata，SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis，Plant J.49（2013）79-90.

［84］S.E.A.Khodary，Effect of salicylic acid on growth，photosynthesis and carbohydrate metabolism in salt stressed maize plants，Int.J.Agric.Biol.6（2004）5-8.

［85］Z.Yang，S.Cao，Y.Zheng，Y.Jiang，Combined salicyclic acid and ultrasound treatments for reducing the chilling injury on peach fruit，J.Agric.Food Chem.60（2012）1209-1212.

［86］K.A.Fayez，S.A.Bazaid，Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate，J.Saudi Soc.Agric.Sci.13（2014）45-55.

［87］S.Munne-Bosch，J.Penuelas，Photo and antioxidative protection and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants，Planta 217（2003）758-766.

［88］H.Bandurska，A.Stroinski，The effect of salicylic acid on barley response to water deficit，Acta Physiol.Plant.27 （2005）379-386.

［89］X.Xie，K.Yoneyama，K.Yoneyama，The strigolactone story，Annu.Rev.Phytopathol.48（2010）93-117.

［90］C.Ruyter-Spira，S.Al-Babili，S.van der Krol，H. Bouwmeester，The biology of strigolactones，Trends Plant Sci.18（2013）72-83.

［91］K.Yoneyama，T.Kisugi，X.Xie，K.Yoneyama，Chemistry of strigolactones:why and how do plants produce so many strigolactones？in:F.J.de Bruijn（Ed.）Molecular Microbial Ecology of the Rhizosphere，vol.1&2，John Wiley&Sons Ltd.，Hoboken，NJ 2013，pp.373-379.

［92］H.Koltai，C.A.Beveridge，Strigolactones and the coordinated development of shoot and root，in:F.Baluska（Ed.），Long-Distance Systemic Signaling and Communication in Plants，Springer，Berlin 2013，pp.189-204.

［93］C.Ruyter-Spira，W.Kohlen，T.Charnikhova，A.van Zeijl，L. van Bezouwen，N.de Ruijter，C.Cardoso，J.A.Lopez-Raez，R. Matusova，R.Bours，F(xiàn).Verstappen，H.Bouwmeester，Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis:another belowground role for strigolactones？Plant Physiol.155 （2011）721-734.

［94］V.Gomez-Roldan，S.Fermas，P.B.Brewer，V.Puech-Pages，E.A.Dun，J.P.Pillot，F(xiàn).Letisse，R.Matusova，S.Danoun，J.C. Portais，H.Bouwmeester，G.Becard，C.A.Beveridge，C. Rameau，S.F.Rochange，Strigolactone inhibition of shoot branching，Nature 455（2008）189-194.

［95］M.Umehara，A.Hanada，S.Yoshida，K.Akiyama，T.Arite，N. Takeda-Kamiya，H.Magome，Y.Kamiya，K.Shirasu，K. Yoneyama，J.Kyozuka，S.Yamaguchi，Inhibition of shoot branching by new terpenoid plant hormones，Nature 455 （2008）195-200.

［96］Y.Kapulnik，P.M.Delaux，N.Resnick，E.Mayzlish-Gati，S. Wininger，C.Bhattacharya，N.Séjalon-Delmas，J.P.Combier， G.Bécard，E.Belausov，T.Beeckman，E.Dor，J.Hershenhorn，H.Koltai，Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis，Planta 233（2011）209-216.

［97］Y.Kapulnik，H.Koltai，Strigolactone involvement in root development，response to abiotic stress，and interactions with the biotic soil environment，Plant Physiol.166（2014）560-569.

［98］M.J.Soto，M.N.Fernandez-Aparicio，V.Castellanos-Morales，J.M.Garcia-Garrido，J.A.Ocampo，M.J.Delgado，H.Vierheilig，F(xiàn)irst indications for the involvement of strigolactones on nodule formation in alfalfa（Medicago sativa），Soil Biol. Biochem.42（2010）383-385.

［99］E.Foo，N.W.Davies，Strigolactones promote nodulation in pea，Planta 234（2011）1073-1081.

［100］M.Vurro，K.Yoneyama，Strigolactones-intriguing biologically active compounds:perspectives for deciphering their biological role and for proposing practical application，Pest Manag.Sci.68（2012）664-668.

［101］M.A.Harrison，Cross-talk between phytohormone signaling pathways under both optimal and stressful environmental conditions，in:N.A.Khan，R.Nazar，N.Iqbal，N.A.Anjum （Eds.），Phytohormones and Abiotic Stress Tolerance in Plants，Springer-Verlag，Berlin Heidelberg 2012，pp.49-76.

［102］A.Kohli，N.Sreenivasulu，P.Lakshmanan，P.P.Kumar，The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses，Plant Cell Rep.32（2013）945-957.

［103］R.Singh，N.S.Jwa，Understanding the responses of rice to environmental stress using proteomics，J.Proteome Res.12 （2013）4652-4669.

［104］C.Pinheiro，M.M.Chaves，Photosynthesis and drought:can we make metabolic connections from available data？J.Exp. Bot.62（2011）869-882.

［105］M.R.Grant，J.D.Jones，Hormone（dis）harmony moulds plant health and disease，Science 324（2009）750-752.

［106］R.Desikan，K.Last，R.Harrett-Williams，C.Tagliavia，K.Harter，R.Hooley，J.T.Hancock，S.J.Neill，Ethylene-induced stomatal closure in Arabidopsis occurs via Atrboh F-mediated hydrogen peroxide synthesis，Plant J.47（2006）907-916.

［107］C.Wasternack，Jasmonates:an update on biosynthesis，signal transduction and action in plant stress response，growth and development，Ann.Bot.100（2007）681-697.

［108］D.Huang，W.Wu，S.R.Abrams，J.Adrian，A.J.Cutler，The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors，J.Exp.Bot.59（2008）2991-3007.

［109］S.Munemasa，K.Oda，M.Watanabe-Sugimoto，Y.Nakamura，Y.Shimoishi，Y.Murata，The coronatine-insensitive 1 mutationreveals the hormonalsignaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells.Specific impairment of ion channel activation and second messenger production，Plant Physiol.143（2007）1398-1407.

［110］E.H.Kim，Y.S.Kim，S.H.Park，Y.J.Koo，Y.D.Choi，Y.Y.Chung，I.J.Lee，J.K.Kim，Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice，Plant Physiol.149（2009）1751-1760.

［111］S.Y.Zhu，X.C.Yu，X.J.Wang，R.Zhao，Y.Li，R.C.Fan，Y. Shang，S.Y.Du，X.F.Wang，F(xiàn).Q.Wu，Y.H.Xu，X.Y.Zhang，D.P. Zhang，Two calcium-dependent protein kinases，CPK4 and CPK11，regulate abscisic acid signal transduction in Arabidopsis，Plant Cell 19（2007）3019-3036.

［112］H.Walia，C.Wilson，A.Wahid，P.Condamine，X.Cui，T.J.Close，Expression analysis of barley（Hordeum vulgare L.）during salinity stress，F(xiàn)unct.Integr.Genomics 6（2006）143-156.

［113］P.Stamm，P.P.Kumar，Auxin and gibberellin responsive Arabidopsis SMALL AUXIN UP RNA36 regulates hypocotyl elongation in the light，Plant Cell Rep.32（2013）759-769.

［114］S.Depuydt，C.S.Hardtke，Hormone signalling crosstalk in plant growth regulation，Curr.Biol.21（2011）R365-R373.

［115］A.Linkies，G.Leubner-Metzger，Beyond gibberellins and abscisic acid:how ethylene and jasmonates control seed germination，Plant Cell Rep.31（2012）253-270.

［116］N.Iqbal，R.Nazar，M.R.K.Iqbal，A.Masood，A.K.Nafees，Role of gibberellins in regulation of source sink relations under optimal and limiting environmental conditions，Curr.Sci. 100（2011）998-1007.

［117］G.Krouk，S.Ruffel，R.A.Gutierrez，A.Gojon，N.M.Crawford，G.M.Coruzzi，B.Lacombe，A framework integrating plant growth with hormones and nutrients，Trends Plant Sci.16 （2011）178-182.

［118］D.A.Capiati，S.M.Pa?s，M.T.Tellez-Inon，Wounding increases salt tolerance in tomato plants:evidence on the participation of calmodulin-like activities in cross-tolerance signaling，J.Exp.Bot.57（2006）2391-2400.

［119］K.E.Zinn，M.Tunc-Ozdemir，J.F.Harper，Temperature stress and plant sexual reproduction:uncovering the weakest links，J.Exp.Bot.61（2010）1959-1968.

［120］P.Thakur，S.Kumar，J.A.Malik，J.D.Berger，H.Nayyar，Cold stress effects on reproductive development in grain crops: an overview，Environ.Exp.Bot.67（2010）429-443.

［121］S.Kumar，J.Malik，P.Thakur，S.Kaistha，K.D.Sharma，H.D. Upadhyaya，J.D.Berger，H.Nayyar，Growth and metabolic responses of contrasting chickpea（Cicer arietinum L.）genotypes to chilling stress at reproductive phase，Acta Physiol.Plant.33（2011）779-787.

［122］X.J.Zhang，G.Y.Yang，R.Shi，X.M.Han，L.W.Qi，R.G.Wang，L.M.Xiong，G.J.Li，Arabidopsis cysteine-rich receptor-like kinase 45 functions in the responses to abscisic acid and abiotic stresses，Plant Physiol.Biochem.67（2013）189-198.

［123］K.D.Sharma，Pollen development under cold stress:a molecular perspective，Austin J.Genet.Genomic Res.1 （2014）4.

［124］M.Kolaksazov，F(xiàn).Laporte，K.Ananieva，P.Dobrev，M.Herzog，E.D.Ananiev，Effect of chilling and freezing stresses on jasmonate content in Arabis Alpina，Bulg.J.Agric.Sci.19 （2013）15-17.

［125］F.A.Gharib，A.Z.Hegazi，Salicylic acid ameliorates germination，seedling growth，phytohormone and enzymes activity in bean（Phaseolus vulgaris L.）under cold stress，J. Am.Sci.6（2010）675-683.

［126］R.V.Bhaskar，B.Mohanty，V.Verma，E.Wijaya，P.P.Kumar，A hormone-responsive c1-domain-containing protein at5g17960 mediates stress response in Arabidopsis thaliana，PLoS ONE 10（2015），e0115418.

［127］Q.Zhang，J.J.Li，W.J.Zhang，S.N.Yan，R.Wang，J.F.Zhao，Y.J. Li，Z.G.Qi，Z.X.Sun，Z.G.Zhu，The putative auxin efflux carrier OsPIN3t is involved in the drought stress response and drought tolerance，Plant J.72（2012）805-816.

［128］M.L.Chhabra，A.Dhawan，N.Sangwan，K.Dhawan，D.Singh，Phytohormones induced amelioration of high temperature stress in Brassica juncea（L.）Czern&Coss，Proceedings of 16th Australian Research Assembly on Brassicas，Ballarat，Australia，10-14 September，2009.

［129］M.De Block，L.Herrera-Estrella，M.Van Montagu，J.Schell，P. Zambryski，Expression of foreign genes in regenerated plants and their progeny，EMBO J.3（1984）1681-1689.

［130］J.Paszkowski，R.D.Shillito，M.Saul，V.Mandak，T.Hohn，I. Potrykus，Direct gene transfer to plants，EMBO J.3（1984）2717-2722.

［131］Y.Narusaka，M.Narusaka，S.Yamasaki，M.Iwabuchi，Methods to transfer foreign genes to plants，in:Y.O.Ciftci （Ed.），Transgenic Plants-Advances and Limitations，InTech，2012（Rijeka，Croatia&Shanghai，China）.

［132］B.Darbani，A.Eimanifar，C.N.Stewart，W.N.Camargo，DNA delivery methods to produce transgenic plants，Turk.J.Biol. 7（2008）385-402.

［133］S.B.Gelvin，Agrobacterium-mediated plant transformation: the biology behind the“gene-jockeying”tool，Microbiol.Mol. Biol.Rev.67（2003）16-37.

［134］A.Lorence，R.Verpoorte，Gene transfer and expression in plants，Methods Mol.Biol.267（2004）329-350.

［135］N.Yookongkaew，M.Srivatanakul，J.Narangajavana，Development of genotype-independent regeneration system for transformation of rice（Oryza sativa ssp.indica），J. Plant Res.120（2007）237-245.

［136］W.Broothaerts，H.J.Mitchell，B.Weir，S.Kaines，L.M.A. Smith，W.Yang，J.E.Mayer，C.Roa-rodriguez，R.A.Efferson，Gene transfer to plants by diverse species of bacteria，Nature 433（2005）629-633.

［137］J.V.Cabello，A.F.Lodeyro，M.D.Zurbriggen，Novel perspectives for the engineering of abiotic stress tolerance in plants，Curr.Opin.Biotechnol.26（2014）62-70.

［138］M.C.Jewell，B.C.Campbell，Godwin ID，Transgenic plants for abiotic stress resistance，in:C.Kole，C.Michler，A.G. Abbott，T.C.Hall（Eds.），Transgenic Crop Plants，Vol.2: Utilization and Biosafety，Springer-Verlag，Berlin 2010，pp.67-131.

［139］H.Y.Park，H.Y.Seok，B.K.Park，S.H.Kim，C.H.Goh，B.H.Lee，C.H.Lee，Y.H.Moon，Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress，Biochem.Biophys. Res.Commun.375（2008）80-85.

［140］J.T.Lee，V.Prasad，P.T.Yang，J.F.Wu，T.H.D.Ho，Y.Y.Charng，M.T.Chan，Expression of Arabidopsis CBF1 regulated by an ABA/stress inducible promoter in transgenic tomato confers stress tolerance without affecting yield，Plant Cell Environ. 26（2003）1181-1190.

［141］D.Al-Abed，P.Madasamy，R.Talla，S.Goldman，S. Rudrabhatla，Genetic engineering of maize with the Arabidopsis DREB1A/CBF3 gene using split-seed explants，Crop Sci.47（2007）2390-2402.

［142］Y.Lu，Y.Li，J.Zhang，Y.Xiao，Y.Yue，L.Duan，Z.Li，Overexpression of Arabidopsis molybdenum cofactor sulfurase gene confers drought tolerance in maize （Zea mays L.），PLoS One 8（2013），e52126 http://dx.doi.org/10. 1371/journal.pone.0052126.

［143］S.G.Hwang，H.C.Chen，W.Y.Huang，Y.C.Chu，C.T.Shi，W.H. Cheng，Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology，Plant Sci. 178（2010）12-22.

［144］Y.Xu，P.Burgess，X.Zhang，B.Huang，Enhancing cytokinin synthesis by overexpressing ipt alleviated drought inhibition of root growth through activating ROS-scavenging systems in Agrostis stolonifera，J.Exp.Bot.（2016），erw019 http://dx.doi.org/10.1093/jxb/erw019.

［145］E.B.Merewitz，H.Du，W.Yu，Y.Liu，T.Gianfagna，B. Huang，Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation，J.Exp.Bot.63（2012）1315-1328.

［146］Y.Woo，H.Park，M.Suudi，J.Yang，J.Park，K.Back，Y.Park，G. An，Constitutively wilted 1，a member of the rice YUCCA gene family，is required for maintaining water homeostasis and an appropriate root to shoot ratio，Plant Mol.Biol.65（2007）125-136.

［147］M.Lee，J.Jung，D.Han，P.Seo，W.Park，C.Park，Activation of a flavinmonooxygenase gene YUCCA7 enhances drought resistance in Arabidopsis，Planta 235（2011）923-938.

［148］J.I.Kim，D.Baek，H.C.Park，H.J.Chun，D.H.Oh，M.K.Lee，J.Y. Cha，W.Y.Kim，M.C.Kim，W.S.Chung，H.J.Bohnert，S.Y.Lee，R.A.Bressan，S.W.Lee，D.J.Yun，Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit，Mol.Plant 6（2013）337-349.

［149］T.Sakamoto，M.Yoichi，I.Kanako，K.Masatomo，I.Hironori，K.Toshiaki，I.Shuichi，M.Makoto，T.Hiroshi，Geneticmanipulation of gibberellin metabolism in transgenic rice，Nat.Biotechnol.21（2003）909-913.

［150］Y.J.Li，J.C.Zhang，J.Zhang，L.Hao，J.P.Hua，L.S.Duan，M.C. Zhang，Z.H.Li，Expression of an Arabidopsis molybdenum factor sulphurase gene in soybean enhances drought tolerance and increases yield under field conditions，Plant Biotechnol.J.11（2013）747-758.

［151］J.Zhang，H.Y.Yu，Y.S.Zhang，Y.B.Wang，M.Y.Li，J.C.Zhang，L.S.Duan，M.C.Zhang，Z.H.Li，Increased abscisic acid levels in transgenic maize overexpressing AtLOS5 mediated root ion fluxes and leaf water status under salt stress，J.Exp.Bot. （2016），erv528 http://dx.doi.org/10.1093/jxb/erv528.

［152］A.C.Estrada-Melo，C.Ma，M.S.Reid，C.Z.Jiang，Overexpression of an ABA biosynthesis gene using a stress-inducible promoter enhances drought resistance in petunia，Hortic.Res.2（2015）15013，http://dx.doi.org/10. 1038/hortres.2015.13.

［153］Z.Q.Zhang，Y.F.Wang，L.Q.Chang，T.Zhang，J.An，Y.S.Liu，Y.M.Cao，X.Zhao，X.Y.Sha，T.M.Hu，P.Z.Yang，MsZEP，a novel zeaxanthin epoxidase gene from alfalfa（Medicago sativa），confers drought and salt tolerance in transgenic tobacco，Plant Cell Rep.14（2015）1-5.

［154］X.G.Mao，H.Y.Zhang，S.J.Tian，X.P.Chang，R.L.Jing，TaSnRK2.4，an SNF1-type serine/threonine protein kinase of wheat（Triticum aestivum L.），confers enhanced multistress tolerance in Arabidopsis，J.Exp.Bot.61（2010）683-696.

［155］I.J.Kim，D.Baek，H.C.Park，H.J.Chun，D.H.Oh，M.K.Lee，J.Y. Cha，W.Y.Kim，M.C.Kim，W.S.Chung，H.J.Bohnert，Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit，Mol.Plant 6（2013）337-349.

［156］H.Jung，D.K.Lee，D.Y.Choi，J.K.Kim，OsIAA6，a member of the rice Aux/IAA gene family，is involved in drought tolerance and tiller outgrowth，Plant Sci.236（2015）304-312.

［157］M.E.Ghanem，A.Albacete，A.C.Smigocki，I.Frébort，H. Pospí?ilová，C.Martínez-Andújar，M.Acosta，J. Sánchez-Bravo，S.Lutts，I.C.Dodd，F(xiàn).Pérez-Alfocea，Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato（Solanum lycopersicum L.）plants，J.Exp.Bot.62（2011）125-140.

［158］W.M.Qiu，M.Y.Liu，G.R.Qiao，J.Jiang，L.H.Xie，R.Y.Zhuo，An isopentenyltransferase gene driven by the stress-inducible rd29A promoter improves salinity stress tolerance in transgenic tobacco，Plant Mol.Biol.Report.30（2012）519-528.

［159］E.?i?ková，P.I.Dobrev，Y.Muhovski，P.Ho?ek，K.Hoyerová，D.Haisel，I.Hichri，Tomato（Solanum lycopersicum L.）SlIPT3 and SlIPT4 isopentenyltransferases mediate salt stress response in tomato，BMC Plant Biol.15（2015）85，http://dx. doi.org/10.1186/s12870-015-0415-7.

［160］T.Werner，E.Nehnevajova，I.K?llmer，O.Novák，M.Strnad，U.Kr?mer，T.Schmulling，Root-specific reduction of cytokinin causes enhanced root growth，drought tolerance，and leaf mineral enrichment in Arabidopsis and tobacco，Plant Cell 22（2010）3905-3920.

［161］H.Pospí?ilová，E.Jiskrová，P.Vojta，K.Mrízová，F(xiàn).Koká?，M.M.?udejková，V.Bergougnoux，O.Plíhal，J.Klime?ová，O. Novák，L.Dzurová，Transgenic barley overexpressing a cytokinin dehydrogenase gene shows greater tolerance to drought stress，New Biotechnol.（2016）http://dx.doi.org/10. 1016/j.nbt.2015.12.005.

［162］Z.J.Zhang，F(xiàn).Li，D.J.Li，H.W.Zhang，R.F.Huang，Expression of ethylene response factor JERF1 in rice improves tolerance to drought，Planta 232（2010）765-774.

［163］H.Du，N.Wu，F(xiàn).Cui，L.You，X.H.Li，L.Z.Xiong，A homolog of ETHYLENE OVER-PRODUCER，OsETOL1，differentially modulates drought and submergence tolerance in rice，Plant J.78（2014）834-849.

［164］J.E.Habben，X.M.Bao，N.J.Bate，J.L.DeBruin，D.Dolan，D. Hasegawa，T.G.Helentjaris，R.H.Lafitte，N.Lovan，H.Mo，K. Reimann，J.R.Schussler，Transgenic alteration of ethylene biosynthesis increases grain yield in maize under field drought-stress conditions，Plant Biotechnol.J.12（2014）685-693.

［165］J.Shi，J.E.Habben，R.L.Archibald，B.J.Drummond，M.A. Chamberlin，R.W.Williams，H.R.Lafitte，B.P. WeersOverexpression of ARGOS genes modifies plant sensitivity to ethylene，leading to improved drought tolerance in both Arabidopsis and maize Plant Physiol.169 （2015）266-282.

［166］S.Koh，S.C.Lee，M.K.Kim，J.H.Koh，S.Lee，G.An，S.Choe，S.R. Kim，T-DNA tagged knockout mutation of rice OsGSK1，an orthologue of Arabidopsis BIN2，with enhanced tolerance to various abiotic stresses，Plant Mol.Biol.65（2007）1158-1164.

［167］F.L.Li，T.Asami，X.Z.Wu，E.W.T.Tsang，A.J.Cutler，A putative hydroxysteroid dehydrogenase involved in regulating plant growth and development，Plant Physiol.145 （2007）87-97.

［168］Y.Feng，Y.H.Yin，S.Z.Fei，Downregulation of BdBRI1，a putative brassinosteroid receptor gene produces a dwarf phenotype with enhanced drought tolerance in Brachypodium distachyon，Plant Sci.234（2015）163-173.

22 August 2015

*Corresponding authors.

E-mail addresses:shabirhussainwani@gmail.com（S.H.Wani），vinaymalik123@gmail.com（V.Kumar）.

Peer review under responsibility of Crop Science Society of China and Institute of Crop Science，CAAS.

http://dx.doi.org/10.1016/j.cj.2016.01.010

2214-5141/?2016 Crop Science Society of China and Institute of Crop Science，CAAS.Production and hosting by Elsevier B.V.This is an open access article under the CC BY-NC-ND license（http://creativecommons.org/licenses/by-nc-nd/4.0/）.