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26 Transcription Factors: Improving Abiotic Stress Tolerance in Plants Tetsuya Ishida, Yuriko Osakabe, and Shuichi Yanagisawa Plant growth and productivity are greatly affected by environmental abiotic stresses, including drought, high salinity, high or low temperature, nutrient starvation, and excess metals in soils. After perceiving these stress signals, plants modulate the expression levels of various genes to adapt to and overcome environmental changes. Transcription factors thus play central roles in the regulatory networks that mediate the adaptation of plants to various environmental stresses. Although our knowledge of the transcription factors associated with abiotic stress response in crops is still limited, a number of such transcription factors have been recently identied, mainly in the model plant, Arabidopsis thaliana. In addition, several examples of transcription factors being successfully utilized to improve abiotic stress tolerance have now been reported, suggesting that this is a promising strategy to enhance stress tolerance in crops. In this chapter, we provide an overview of the present knowledge of plant transcription factors associated with various abiotic stress responses and their potential application to the enhancement of abiotic stress tolerance in plants. 26.1 Introduction Plants must adequately adapt to uctuations in the environment in which they grow as they cannot move from place to place. During the adaptation to stress conditions, plants modulate the expression of numerous genes. For instance, it has been shown by transcriptome analysis that drought stress induces expression of 277 genes, and represses another 79 genes, in Arabidopsis [1]. The expression levels of individual genes can be modulated through transcriptional control, alternative splicing events, and changes in RNA stability. Furthermore, the abundance of functional and active proteins can be regulated in response to stress signals by translational control, posttranslational modications, and degradation mechanisms. Although abiotic Improving Crop Resistance to Abiotic Stress, First Edition. Edited by Narendra Tuteja, Sarvajeet Singh Gill, Antonio F. Tiburcio, and Renu Tuteja Ó 2012 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2012 by Wiley-VCH Verlag GmbH & Co. KGaA. j 591

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26Transcription Factors: Improving Abiotic StressTolerance in PlantsTetsuya Ishida, Yuriko Osakabe, and Shuichi Yanagisawa

Plant growth and productivity are greatly affected by environmental abiotic stresses,including drought, high salinity, high or low temperature, nutrient starvation, andexcess metals in soils. After perceiving these stress signals, plants modulate theexpression levels of various genes to adapt to and overcome environmental changes.Transcription factors thus play central roles in the regulatory networks that mediatethe adaptation of plants to various environmental stresses. Although our knowledgeof the transcription factors associated with abiotic stress response in crops is stilllimited, a number of such transcription factors have been recently identified,mainly in the model plant, Arabidopsis thaliana. In addition, several examples oftranscription factors being successfully utilized to improve abiotic stress tolerancehave now been reported, suggesting that this is a promising strategy to enhancestress tolerance in crops. In this chapter, we provide an overview of the presentknowledge of plant transcription factors associated with various abiotic stressresponses and their potential application to the enhancement of abiotic stresstolerance in plants.

26.1Introduction

Plants must adequately adapt to fluctuations in the environment in which they growas they cannot move from place to place. During the adaptation to stress conditions,plants modulate the expression of numerous genes. For instance, it has been shownby transcriptome analysis that drought stress induces expression of 277 genes, andrepresses another 79 genes, in Arabidopsis [1]. The expression levels of individualgenes can be modulated through transcriptional control, alternative splicing events,and changes in RNA stability. Furthermore, the abundance of functional and activeproteins can be regulated in response to stress signals by translational control,posttranslational modifications, and degradation mechanisms. Although abiotic

Improving Crop Resistance to Abiotic Stress, First Edition.Edited by Narendra Tuteja, Sarvajeet Singh Gill, Antonio F. Tiburcio, and Renu Tuteja� 2012 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2012 by Wiley-VCH Verlag GmbH & Co. KGaA.

j591

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stress responses in plants likely include various mechanisms to induce specificproteins, transcriptional control appears to be an important component of theseprocesses.

Transcriptional control is typically exerted through the action of transcriptionfactors that are specifically involved in particular signal responses. To more fullyunderstand the molecular mechanisms underlying stress-responsive gene expres-sion and thereby uncover potential strategies to improve stress tolerance in plants,the identification of the key transcription factors involved is absolutely necessary.Only a limited number of such analyses using crops have been conducted to date, buttranscription factors associated with abiotic stresses, namely, drought, high salinity,cold and heat, nutrient starvation, and excess metals in the soil, have been identifiedin recent studies both in themodel dicotArabidopsis and in rice, amonocot plant andone of the most important crops in the world. Furthermore, several successes inimproving stress tolerance have also been reported using these identified transcrip-tion factors. In this chapter, we provide an overview of these successful applicationsand also of the present knowledge of transcription factors involved in stressresponses in plants.

26.2Transcription Factors Involved in the Drought Stress Response

Aswater limitation severely impacts agricultural productivity, the enhanced toleranceto drought is one of the most important and sought after traits in the molecularbreeding of crops. Drought stress exerts its effects on various cellular and molecularevents in plants, particularly upon the expression of a variety of genes that areinvolved in not only stress tolerance but also in the enhancement of stress responsepathways. Indeed, transcriptome analyses have now indicated that more than 300transcripts are modulated by drought stress [1]. Owing to the diverse effects ofdrought stress, plant responses to water stress are thought to be regulated by anorchestrated but complex series of signaling networks, the details of which remain tobe elucidated [2, 3]. Furthermore, as drought and salinity stresses have been found tocause similar changes in the transcriptome inArabidopsis [4], the signaling pathwaysassociated with these stresses may influence and activate each other or operatethrough a sharedmechanism. In addition, a plant hormone, abscisic acid (ABA), hasbeen shown to play a critical role in drought stress. ABA is dramatically producedunder drought and salinity stress conditions and influences the expression of variousgenes that respond to them. Drought and salinity stress signaling and ABA signalingtherefore are integrated into a complex regulatory network that forms part of thestress response mechanism in plants.

The cellular processes that operate in response to drought stress are initiated by theperception of these conditions by specific sensors. Recent studies have revealedthe role of AtHK1/AHK1 in the perception of drought stress. AtHK1/AHK1 is ahistidine kinase in the two-component signaling system, which also mediates

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osmotic stress signaling in prokaryotes [5, 6]. Tran et al. have shown that AHK1functions as an osmosensor and that its overexpression improves tolerance todrought stress in Arabidopsis [6]. RPK1, a receptor-like kinase that is localized toplasmamembrane and controls several ABA responses inArabidopsis, was also foundto be involved in the early steps of osmotic stress signaling in plant cells [7, 8]. As thecomponents that function directly downstream of AtHK1/AHK1 and RPK1 have yetto be identified, the molecular mechanisms underlying drought stress signaling inplants remain mostly unknown. However, in the past decade, the knowledge of thetranscriptional control that functions during drought stress signaling has increasedmarkedly through the identification of several transcription factors that play criticalroles in the drought stress response in plants (Table 26.1).

26.2.1DREB2 Transcription Factors

Similar to other types of transcriptional regulation, stress-responsive transcriptionis mediated by particular cis-acting elements and trans-acting transcription factorsthat recognize these cis-elements [3]. Indeed, the drought-responsive cis-element(DRE, 50-TACCGACAT-30) has been identified in the promoter regions of droughtand salinity stress-inducible genes. Furthermore, a part of the DRE (50-CCGAC-30)has also been reported to function as the cis-element that regulates transcriptionfrom various cold-responsive gene promoters, and has been designated as the C-repeat (CRT) and the low-temperature-responsive element (LTRE) [9–12]. Thissuggests a close relationship between the regulatory mechanisms for drought andcold stress-responsive gene expression. Transcription factors that specificallyrecognize the DRE/CRTsequence have now been identified using yeast one-hybridscreening and are referred to as DREB1/CBF (DRE binding protein 1/CRT bindingfactor) and DREB2 [11, 13]. DREB1/CBFandDREB2 form the DREB/CBF family, asubfamily of the plant-specific AP2 (APETALA2)/ERF transcription factorfamily [14].

Although the function of DREB1/CBF was specifically characterized in the coldstress response in Arabidopsis, as discussed further later, expression of the DREB2genes, DREB2A and DREB2B, is induced by both dehydration and salinity stressbut not by cold stress [13–15]. Hence, DREB2 appears to be involved in both thedrought and the salinity stress response. This induction of DREB2 genes precedesthe induction of other stress-responsive genes that play roles in stress tolerance,such as LEA (late-embryogenesis abundant protein) genes, in agreement with theprimary role of DREB2 in the drought stress response. However, the overexpres-sion of DREB2A under the control of the cauliflower mosaic virus 35S RNA (35S)promoter does not affect the stress tolerance of transgenic Arabidopsis plants. Thisunexpected contradiction was resolved by further characterization of the DREB2Aprotein, which revealed that posttranslational modification is necessary for its fullactivation [13]. Indeed, Sakuma et al. showed that the negative regulatory domainexists in the central region of DREB2A and that deletion of this negative regulatory

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Table26.1

Tran

scriptionfactorsinvolved

indrou

ght,salin

ity,cold,

andheat

stress

tolerance.

Class

Type

Gene

cis-elem

ents

Indu

ction

Stress

References

APETA

LA2(AP2)

DREB/C

BF

DREB1A

/CBF3

DRE/CRT

Cold

Freezing,

drou

ght,salin

ity

[13,

45]

DREB/C

BF

DREB1B

/CBF1

DRE/CRT

Cold

Freezing,

drou

ght

[44]

DREB/C

BF

DREB1C

/CBF2

DRE/CRT

Cold

[freezing],[drou

ght],

[salinity]

[81]

DREB/C

BF

DREB1D

/CBF4

DRE/CRT

Drough

tFreezing,

drou

ght

[82]

DREB/C

BF

DREB2A

DRE/CRT

Drough

t,salin

ity

Droug

ht,heat

[16,

18]

Leucinezipp

er(bZIP)

AREB

AREB1/ABF2

ABRE

Drough

t,salin

ity,ABA

Droug

ht,salin

ity,glucose

[22–24

]AREB

AREB2/ABF4

ABRE

Drough

t,salin

ity,ABA

Droug

ht,salin

ity

[21]

AREB

ABF3

ABRE

Drough

t,salin

ity,ABA

Droug

ht,salin

ity

[21]

Nucleartran

scription

factor

NF-X

NF-X1

X1-bo

xSalin

ity,osmotic

Salin

ity,heat

[38,

80]

NFYA

NFYA

5CCAAT

Drough

t,ABA

Droug

ht

[39]

R2R

3-MYB

MYB

AtM

YB60

—Dow

nregu

latedby

drou

ght,ABA

[drough

t][41]

MYB

AtM

YB61

——

Decreased

stom

atal

aperture

[42]

MYB

AtM

YB15

Myb

recogn

ition

sequ

ences

Cold

[freezing]

[62]

Hom

eodo

main

OCP

OCP3

—Dow

nregu

latedby

drou

ght,ABA

[drough

t][43]

C2H

2zinc-finger

ZPT2

STZ

A(G/C

)TCold,

drou

ght,salin

ity,ABA

Droug

ht

[56]

Basic

helix–loop

–helix

MYC

ICE1

CATTTG

—Freezing

[57,

58]

Calmod

ulin

binding

CAMTA

CAMTA

3CM

Motifs

——

[64]

Heatshockfactor

HSF

AtH

sfA2

HSE

Heat

Heat

[72]

HSF

AtH

sfA3

HSE

Heat

Heat

[78,

79]

�—�indicatesthat

thebindingsequ

ence

andtheindu

cerhavenot

been

iden

tified

yet.Bracket

indicatesthat

genedisruptionim

proved

stress

tolerance.

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domain results in the production of a constitutively active form of this protein [16].Hence, transgenic Arabidopsis plants overexpressing the constitutively active formof DREB2A showed a stronger tolerance to drought stress, accompanied by anupregulation of various stress-responsive genes [16]. The protein that interacts withthe negative regulatory domain of DREB2A has recently been identified, as DRIP1(DREB2A interacting protein 1), and is a C3HC4 RING domain-containing protein.Furthermore, negative regulatory mechanisms for DREB2A activity was suggestedto involve 26S proteasome pathway-dependent proteolysis mediated by DRIP1 andits homologue DRIP2 [17].

Interestingly, the upregulated genes in the transgenic Arabidopsis overexpressingDREB2A include not only drought and salinity stress-responsive genes under theseconditions but also genes encoding heat shock proteins (HSPs) [18]. As expected,transgenic Arabidopsis plants overexpressing such genes also show an increasedtolerance to heat stress, whereas the corresponding knockout plants are impaired inthis respect [18]. This observation also implies the presence of a complex regulatorynetwork involving a crosstalk among various stress signaling pathways.

26.2.2Transcription Factors that Interact with the ABA-Responsive Element in DroughtStress-Responsive Promoters

Drought and salinity stress conditions are partly mediated by ABA that inducesexpression of various genes through theABA-responsive cis-element, theABRE.BothDRE/CRT and ABRE have been found in many stress-responsive gene promoters,suggesting that ABRE also plays a role in stress-responsive transcription [3]. AREB/ABFs (ABRE binding proteins/ABRE binding factors) have been identified in Arabi-dopsis, and theyarebZIP-type transcription factors [19, 20].Consistentwith their roles,the AREB/ABF transcripts accumulate in response to the exogenous application ofABA and to drought and salinity stress treatments [20]. Furthermore, the overexpres-sion of ABF3 and ABF4/AREB2 in Arabidopsis increases the expression of ABA-responsive genes such as the LEA genes and results in the enhancement of ABAsensitivity, glucosesensitivity, anddroughtstress tolerance [21].TheoverexpressionofABF2/AREB1 inArabidopsis also enhancesABAandglucose sensitivity and improvesdrought tolerance. In contrast, theabf2/areb1mutants exhibited reduced sensitivity ofglucose, which was not observed in the abf3 and abf4/areb2 mutants [22]. Similareffects caused by overexpression of ABF/AREB proteins but different phenotypes bydisruption of ABF/AREB genes may be suggestive of redundant but different roles.Similar to DREB2A, the modification of the ABF2/AREB1 protein was found to berequired for the full activation of ABF2/AREB1 [23, 24]. The overexpression of theactive formofABF2/AREB1 inArabidopsis, therefore, increasedABA-responsivegeneexpression and drought tolerance more strongly [23, 24].

The transactivation activity of ABF2/AREB1 has been shown to depend on ABAand thus is lower in the ABA-insensitive mutant abi1 [20]. Since the ABI1 protein is aphosphatase 2C (PP2C) [25, 26], ABA-dependent phosphorylation/dephosphoryla-tion is thought to be involved in the activation of AREB/ABF proteins. Indeed,

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Furihata et al. have shown that ABA treatment stimulates the activity of a 42-kDaprotein kinase inArabidopsis and induces the phosphorylation of Ser/Thr residues atR-X-X-S/T sites in AREB1 [24]. Furthermore, it has been revealed that the activity ofthe 42-kDa kinase toward ABF1, ABF2/AREB1, and ABI5 is impaired in thesnrk2.2snrk2.3 double mutant that harbors mutations in two genes encoding type-2 SNF1-related protein kinases (SnRK2.2/SRK2D and SnRK2.3/SRK2I) [27]. Thesnrk2.2snrk2.3snrk2.6 triple mutant shows severe phenotypes in terms of the ABAsensitivity, the phosphorylation of ABF/AREBs, and the ABA-dependent geneexpression [28–31]. The SnRKs have, therefore, been shown to be involved in theactivation of AREB/ABFs. It was recently revealed that ABA promotes interactionsbetween ABA receptors, PYR/PYL/RCARs, and PP2Cs, ABI1 and ABI2, which arenegative regulators of ABA signaling [32, 33], and thereby inhibits PP2C activity tocontrol ABA signaling [34, 35]. Therefore, ABA likely regulates ABF/AREB activitythrough the PYR/PYL/RCAR–PP2C–SnRK cascade and then contributes to thedrought and salinity stress response pathways, although the exact mechanism isunknown.

26.2.3Additional Transcription Factors Involved in the Drought Stress Response

Transcription factors of the MYB, NAC, and other families have also been suggestedto play roles in the drought response in plants [3]. One of these is a novel C2H2-typetranscription factor, DST (DROUGHTANDSALT TOLERANCE), which controls theexpression of genes involved in H2O2 homeostasis and mediates H2O2-inducedstomatal closure and abiotic stress tolerance in rice [36]. Both H2O2 and hydroxylradicals are typical reactive oxygen species (ROS). ROS production is induced by bothabiotic and biotic stress, including high light, osmotic stress, and pathogen attack,andROS detoxification is one of themost important steps in stress tolerance. Furthercharacterization of DSTmight, therefore, clarify the interaction between ROS andABA signaling pathways in the drought and salinity stress responses.

Another transcription factor associated with drought and salt stresses is anArabidopsis factor that is structurally related to the human NF-X1 protein (nucleartranscription factor X-box binding 1) and contributes to salt and defenseresponses [37, 38]. Li et al. have shown that NFYA5, a drought stress-induciblenuclear transcription factor Y, plays a role in controlling stomatal aperture anddrought tolerance [39]. Several transcription factors have also been found to regulatestomatal apertures under conditions of drought stress. Overexpression of an NACtranscription factor in rice, SNAC1 (stress-responsive NAC 1), which is expressed inguard cells, leads to an increased ABA sensitivity and stomatal closure and results inimproved drought and salt tolerance [40]. Two MYB transcription factors, AtMYB60andAtMYB61, which are also expressedmainly in guard cells, have been functionallycharacterized as importantmodulators of stomatal aperture and drought tolerance inArabidopsis. AtMYB60 is anegative regulator of stomatal closure under drought stressconditions and the atmyb60 null mutation results in the constitutive reduction ofstomatal opening,whereasAtMYB61 is a positive regulator of this process and its loss

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of function results in more-open stomata [41, 42]. OCP3, encoding a transcriptionfactor of the homeodomain family, also plays a role in controlling the ABA-inducedstomatal aperture and drought resistance [43]. These factors are likely to be associatedwith complex mechanisms underlying drought stress signaling in stomata.

26.3Transcription Factors that Mediate the Response to Cold Stress

As the expression of DREB1/CBF proteins (DREB1A-C/CBF1-3) is induced by coldstress [13, 15], these factors appear to be specifically engaged in the transcriptionalregulation of cold stress-responsive genes. Consistent with their induction, theoverexpression of DREB1B/CBF1 under the control of the 35S promoter increasestolerance to cold stress inArabidopsis [44]. Interestingly, however, the overexpressionof DREB1/CBF enhances the tolerance to not only cold stress but also drought andsalinity stress conditions [13, 45, 46], suggesting either that a crosstalk exists amongstress signaling pathways or that a mechanism shared by different stress signalingpathways is activated. Although the improved tolerance to cold stress indicates thatthe utilization of DREB1/CBF is an effective approach to improve cold stresstolerance, transgenic Arabidopsis lines overexpressingDREB1/CBF also show severegrowth defects [45]. Hence, Kasuga et al.were able to overexpressDREB1/CBFunderstress conditions using only a stress-inducible promoter [45]. As the newly generatedtransgenic Arabidopsis did not manifest any negative effect in terms of plantgrowth [45], the strategy with DREB1/CBF appears to be now a practical approachthat can be applied to crop improvement. In fact, the overexpression ofDREB1/CBFgenes also increased tolerance to freezing, chilling, and drought stress in variousplant species, including Brassica napus, tobacco, tomato, rice, wheat, and maize[47–54]. The overexpression ofDREB1/CBF in Arabidopsis triggers the upregulationof not only various stress-responsive genes including LEAprotein and cold-inducibleKIN protein genes but also a C2H2 zinc finger transcription factor gene. This gene,termed STZ, is one of the direct target genes of DREB1/CBF [55, 56]. Because theoverexpression of STZ, which functions as a transcriptional repressor, also enhancesthe tolerance to drought stress [56], the transcriptional cascade includingDREB/CBFand STZ appears to play a key role in the cold stress response in Arabidopsis.

The presence of a complex regulatory mechanism underlying the expressionof DREB1/CBF in response to stress signals has been revealed. The ICE1 (inducerof CBF expression 1), HOS1 (high expression of osmotically responsive gene 1), andMYB15 genes were found to encode factors involved in this regulatory mechanism(Figure 26.1). ICE1, a basic helix–loop–helix (bHLH) transcription factor, is a majorpositive regulator ofCBF3 through the binding ofmultiple cis-regulatory elements inthe promoter and promotion of transcription [57, 58]. On the other hand, HOS1 is aRING-type ubiquitin E3 ligase that negatively regulates DREB1/CBF gene expres-sion [59]. Miura et al. showed that the low-temperature-induced sumoylation of ICE1is mediated by the SIZ1 protein, a SUMO E3 ligase, and that this process is a keyregulatory component of cold stress-responsive gene expression [60]. This process is

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inhibited by HOS1, which mediates the ubiquitination and degradation of ICE1[58, 61].MYB15 that interactswith ICE1 is another regulator that binds andnegativelyregulates transcription from the CBF promoters [62]. Thus, cold stress influencesDREB1/CBF gene expression via protein sumoylation and ubiquitination and fine-tunes the expression of various stress-responsive genes during the stress toleranceresponse in plants (Figure 26.1) [63].

On the other hand, CAMTA3, a member of the CAMTA (calmodulin bindingtranscription activator) family of transcription factors, has been shown to be a positiveregulator of theDREB1C/CBF2 gene [64]. The camta3mutant plants show a reducedinduction of CBF2 under cold stress conditions, and the camta1 camta3 doublemutant shows a reduced freezing tolerance. This suggests a connection betweencalcium signaling and cold-regulated gene expression.

26.4Transcription Factors Mediating the Response to Heat Stress

Heat stress tolerance (thermotolerance) is also under the control of coordinatedsignaling pathways [65]. Heat stress or heat shock induces the synthesis andaccumulation of heat shock proteins in both plants and animals. TheHSPs comprise

Cold stress

DREB1A/CBF3

DRE/CRT

Stress-responsive gene expression

HOS1

SIZ1(SUMO E3)

ICE1

MYB15

MYB BS DREB1A/CBF3MYC BS

SUMO

?

ChromosomalDNA

Target genes ChromosomalDNA

Figure 26.1 The transcriptional network thatoperates during the cold stress response. TheDREB1A/CBF3 transcription factor that bindsthe DRE/CRT cis-acting elements and

regulates transcription is expressed under thecontrol of multiple components, includingMYB15, ICE1, SIZ1, and HOS1, in response tocold stress.

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five protein families, namely, the HSP100, HSP90, HSP70, and HSP60 families andthe small HSPs (sHSPs) [66]. HSPs primarily function as molecular chaperones toprevent the aggregation of denatured proteins caused by heat shock and to promotethe appropriate refolding of denatured proteins [67].

The heat-inducible expression ofHSP genes is regulated by heat shock transcrip-tion factors (HSFs) that are conserved in eukaryotes. HSFs bind to heat shock-responsive elements (HSEs), which are conserved cis-elements in the HSP genepromoters [68]. Among 21 HSFs in Arabidopsis, AtHsfA1a and AtHsfA1b havealready been shown to play important roles in the expression of HSP genes in theearly phase of the heat shock response [69, 70]. Furthermore, Guo et al. havedetermined the AtHsfA1a binding sites in vivo and shown that they are located inthe promoter regions of a set of classical heat shock protein genes and a transmem-brane CLPTM1 family protein gene [71]. A heat stress-induced HSF, AtHsfA2, hasalso been shown to activate HSP expression and then enhance acquired thermo-tolerance in Arabidopsis [72].

The heat stress response is mediated through the modulation of HSF activity byHSPs. Under nonstress conditions, constitutively expressed HSFs are inactivated bythe binding of HSPs and maintained in the cytosol. However, when plants perceiveheat stress, the HSP–HSFcomplexes dissociate and the HSFs localize to the nucleusto regulate gene expression [73–76]. Furthermore, the activity of HSFs is also knownto be regulated by additional mechanisms. For instance, the activity of HSFs ismodulated through phosphorylation/dephosphorylation events in response to heatstress [74, 77]. On the other hand, the heat stress response has also been found to bedecreased by the heat shock factor binding protein 1 (HSBP1) that binds HSFs andthen inhibits HSF activity [74]. Interaction with HSBP1 thus represents anotherregulatory mechanism for HSF activity.

Interestingly, the drought stress-responsive transcription factor, DREB2A, alsoinfluences heat tolerance [16, 17]. The overexpression of DREB2A in Arabidopsisincreases heat tolerance by inducing the expression of the AtHsfA3 gene [78, 79].NF-X1 that was initially identified as a transcription factor associated with the salinitystress response [37, 38] has also been reported to contribute to heat tolerance [80].These findings consistently indicate a connection between heat stress and otherstress signaling pathways in the complex regulatory network that mediates stressresponses in plants.

26.5Transcription Factors Involved in Nutrient Deficiency

Plant nutrients in the soil, particularly nitrogen and phosphorus, are major factorsthat affect plant growth. Plants have, therefore, developed mechanisms to effectivelyabsorb and utilize plant nutrients. In the past decade, several transcription factorsinvolved in nutrient deficiency have been identified. Furthermore, genetic modifica-tions based on these factors suggest that theymay be potent tools for improving plantgrowth under nutrient-deficient conditions (Table 26.2).

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26.5.1Transcription Factors Involved in the Nitrogen Response

Nitrogen is amacronutrient that is required in abundance for plants. Plants activelyattempt to obtain inorganic nitrogen in the soil due to the constitutive constraintson nitrogen availability in natural ecosystems. Although plants can use both nitrateand ammonia in the soil as a nitrogen source, nitrate is the major source for landplants. The possible roles of nitrate, nitrite, and glutamine as nitrogen signals thatregulate cellular processes in plant cells have been proposed in the past [83–87], andnitrate has been well characterized as the main nitrogen signal. Therefore, bothnitrate-inducible responses and nitrogen-deficient responses are likely to be closelyrelated to nutrient-deficient stress responses. Transcription factors involved innitrate-inducible and nitrogen-deficient responses are given equal weight in thissection.

Table 26.2 Transcription factors involved in nutrient responses.

Nutrient Gene Gene family Species References

N ANR1 MADS A. thaliana [102, 103]NSR1 MYB A. thaliana [95]NLP7 RWP-RK A. thaliana [96]LBD37/38/39 LBD A. thaliana [97]GNC GATA A. thaliana [99]Dof1 Dof Zea mays [101, 102]

P PHR1 MYB A. thaliana [94, 105]PHL1 MYB A. thaliana [105]PHR2 MYB A. thaliana [95]OsPHR1 MYB O. sativa [108]OsPHR2 MYB O. sativa [108]MYB62 MYB A. thaliana [115]ZAT6 C2H2 zinc finger A. thaliana [116]WRKY75 WRKY A. thaliana [117]WRKY6 WRKY A. thaliana [118]BHLH32 bHLH A. thaliana [120]OsPTF1 bHLH O. sativa [121]

S SLIM1 EIL A. thaliana [124]Fe FER bHLH Lycopersicon esculentum [130]

FIT1 bHLH A. thaliana [132, 133]AtbHLH38/39 bHLH A. thaliana [134, 135]OsIRO2 bHLH O. sativa [136]IDEF1 ABI3/VP1 O. sativa [139]IDEF2 NAC O. sativa [143]

Zn bZIP19/23 bZIP A. thaliana [149]

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Transcriptome analysis of nitrogen-deficient response in rice roots has revealedthat the modulation of a number of genes, including putative transcription factorgenes, is induced by nitrogen-deficient conditions [88]. However, no additionalinformation on these genes has yet been reported. On the other hand, thenitrate-inducible response in plants has been analyzed inmore detail. Transcriptomeanalysis has revealed that the expression of numerous genes is modulated inresponse to the nitrate supply even in the Arabidopsis mutant that has little nitratereductase (NR) activity [84, 89, 90]. Thus, nitrate has been suggested to function as asignal molecule and to directly modulate gene expression because it is reduced toammonium by reductive reactions catalyzed by two enzymes, NR and nitritereductase (NIR), and then assimilated into glutamine. Furthermore, a cis-elementthat is sufficient to drive nitrate induction was recently identified in promoteranalysis of the Arabidopsis gene for NIR [91]. This element did not respond toglutamine, although the expression ofNIR was found to be repressed by glutamine,in an experiment that defined the multiple cis-elements involved in the nitrogenresponse [91].

Transcription factors that bind directly to the identified nitrate-responsive cis-element have not been elucidated as yet. However, several genes encoding tran-scription factors are known to respond to nitrogen starvation or nitrate supply.Arabidopsis ANR1, which encodes an MADS transcription factor, is expressedpreferentially in roots [92]. Although lateral roots proliferate in response to a localizednitrate supply, this proliferation does not occur when expression of ANR1 issuppressed or ANR1 is disrupted [92, 93]. ANR1 was also found to be induced bynitrate starvation and repressed by the subsequent nitrate resupply, suggesting apossible feedback regulation of the lateral root growth rates via the nitrogen status ofthe plant [93]. There are also seven other MADS-box genes, which are slightlyupregulated by nitrate starvation [93].

An Arabidopsis gene for NSR1, which is structurally close to the PHR1 (PHOS-PHORUS STARVATION RESPONSE 1) transcription factor involved in the phos-phate (Pi) starvation response [94], is also induced by nitrate starvation, although ithas not yet been characterized in any detail [95]. The Arabidopsis NLP7 gene thatencodes a RWP-RK transcription factor also appears to be involved in the nitrogenresponse, although its expression is not regulated by the nitrogen source or by thepresence of nitrate [96]. When the NLP7 gene was disrupted in Arabidopsis, theplants exhibited the features of nitrogen-starved plants, such as an increase in theratio of root/shoot, a longer primary root, and a higher lateral root density.Induction of the nitrate transporter genes (NRT2.1 and NRT2.2) and the NR genes(NIA1 and NIA2) by nitrate was found to be impaired in the nlp7 mutant. Thus,NLP7 is a putative regulatory protein for nitrogen assimilation, although there is nodirect evidence that NLP7 directly regulates the expression of nitrate-induciblegenes.

The nitrate-inducible LBD37/38/39 genes of Arabidopsis are members of theLBD (LATERAL ORGAN BOUNDARY DOMAIN) family of transcription fac-tors [97]. Because these genes are induced by not only nitrate but also other

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nitrogen sources, ammonium and glutamine, these genes are nitrogen responsiverather than nitrate responsive. Overexpression of LBD37, LBD38, or LBD39suppresses the expression of PAP1 and PAP2 that encode MYB transcriptionfactors regulating expression of genes involved in anthocyanin synthesis [98]. Theoverexpression of LBD37, LBD38, or LBD39 also repressed the expressions ofnitrate transporter genes and NR genes [97], suggesting that LBD37/38/39proteins play negative roles in the nitrogen response.

An Arabidopsis gene, GNC (GATA, NITRATE-INDUCIBLE, CARBON-METABO-LISM INVOLVED), was also shown to be a nitrate-inducible gene [99]. This geneencodes a GATA transcription factor and is expressed in leaves and buds in responseto nitrate, but not in roots. In the gncmutant, the chlorophyll level is reduced and theexpression of genes involved in carbonmetabolism is repressed. The gncmutant wasalso found to bemore sensitive to exogenous glucose, whereas transgenicArabidopsisoverexpressing GNC is less so. Carbon and nitrogen metabolism are closelylinked [100] because nitrogen assimilation requires not only inorganic nitrogen butalso the carbon skeleton 2-oxoglutarate (2-OG) that is produced from photoassimi-lated carbohydrates. On the basis of the phenotype of the gnc mutant and the GNCoverexpressors,GNC is proposed to function in the regulation of carbon andnitrogenmetabolism in response to nitrate.

Although recent studies have identified several transcription factors involved inthe nitrate response and/or nitrate status in plant cells, the enhancement ofnitrogen assimilation, one of the most important agricultural traits sought afterby breeders, has not been achieved yet using these factors. However, suchenhancement was achieved using Dof1, a member of plant-specific Dof transcrip-tion factor family (Figure 26.2) [101]. The transgenic Arabidopsis lines expressingthe Dof1 transcription factor, a putative regulator of 2-OG production, were foundto show enhanced nitrogen assimilation and a larger pool of organic nitrogen andthus showbetter growth under the low-nitrogen conditions (Figure 26.2) [102]. Thissuggested the importance of the coordinated modulation of carbon and nitrogenmetabolism in improving the adaptive ability of plants to nitrogen-deficientenvironments.

26.5.2Phosphate Starvation-Responsive Transcription Factors

26.5.2.1 PHR1 Involved in Phosphate Starvation ResponsePhosphorus is a major structural component of nucleic acids and membrane lipidsand takes part in the regulation of many biochemical and physiological processes.Plants acquire phosphorus as inorganic phosphate (Pi). Several transcription factorsinvolved in the Pi starvation response have been recently identified in vascular plants.Among these, PHR1 fromArabidopsis thalianawas the first to be isolated and is thusthe most well characterized of these transcription factors [94]. The gene encodingPHR1was identified by a genetic screen of a transgenicArabidopsis line harboring theAtIPS1::GUS reporter construct that was specifically responsive to Pi starvation. Inthe phr1 mutant, the root/shoot ratio was impaired and anthocyanin did not

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accumulate under Pi starvation conditions. Furthermore, the cellular Pi content waslower in the phr1 mutant than in the wild-type Arabidopsis under Pi-sufficientconditions. In accordance with the phr1mutant phenotype, the expression of severalPi-responsive genes including genes encoding Pi transporters, acid phosphatases,and enzymes involved in anthocyanin biosynthesis was found to be impaired in thephr1mutant [94, 103, 104]. Conversely,whenPHR1was overexpressed inArabidopsis,the Pi content in the shoots increased, accompanied by the elevated expression ofseveral Pi starvation-responsive genes [104].

PHR1 is a member of the MYB-CC gene family, which is a subtype of the MYBsuperfamily and includes 15 members in Arabidopsis [105]. Among these, PHL1(PHR1-LIKE1) is phylogenetically most closely related to PHR1. It has been shownthat PHR1 and PHL1 are functionally redundant in Arabidopsis [105] and formheterodimers to bind an imperfect palindromic DNA sequence called P1BS (50-GNATATNC-30), which are enriched in the promoter regions of many Pi starvation-responsive genes [94, 105–107]. Although PHR1 expression is not affected by the Pistatus, another PHR1 homologue, PHR2, was found to be induced by Pi depriva-tion [94, 95]. Thus, PHR2 could also be involved in the Pi starvation response,although it has not yet been characterized in sufficient detail. Although rice has twoPHR1 homologues, OsPHR1 and 2, only the OsPHR2 overexpressor accumulates

Figure 26.2 Improvement of plant growthby Dof1 under the low-nitrogen conditions.(a) The glutamine content is lower in controlArabidopsis plants than the transgenicArabidopsis plants expressing the Dof1transcription factor, and control Arabidopsisplants withered their leaves earlier when theywere grown under the low-nitrogen conditions.

(b) The metabolic pathway for nitrogenassimilation in plants. PEP:phosphoenolpyruvate; OAA: oxaloacetate;PEPC: phosphoenolpyruvate carboxylase; PK:pyruvate kinase; CS: citrate synthase; ICDH:isocitrate dehydrogenase. PEPC, PK, CS, andICDH genes are putative target genes of theDof1 transcription factor.

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excess Pi in its shoots with upregulated levels of Pi starvation-responsive genetranscripts, similar to PHR1 overexpressing Arabidopsis [104, 108].

In addition to the analyses of the physiological roles of PHR1 and related factors,the molecular regulation of PHR1 expression has also been studied. Because theexpression levels of PHR1 and the nuclear localization of the PHR1 protein areunchanged by the Pi status, posttranslational modifications can be considered to bethe regulatory mechanism for PHR1 activity [94]. Indeed, the PHR1 protein wasrevealed to be sumoylated by SIZ1, a small ubiquitin-like modifier (SUMO) E3ligase [109]. The functional relationship between PHR1 activity and sumoylation wasfurther shownby themodified expression of target genes of PHR1 in the siz1mutant.These target genes, AtIPS1 and AtRNS1, were induced more slowly in the siz1mutant than the wild type by Pi starvation, in agreement with the putative positiveregulation of PHR1by SIZ1. The siz1mutant also exhibitedmore severe Pi starvationphenotypes under such conditions, such as retarded primary roots, extensive lateralroots, and root hair development, an increase in the root/shoot growth ratio, andanthocyanin accumulation, although the intracellular Pi content in the siz1 mutantwas similar to that of wild- type Arabidopsis [109].

A microRNA, miR399, was found to be another of the PHR1 targets [103].In plants, miRNAs recognize specific mRNA sequences based on sequencecomplementarity and function to cleave their target mRNAs. As the target ofmiR399 is the mRNA of PHO2 encoding a ubiquitin-conjugating E2 enzyme,Arabidopsis lines overexpressing miR399 exhibit a phenotype similar to that of thepho2 mutant [103, 110]. Interestingly, other small noncoding RNAs from AtIPS1and At4 contain a sequence motif that is partially complementary to miR399 andinhibit the cleavage of PHO2 mRNA by miR399 [111, 112]. As the expression ofAtIPS1/At4 is also induced by Pi starvation, differential induction modes ofmiR399 and AtIPS1/At4 and/or the translocation of miRNA399 has been sug-gested to regulate the PHO2mRNA level in response to changes in the availabilityof Pi [113].

26.5.2.2 Additional Transcription Factors Induced by Phosphate StarvationIn addition to PHR1 and its homologues, several other transcription factors havebeen shown to be involved in the Pi starvation response. Some of them wereidentified throughmicroarray analysis of Pi starvation-responsive genes [106, 114].MYB62 of Arabidopsis encodes an R2R3-type MYB transcription factor and itsexpression in leaves is induced by Pi starvation [115]. When MYB62 is over-expressed, the root system architecture is altered. Furthermore, the root/shootratio increases under conditions of Pi sufficiency, anthocyanin accumulates, andthe acid phosphatase activity is elevated. The expression of several Pi starvation-induced genes has also been shown to be suppressed in MYB62 overexpressinglines. Thus, MYB62 is suggested to function as a repressor of the Pi starvationresponse [115].

Arabidopsis ZAT6, encoding a C2H2 zinc finger transcription factor, was also foundto be induced byPi starvation [116].Overexpression ofZAT6 inArabidopsis leads to an

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increased accumulation of anthocyanin and acid phosphatase secretion, a reductionboth in the Pi uptake and in the total Pi content, and retardation of primary roots inyoung seedlings. However, when plants overexpressing ZAT6 become older, theyform longer lateral roots, which leads to an increased root/shoot ratio and total Picontent. Moreover, the expression of several Pi starvation-inducible genes is sup-pressed in the ZAT6 overexpressing lines, indicating that ZAT6 is also a repressor ofthe Pi starvation response.

WRKY75 is another Pi starvation-inducible gene [117]. The suppression ofWRKY75 by RNAi results in an increased anthocyanin accumulation, reduced Piuptake, and reduced acid phosphatase activity. In addition, the lateral rootlength and number and the root hair number are increased in these knockdownplants, leading to an increased Pi content. Furthermore, the expression of Pistarvation-inducible genes is also suppressed in the WRKY75 RNAi lines. Hence,WRKY75 has been suggested to be a positive regulator of Pi starvation response.The involvement of another WRKY gene, WRKY6, in the Pi starvation responsewas also indicated by the phenotype of Arabidopsis lines overexpressing this geneunder low Pi conditions. Similar to the pho1 mutant, these transgenic lineswere found to be defective in loading Pi into the xylem [118, 119]. It was shownthat WRKY6 can bind to two W-boxes of the PHO1 promoter to repress the PHO1gene. In addition, WRKY42, the closest homologue of WRKY6, also repressesPHO1 expression. Furthermore, degradation of the WRKY6 protein by the 26Sproteasome under low Pi conditions was found to cause the repression ofPHO1 [118], indicating a molecular mechanism for Pi starvation that is mediatedby a transcription factor.

Another Pi starvation-inducible gene in Arabidopsis, BHLH32, encodes a bHLHtranscription factor [120]. In the bhlh32 mutant grown under Pi-sufficient condi-tions, the Pi starvation-inducible expression of PPCK (phosphoenolpyruvate car-boxylase kinase) genes, anthocyanin accumulation, and root hair formations werepromoted. Also, the Pi content in the mutant was higher than that of the wild-typeArabidopsis. Thus, BHLH32 is likely to be a negative regulator of the Pi starvationresponse.

The OsPTF1 (Rice Pi starvation-induced transcription factor 1) gene encoding abHLH transcription factor was identified using a subtractive hybridization methodwith a cDNA library that was constructed using mRNA from rice roots subjected toPi starvation [121]. The expression of OsPTF1 was found to be upregulated byPi starvation in roots but remained constitutively active in shoots. Transgenic riceplants overexpressing OsPTF1 showed increase in the tiller number, shoot and rootbiomass, and the Pi content under low Pi conditions compared to wild-type riceplants.

Although the involvement of several Pi starvation-inducible transcriptionfactor genes in the Pi starvation response has been conclusively shown byphenotypic analyses of the corresponding mutants and/or transgenic plants,the molecular functions of these factors and their target genes remain to beclarified.

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26.5.3Transcription Factors Associated with the Sulfur Starvation Response

Sulfur is an essential macronutrient required for plant growth. Plants uptake sulfatein the soil and use it for synthesis of cysteine and methionine, which are furtherutilized for the biosynthesis of other sulfur-containing organic compounds. Becauseof the important roles a number of sulfur-containing compounds play in plants,sulfur starvation induces the expression of sulfate transporters and activates theuptake of sulfate in roots. It is known that SULTR1;1 and SULTR1;2 are the high-affinity sulfate transporters inArabidopsis, the transcripts of which are upregulated bysulfur starvation and downregulated by the sulfur-containing metabolites, cysteineand glutathione [122]. Analysis of theSULTR1;1 gene promoter revealed the presenceof a sulfur-responsive cis-element (SURE), which directs both the induction of thisgene by sulfur starvation and its repression by cysteine and glutathione [123].Furthermore, a 7-bp sequence within the SURE was found to be the core sequencethat functions in the response to sulfur starvation. This core sequence is present inmany sulfur starvation-responsive gene promoters [123], although not in theSULTR1;2 promoter. No SURE binding protein has yet been identified.

Although transcription factors directly regulate the expression of sulfur starvation-responsive genes, a mutation in a gene encoding the SLIM1 (SULFUR LIMITA-TION 1) transcription factor has been found to affect the sulfur starvation-responsivegene. SLIM1 was identified through the analysis of an Arabidopsis mutant in whichthe expression of GFP originating from the SULTR1;2 promoter::GFP construct wasabolished under sulfate starvation conditions [124]. SLIM1 is amember of the EIN3/EIL family that includes the ethylene-responsive transcription factors, EIN3 andEIL1, in Arabidopsis [125], but appears to be functionally distinguishable from othermembers of the EIL family, as they cannot rescue the phenotype of the slim1mutants [124]. In the slim mutant, the sulfate uptake activity was reduced and thegrowth of primary roots was inhibited under the sulfur-limiting conditions. Tran-scriptome analysis of the slim1mutant revealed that SLIM1 functions to upregulatethe genes for several isoforms of sulfate transporters, including SULTR1;1 andSULTR1;2 that function to uptake sulfate and SULTR4;2 that functions to releasesulfate from the vacuoles in root tissues [122, 126] in response to sulfur starvation. Inaddition, a serine acetyltransferase gene, SERAT3;1, involved in cysteine synthesis,and a thioglucosidase gene involved in the degradation of glucosinolates for catabolicsulfur recycling were found to be upregulated under sulfate starvation conditions inthe SLIM1-dependent manner [127]. The expression of genes encoding enzymesinvolved in the biosynthesis of glucosinolate, a major sulfur-containing secondarymetabolite [128], was also affected by the slim1mutation. Hence, SLIM1 is proposedto be a global regulator of sulfate metabolic pathways [124]. Since the level of SLIM1mRNA is not modulated by changes in the sulfur conditions, posttranscriptionalmodifications in response to sulfur starvation may be critical for controlling SLIMactivity [124]. Despite the close relationship between the SLIM activity and the sulfurstarvation response, it is still unknown whether SLIM directly regulates genes thatfunction in the regulatory network underlying the sulfur starvation response.

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26.5.4Iron Response-Related Transcription Factors

Iron is an essential micronutrient for plants and is required for cellular processesincluding photosynthesis and nitrogen fixation in legumes. Under aerobic oralkaline conditions, iron is present in an oxidized low-soluble Fe(III) form in thesoil, which is not readily available for plants. Plants thus need to develop amechanism for the effective acquisition of iron in the soil. Higher plants, withthe exception of grasses, release protons around the roots to lower the pH, inducethe expression of Fe(III) chelate reductase to reduce iron to the more-soluble Fe(II)form, and induce an Fe(II) transporter system for the uptake of Fe(II) into the rootepidermis. This plant response to iron deficiency is called the strategy Iresponse [129]. On the other hand, grasses have evolved a distinct strategy foriron uptake that is known as strategy II. They produce molecules of the mugineicacid family called phytosiderophores (PSs). PSs are secreted around the roots toform the soluble Fe(III)–PS complex, which is then taken up into the root cellsthrough the Fe(III)–PS complex transporters [129].

The tomato FER was the first identified transcription factor associated with thestrategy 1 response [130]. FER is a bHLH transcription factor expressed in roots underiron-deficient conditions [130]. Its abundance appears to be posttranscriptionallymodulated, as it is detectable only when the iron levels are low. This is despite thefact that FER is constitutively and strongly expressed under the control of the 35Spromoter [131]. In the fermutant tomato, there is a decrease in Fe(III) chelate reductaseactivity and expression of the Fe(II) transporter gene [130]. Similarly,Arabidopsis FIT1/FRU (Fe-DEFICIENCY-INDUCED TRANSCRIPTION FACTOR1/FER-LIKE REGU-LATOROF IRONUPTAKE), an orthologue of tomato FER [130, 131], was shown to beinvolved in the expressionof theFe(III) chelate reductase (FRO2)gene andpromote theaccumulation of Fe(II) transporter (IRT1) in the roots under iron-deficient condi-tions [132, 133]. The overexpression of FIT1 did not affect the expression of FRO2 andIRT1.However, when FIT1 was coexpressed strongly with AtbHLH38 or AtbHLH39,which physically interactwith FIT1, bothFRO2 and IRT1were constitutively expressedregardless of the iron conditions [134]. Furthermore, Fe(III) chelate reductase activitywas higher in the transgenic Arabidopsis lines, coexpressing FIT1 and AtbHLH38 orAtbHLH39, than in the wild-type and transgenic lines overexpressing FIT1,AtbHLH38, orAtbHLH39 alone.Moreover, the coexpressors accumulate IRT1 proteinregardless of the iron conditions, resulting in the accumulation of more iron in theirshoots [134]. As the AtbHLH38 and AtbHLH39 genes are upregulated under condi-tions of iron deficiency [134, 135], the cooperative action of FIT1, and AtbHLH38 andAtbHLH39, has been shown to play a critical role in the response to this stress.

The transcription factor involved in the strategy II response has also been identifiedthrough the profiling of iron deficiency-induced genes [136, 137]. This was a ricebHLH transcription factor, OsIRO2. Under iron-deficient conditions, rice plantsoverexpressing OsIRO2 exhibited improved growth, whereas the knockdown linesgenerated by RNAi showed a reduced biomass and accumulated less iron [137]. Theexpression of many genes involved in PS biosynthesis and a Fe(III)-PS transporter

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gene, OsYSL15, was enhanced in the OsIRO2 overexpressors and repressed in theRNAi lines [137, 138]. Recently, it has been shown thatOsIRO2 expression is regulatedby another transcription factor, IDEF1 [139]. IDEF1 is a member of the ABI3/VP1family of transcription factors and binds to the iron deficiency-responsive cis-element,IDE1, which is present in the promoter of the barley IDS2 gene involved in PSbiosynthesis [139, 140]. Transgenic rice expressing IDEF1under the control of an irondeficiency-inducible promoter exhibited improved tolerance to iron deficiency [139],accompanied by a stronger expression of genes involved in PS biosynthesis, includingOsYSL15, a Fe(II) transporter gene OsIRT1, and a metal-nicotianamine transportergene OsYSL2 [139, 141, 142].

Another iron deficiency-responsive cis-element, IDE2, was found in the promoterof the barley IDS2 gene [140], and it has been shown that a rice NAC transcriptionfactor, IDEF2, binds to this cis-element [143]. When IDEF2 function was repressedusing the RNAi technique and chimera repressor gene-silencing technology(CRES-T), the resulting rice plants accumulated more iron in both their shoots andtheir roots under iron-sufficient conditions. On the other hand, under conditions ofiron deficiency, the iron concentration appears to be lower in the shoots of the RNAiand CRES-T rice lines, whereas the iron concentrations in the roots were higher intransgenic lines. This phenomenon was explained by the hypothesis that the severesuppression ofOsYSL2 in the IDEF2 RNAi rice and the CRES-Trice lines under irondeficiency might prevent OsYSL2 from translocating iron from the roots to theshoots [142, 143]. Transcripts of IDEF1 and IDEF2 are constitutively expressedregardless of the iron conditions, and IDEF proteins may therefore be modified andregulated posttranscriptionally [139, 143].

26.5.5Zinc Deficiency-Responsive Transcription Factors

Zinc is an essential micronutrient and an essential cofactor for many transcriptionfactors, protein interaction domains, and enzymes both in plants and in ani-mals [144]. Members of the ZIP family of metal transporters play a major role inzinc uptake in plants [145]. In Arabidopsis, a ZIP transporter gene, ZIP4, is stronglyinduced in response to zinc deficiency [146].UsingZIP4promoter fragments as baitsin a yeast one-hybrid assay, two homologous transcription factors, bZIP19 andbZIP23, were identified recently [147]. These factors act redundantly, and theexpression levels of both genes are higher under zinc-deficient conditions. Further-more, the bzip19 bzip23 double mutant exhibited a zinc deficiency-hypersensitivephenotypeunder zinc-deficient conditions. Both the bZIP19 and the bZIP23proteinswere found to bind a 10-bp imperfect palindromic sequence, termed the ZDRE.Subsequently, ZDRE motifs were identified in the promoters of ZIP transportergenes that are responsive to zinc deficiency. Consistent with the roles bZIP19 andbZIP23 play in zinc deficiency-responsive transcriptional control, zinc deficiency-responsive ZIP transporter genes were not found to be induced in the bzip19 bzip23double mutant by a zinc deficiency. Orthologues of bZIP19 and bZIP23, their targetgenes, and the ZDRE motif are conserved in different plant species, indicating that

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mechanisms underlying the zinc-deficiency response are conserved in the plantkingdom [147].

26.6Transcription Factors Involved in Responses to Excess Metals in the Soil

Some metals in the soil are known to induce stress responses. Transcription factorsinvolved in the tolerance to excess aluminum (Al) and cadmium (Cd) in the soil havebeen identified, suggesting that they could be used in future strategies to developmetal-resistant crops.

26.6.1Transcription Factors Mediating Al Tolerance

Ionic Al that is produced in acidic soils inhibits root elongation, even at lowconcentrations. The consequent inhibition of water and nutrient uptake results ina reduction in crop production [148]. One of the best-known mechanisms to tolerateAl is to excrete organic acid anions, which chelate this metal [148]. In the case ofArabidopsis, malate is excreted and the expression of a malate transporter gene,AtALMT1, is induced in response to Al [149]. STOP1 (SENSITIVE TO PROTONRHIZOTOXICITY 1) encoding a C2H2-type zinc finger protein was found to be aregulator of this Al response [150]. An Arabidopsis mutant, stop1, was originallyisolated by its hypersensitivity to proton rhizotoxicity andwas found to exhibit shorterroots under Al stress and low pH conditions. On the other hand, another C2H2-typezinc finger protein, ART1 (Al resistance transcription factor 1), regulates Al tolerancein rice [151]. Similar to the case of the stop1mutant of Arabidopsis, the root length ofthe art1mutantwas shorter than that of thewild-type rice underAl stress. In responseto Al, ART1 induces the expression of Al tolerance genes including STAR1 andSTAR2, which encode ATP binding and transmembrane domains of a novel ABCtransporter, respectively [151, 152]. The ABC transporter transports UDP glucose,which may be used to modify the cell wall [152]. Neither the STOP1 transcript levelsnor the ART1 transcript levels were affected by Al treatment, suggesting that theexpression of STOP1 and ART1 may be posttranscriptionally regulated by the Alconditions. As microarray data have shown that genes downstream of STOP1 aredifferent from those ofART1, except in a few cases, STOP1 andART1were suggestedto produce Al tolerance via different mechanisms in distinct plant species [151, 153].

26.6.2The HsfA4a Transcription Factor that Confers Cd Tolerance

Cd is one of themost dangerous heavymetals in the environment. Recently, class A4heat shock transcription factors (HsfA4a) were found to confer Cd tolerance in riceand wheat (Triticum aestivum) [154]. Wheat and rice HsfA4a proteins were identifiedas factors that conferred Cd tolerance to a Cd-hypersensitive yeast strain. Over-

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expression ofwheatHsfA4awas also found to enhanceCd tolerance in transgenic riceplants, whereas the knockdown of HsfA4a in rice increased the sensitivity to Cd,suggesting that HsfA4a plays an important role in Cd tolerance in rice. In both riceandwheat, Cd treatment induces the expression ofHsfA4a, which in turn induces theexpression of a gene encoding a metallothionein that is a well-known chelator of Cd.Although further analysis including the identification of additional target genes ofHsfA4a might be necessary, phenotypic analysis of transgenic rice plants over-expressingHsfA4a has already suggested that theHsfA4a transcription factor will beuseful in the future development of Cd-resistant plants to enable the phytoremedia-tion of Cd-contaminated fields.

26.7Conclusions and Prospects

As described in this chapter, a number of transcription factors involved in abioticstress responses have been identified over the past decade. Although most werefound in Arabidopsis, the knowledge obtained using this and other model plants hasallowed us to identify functional homologues in commercially important crops and todevelop strategies for enhancement of stress tolerance in these plants. Transcriptionfactors associated with stress responses may possess the potential to induce thesystematic activation and/or repression of stress-responsive genes in perfect syn-chrony. Thus, when expression of multiple components in a single cascade orpathway or activation ofmultiple different cascades or pathways is needed to improvetolerance to a particular stress signal, the utilization of transcription factors could bean ideal strategy. In fact, the expression of Dof1 led to the enhancement of nitrogenassimilation and better growth under nitrogen-deficient conditions, which had notbeen adequately achieved through the genetic modification of genes for enzymesinvolved in nitrate reduction and assimilation (Figure 26.2). This is a good example ofhow the use of transcription factors can improve stress tolerance via the synchronousmodification of multiple genes.

The phenotypes of transgenic plants overexpressing some transcription factorshave already indicated that it is possible not only to improve tolerance to abiotic stressand increase plant productivity but also to developmetal hyperaccumulator plants forthe phytoremediation of contaminated soil or water. Many transcription factors arelikely expressed in plant cells. Indeed, more than 1000 genes encoding putativetranscription factors have been identified in the Arabidopsis genome [155]. However,the functions ofmost of the plant transcription factors have not yet been determined.Thus, identifying the unknown functions of plant transcription factors may make itpossible in the future to generate crops with superior characteristics.

Recent advances in our understanding of the physiological andmolecular featuresof transcription factors associated with abiotic stress suggest that posttranslationalcontrol is a key regulatory mechanism in many cases. This agrees with the generalhypothesis that the gene expression associatedwith the primary response ismediatedby preexisting transcription factors. Hence, the genetic modification of mechanisms

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underlying such posttranscriptional control may be a strategy to improve the stresstolerance of crops. Thismight be particularly true when the simple overexpression ofa transcription factor does not produce the expected phenotype or results in a strongphenotype with negative effects. In fact, when DREB1/CBF was constitutively andstrongly expressed under the control of the 35S promoter, growth defects wereinduced as the stress response in general involves growth arrest. Further analysis ofthe regulatory mechanisms underlying transcription factor activity control in plantsis thus warranted and would expand the opportunities to develop crops with animproved tolerance to environmental stresses in a more sophisticated manner.

Acknowledgments

We thank theCRESTprogramof the JapanScience andTechnologyAgency (JST), and aGrant-in-Aid for Scientific Research on Innovative Areas (21114004) from theMinistryof Education, Culture, Sports, Science and Technology of Japan for their support. Weapologize that some references could not be cited due to space constraints.

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