Regulatory Network of Transcription Factors in Response to Drought in Arabidopsis and Crops

September 2012

ScienceDirect

Vol. 19 No. 3 1-13

Journal of Northeast Agricultural University (English Edition)

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Regulatory Network of Transcription Factors in Response to Drought in Arabidopsis and Crops Chen Li-miao1, 2, Li Wen-bin2, and Zhou Xin-an1* 1

Key Laboratory of Oil Crop Biology, Ministry of Agriculture, Oil Crops Research Institute, CAAS, Wuhan 430062, China

2

Key Laboratory of Soybean Biology, Ministry of Education, Soybean Research Institute, Northeast Agricultural University, Harbin 150030, China

Abstract: Drought is one of the most important environmental constraints limiting plant growth, development and crop yield. Many drought-inducible genes have been identified by molecular and genomic analyses in Arabidopsis, rice and other crops. To better understand reaction mechanism of plant to drought tolerance, we mainly focused on introducing the research of transcription factors (TFs) in signal transduction and regulatory network of gene expression conferring drought. A TF could bind multiple target genes to increase one or more kinds of stress tolerance. Sometimes, several TFs might act together with a target gene. So drought-tolerance genes or TFs might respond to high-salinity, cold or other stresses. The crosstalk of multiple stresses signal pathways is a crucial aspect of understanding stress signaling. Key words: drought stress, stress tolerance, transcription factor, gene expression, signal pathway CLC number: S332.4; Q943.2

Document code: A

Article ID: 1006-8104(2012)-03-0001-13

involve in different signal pathways. But they are

Introduction

not totally isolated. The crosstalk of multiple stress

Transcription factors (TFs), which are known as

show differential transcript regulations in response to

trans-acting elements, can bind to cis-acting elements

different stresses (Table 2).

located in the promoter of stress-inducible genes,

　Plants have adapted to respond to various environ-

and regulate their expressions. Stress-inducible gene

ment stresses, such as drought, high-salinity, ex-

expressions are regulated by some signal pathways,

treme temperature etc., through a series of stress

such as AREB/ABF, DREB, NAC, MYB/ MYC,

stimuli, signal perception, signal transduction, stress-

WRKY, NFYA, HD-ZIP etc (Table 1). AREB/ABF is

responsive gene expression, appropriate morpho-

ABA-dependent , DREB is ABA-independent, while

logical and physiological, molecular and cellular

NAC, MYB/MYC, WRKY, NFYA, and HD-ZIP

level changes occurred in plants, they protect them-

families include several subfamilies, in which some

self from the damage of biotic and abiotic stresses.

are ABA-dependent, the other are ABA- independent,

TFs play an important role in signal transduction.

even different members in the same subfamily

(Fig. 1).

signal pathways puts these TFs together. These TFs

Received 9 June 2011 Supported by Cultivation of New Varieties of Genetically Modified Major Projects (2011ZX08004-005); Soybean Industry Technology System (CARS-04-PS08) Chen Li-miao (1983-), female, assistant researcher, engaged in the research of soybean molecular cloning and genetic transformation. E-mail: [email protected] * Corresponding author. Zhou Xin-an, researcher, supervisor of Ph. D candidate, engaged in the research of soybean genetics and breeding. E-mail: [email protected] http: //publish.neau.edu.cn

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Journal of Northeast Agricultural University (English Edition)

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Table 1　Sorts of transcription factors in different families Stress-responsive TFs

TFs families

Binding to cis-elements

Core sequence of cis-elements

DREB/CBF

AP2/EREBP

DRE/CRT

CCGAC

AREB/ABF

bZIP

ABRE

CACGTG (G box) CACGTC (C box) TACGTA (A box) MYB/MYC

MYB/MYC

MYBRS/MYCRS

TAACTG

NAC

NAC

NACRS

CATGTG

WRKY

WRKY

WRKYRS

TTGAC (W-BOX)

NF-YA/NF-YB

NF-Y

NF-YRS

CCAAT CAAT (A/T) AT

HD-ZIP

HB

HDERS

TG (HDE1) CAAT (G/C) AT TG (HDE2)

Table 2　Abiotic stress tolerance of transgenic plant over-expressing transcription factors in different species

Gene

Responsive to ABA

Increased tolerance to

Source species

Reference

AREB1

Yes

Drought

Arabidopsis

Furihata et al., 2006

AREB2

Yes

Drought

Arabidopsis

Furihata et al., 2006

ABF3

Yes

Drought

Arabidopsis

Furihata et al., 2006

ABP9

Yes

Drought, heat shock

Arabidopsis

Zhang et al., 2008

OsbZIP23

Yes

Drought, high-salinity

Rice

Xiang et al., 2008

OsbZIP72

Yes

Drought

Rice

Lu et al., 2009

SlAREB

Yes

Drought, salt

Tomato

Hsieh et al., 2010

DREB1A

No

Cold

Arabidopsis

Liu et al., 1998

DREB1B

No

Cold

Arabidopsis

Liu et al., 1998

DREB/

DREB1C

No

Cold

Arabidopsis

Liu et al., 1998

CBF

DREB1D/CBF4

No

Drought (low)

Arabidopsis

Haake et al., 2002

DREB2A

No

Drought, high-salinity

Arabidopsis

Nakashima et al., 2000

DREB2B

No

Drought, high-salinity

Arabidopsis

Nakashima et al., 2000

ANAC019

Yes

Drought, high-salinity

Arabidopsis

Tran et al., 2004

ANAC055

Yes

Drought, high-salinity

Arabidopsis

Tran et al., 2004

ANAC72

Yes

Drought, high-salinity

Arabidopsis

Tran et al., 2004

ANAC092

–

Salt

Arabidopsis

Balazadeh et al., 2010

ANAC102

–

Low-oxygen

Arabidopsis

Christianson et al., 2009

ATAF1

Yes

Drought

Arabidopsis

Lu et al., 2007

SNAC1

Yes

Drought

Rice

Hu et al., 2006

OsNAC52

Yes

Drought

Rice

Gao et al., 2010

OsNAC6

Yes

Drought, high-salinity, cold

Rice

Nakashima et al., 2007

ONAC045

Yes

Drought, high-salinity

Rice

Zheng et al., 2009

OsNAC10

Yes

Drought

Rice

Jeong et al., 2010

AtMYB2

Yes

Drought

Arabidopsis

Abe et al., 2003

MYB96

Yes

Drought

Arabidopsis

Seo et al., 2009

OsMYB3R-2

–

Drought, high-salinity, cold

Rice

Dai et al., 2007

StMYB1R-1

–

Drought

Potato

Shin et al., 2011

Family

bZIP

NAC

MYB

E-mail: [email protected]

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Chen Li-miao et al. Regulatory Network of Transcription Factors in Response to Drought in Arabidopsis and Crops

Continued

Family

Gene

Responsive to ABA

Increased tolerance to

Source species

Reference

ABO3 OsWRKY45

Yes

Drought

Arabidopsis

Ren et al., 2010

Yes

Drought, high-salinity,

Rice

Qiu et al., 2009

0℃ and 42℃ WRKY

NF-Y

HD-ZIP

OsWRKY11

–

Drought, heat shock

Rice

Wu et al., 2009

GmWRKY21

–

Cold

Soybean

Zhou et al., 2008

GmWRKY54

–

Drought, salt

Soybean

Zhou et al., 2008

HvWRKY38

–

Drought

barley

AtNF-YB1

No

Drought

Arabidopsis

Xiong et al., 2010 Nelson et al., 2007

ZmNF-YB2

–

Drought

Maize

Nelson et al., 2007

NFYA5

Yes

Drought

Arabidopsis

Li et al., 2008

ATHB6

Yes

Drought

Arabidopsis

Söderman et al., 1999 Tran et al., 2006

ZFHD1

Yes

Drought, high-salinity

Arabidopsis

HDG11

–

Drought

Arabidopsis

Yu et al., 2008

CpHB-7

Yes

Drought

Craterostigma

Deng et al., 2006

Hahb-4

Yes

Drought

Brassica napus L

Dezar et al., 2005

NaHD20

Yes

Drought

Nicotiana attenuata

Re et al., 2011

plantagineum

Signal reception

Signal transduction pathway Transcription factors Auxin-dependent ABA-dependent

Biotic stress and wounding

Jasmonic aciddefense response

MYB96 (MYB) AtMYB2/AtMYC2 (MYB/MYC) NAC (RD26) AREB/ABF (bZIP) SIAREB (bZIP) AB3 (WRKY)

Drought stress High salinity stress

Regulatory gene expression GH3 RD22

Gly SnRK2 RD29A, COR47

WRKY18+ WRKY40– (WRKY) (WRKY) NFYA5 miR169 (NF-Y) ATHB6+ ATHB7– ATHB12– (HD-ZIPI) (HD-ZIPI) (HD-ZIPI) HDG11 NAC ZFHD1

WRKY60+ (WRKY)

ABI1, ABI2

NCED3, LOS5/ABA3, CIPK3, CAX3, ABI3 ERD1

AtNF-YB1 (NF-Y) ABA-independent Cold stress

DREB2 (AP2/EREBP) DREB1 (AP2/EREBP)

RD29A

Fig. 1　Transcriptional regulatory networks of TFs involved in abiotic stress-responsive gene expressions http: //publish.neau.edu.cn

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Journal of Northeast Agricultural University (English Edition)

Vol. 19 No. 3 2012

drought and other stress in crop plants. Expression of

Study of Drought-inducible Genes in Arabidopsis

OsbZIP23 could be induced by most stresses, such as

Microarray analyses in Arabidopsis identify the pro-

yeast suggested that OsbZIP23 was a transcriptional

ducts of the drought-inducible genes, which are

activator. Transient expression in onion cells reveal-

divided into two types (Shinozaki et al., 2003). One

ed OsbZIP23 protein located in nucleus. Over-ex-

is functional protein, such as water channel, deto-

pressing OsbZIP23 in rice significantly improved to-

xification enzyme, late embryogenesis abundant

lerance to drought and high-salinity stresses and sen-

(LEA) protein, key enzyme for osmolyte biosynthesis

sitivity to ABA. On the contrary, a null mutant of this

(praline, sugar), and protease. Another is regulatory

gene showed significantly decreased sensitivity to a

protein, including transcription factor, protein kinase,

high concentration of ABA and decreased tolerance to

phospholipid metabolism, ABA biosynthesis and so

drought stress and high-salinity, and this phenotype

on. In which, transcription factors play an important

could be complemented by transforming the OsbZIP23

role in regulating drought-inducible gene expression.

back into the mutant. These demonstrated adequately

drought, salt, abscisic acid (ABA), and polyethylene glycol (PEG) treatments. Trans-activation assay in

that OsbZIP23 was an important regulator in ABAAREB/ABFs regulated pathway

dependent drought and high-salinity signal pathway

Some TFs, such as basic leucine zippers (bZIPs),

(Xiang et al., 2008). OsbZIP72 was another positive

regulate stress-responsive gene expressions through

transcription factor. It not only showed a hypersensiti-

ABA signal pathway. There are some cis-elements,

vity to ABA and a higher ability of drought tolerance,

termed Abscisic Acid-Responsive Element Binding

but also activated expression of ABA response genes,

Proteins (ABREs), binding to bZIP-type AREB/ABFs

such as LEAs (Lu et al., 2009). The rice bZIP TF OsABI5

in the promoter of ABA-regulated genes. AREB1,

was also isolated from rice panicles. Expression of

AREB2, and ABF3 in the AREB/ABFs subfamily need

OsABI5 was induced by ABA and high salinity, but

to be activated by ABA and can be induced under

was down-regulated by drought and cold (4℃) stress

drought. These three transcription factors could form

in seedlings. Over-expression of OsABI5 in rice con-

dimers in nucleus, and could interact with an SNF1-

ferred high sensitivity to salt stress. In contrast, down-

related protein kinase 2 (SnRK2) protein kinase de-

regulation of OsABI5 improved stress tolerance, but

signated SRK2D/SnRK2.2, which phosphorylated

decreased fertility of rice. These results demonstrated

the AREB1 polypeptide (Furihata et al., 2006).

that OsABI5 might regulate stress response and plant

To further study AREB1, AREB2, and ABF3

fertility (Zou et al., 2008). In addition, a tomato

function, an areb1 areb2 abf3 triple mutant was

bZIP transcription factor, SlAREB in Arabidopsis

constructed. The mutant was less sensitive to ABA

thaliana and tomato plants regulated stress-related

and had weaker drought tolerance. Therefore, AREB1,

genes including AtRD29A, AtCOR47, and SlCI7-like

AREB2, and ABF3 as transcription factors, collabora-

dehydrin under ABA and abiotic stress treatments.

tively regulated ABA-signaling gene expression under

Taken together, these results showed that SlAREB

drought (Yoshida et al., 2010). In Arabidopsis, a bZIP

might regulate some stress-responsive genes and that

transcription factor, ABP9 (ABA-responsive-element

its over-production improved plant tolerance to water

(ABRE) binding protein 9) constitutive expression

deficit and salt stress (Hsieh et al., 2010).

could improve the photo-synthetic capacity of plants under stress, including drought and heat shock (Zhang

DREBs regulated pathway

et al., 2008). There are some bZIP TFs responding to

Other TFs are in response to drought stress, but no

E-mail: [email protected]

Chen Li-miao et al. Regulatory Network of Transcription Factors in Response to Drought in Arabidopsis and Crops

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respond to ABA, such as DREBs. The dehydration

NAC recognition sequence (NACRS), by analyzing

responsive element binding proteins (DREBs) are

the promoter of the drought inducible EARLY

important transcription factors that regulate the abiotic

RESPONSE TO DEHYDRATION1 (ERD1) gene.

stress-related genes and further improve stress tole-

The expression of ERD1 under drought depended on

rance to plants. DREBs were divided into DREB1/CBF

both the "CACTAAATTGTCAC" ZFHDRS and the

and DREB2 (Yamaguchi-Shinozaki and Shinozaki,

"ANNNNNTCNNNNNNNACACGCATGT" NACRS

2005) which responsed to different stress signals as

sequences (Simpson et al., 2003). They both acted as

cold and drought. They both belong to the EREBP

transcription activators in response to drought stress.

family of transcription factors, and bind to DRE (dehy-

In Arabidopsis, some NAC TFs could be induced

dration-responsive element)/CRT (C-RepeaT), both

by drought, high-salinity, low temperature or other

of which were cis-acting elements in the promoters of

stress. It was reported that ANAC019, ANAC055 or

stress-inducible genes (Yamaguchi-Shinozaki and

ANAC72 over-expression could improve some stress-

Shinozaki, 1994). Their conserved DNA-binding

inducible genes up-regulated and increase drought

motifs were CCGAC. The Arabidopsis genome con-

tolerance in transgenic plants (Fujita et al., 2004;

tained six DREB1/CBF genes and eight DREB2

Tran et al., 2004). They also regulated jasmonic acid-

genes (Sakuma et al., 2002). DREB1A, DREB1B, and

signaled defense response (Ooka et al., 2003; Bu et

DREB1C were strongly induced by cold, but not by

al., 2008). RD26 gene encoding a NAC transcription

drought and high-salinity stress (Liu et al., 1998).

factor was responsive not only to dehydration, but

However, DREB2A and DREB2B genes were on the

also to NaCl, ABA and jasmonic acid treatments. The

contrary (Nakashima et al., 2000). Other DREB1 and

transgenic plants over-expressing RD26 cDNA were

DREB2 genes were weakly induced (Sakuma et al.,

hypersensitive to ABA, and inversely, the transgenic

2002), and some DREB1/CBF genes as DREB1D/

plants with RD26 repressed were insensitive to ABA.

CBF4 also expressed low under drought stress, indicat-

The expressions of many ABA- and stress-induced

ing crosstalk between the DREB1/CBF and the DREB2

genes including RD20 and GLY genes were up-re-

pathways under drought stresses (Haake et al., 2002;

gulated in plants over-expressing RD26 and repressed

Magome et al., 2004). DREB1/CBF and DREB2-

in plants with RD26 repressed. In Arabidopsis proto-

homologous genes were identified in rice, named 10

plasts, RD26 activated a promoter of the GLY gene

OsDREB1s and four OsDREB2s, respectively. They

that was up-regulated in plants over-expressing RD26.

had a similar function with these in Arabidopsis to

Thus, GLY was the target gene of RD26. These results

abiotic stress.

demonstrated that RD26, as a transcription activator, involved in stress-responsive ABA-dependent signal

NAC regulated pathway

transduction pathway (Fujita et al., 2004). ANAC092/

NAC (NAM, ATAF and CUC) transcription factors

AtNAC2/ORE1 was found to act during senescence

(TFs), which are one kind of plant-specific TFs

and respond to salt stress (Balazadeh et al., 2010).

families, have been reported to enhance different

ANAC102 was reported to be induced by low-oxygen

stress tolerance such as drought, high salinity and

stress, and decreasing ANAC102 expression would

cold. Many NAC TFs have been identified in model

reduce seed germination efficiency under a 0.1%

Arabidopsis and crops. More than 105 putative NAC

oxygen treatment, but increasing expression had no

TFs existed in Arabidopsis, 140 in rice (Ooka et al.,

effect on seed germination. Indicating ANAC102

2003), 101 in soybean (Pinheiro et al., 2009) and

as an important regulator of seed germination under

152 in tobacco (Rushton et al., 2008), respectively.

waterlogging (Christianson et al., 2009). ATAF1/

The core motif CACG was identified, which was

ATAF2 both negatively regulated stress-responsive http: //publish.neau.edu.cn

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Journal of Northeast Agricultural University (English Edition)

Vol. 19 No. 3 2012

gene expressions, the difference was that ATAF1 was

and salinity, but had not different effects on low

strongly induced by dehydration and abscisic acid

temperature. The transient expression of GmNAC1,

(ABA) treatment, indicating it regulated drought-

GmNAC5 and GmNAC6 in tobacco leaves promoted

responsive pathway (Lu et al., 2007), ATAF2 re-

senescence and further resulted in cell death. The

pressed the expression of pathogenesis-related genes

function and participating in stress-responsive

in Arabidopsis (Delessert et al., 2005). In rice, there

pathways NAC TFs in soybean would be further

are also some NAC TFs involving in drought, high-

studied.

salinity, low temperature etc. stress. SNAC1 (STRESSRESPON- SIVE NAC 1) over-expression significantly

MYB regulated pathway

increased drought tolerance in transgenic rice, whose

The MYB family is a large family and exists in all

seed setting was 22%-34% higher than that of control

eukaryotes. MYB proteins are main regulators in

during drought stress. The transgenic rice was more

plant development, metabolism and response to biotic

sensitive to ABA treatment and losed water more

and abiotic stresses. AtMYB2 and AtMYC2 both

slowly than WT by closing more stomatal pores, yet

bound cis-elements in the RD22 promoter and co-

showed no significant difference in the rate of photo-

operatively activated the RD22. Microarray analysis

synthesis. Therefore, the yield had not been affected

suggested that target genes of MYC/MYB over-

(Hu et al., 2006). OsNAC52, a rice NAC transcription

expression in transgenic plants might be alcohol

factor, could respond to ABA. OsNAC52 over-expre-

dehydrogenase and ABA-or jasmonic acid (JA)-

ssion activated the expression of downstream genes

inducible genes (Abe et al., 2003). Over-expression

in transgenic Arabidopsis and enhanced tolerance to

of AtMYB2 and AtMYC2 showed hypersensitivity

drought stresses but not growth retardation (Gao et al.,

to ABA and improved drought tolerance of the

2010). Similarly, a rice NAC gene, ONAC045, was

transgenic plants. A R2R3-type MYB transcription

also induced by drought, high salt, and low tempera-

factor, MYB96, regulated drought stress response

ture stress and ABA treatment in leaves and roots.

by integrating ABA and auxin signals. The MYB96-

Over-expressing ONAC045 in rice enhanced tolerance

mediated ABA signals were integrated into an auxin

to drought and salt treatments (Zheng et al., 2009).

signaling pathway that involved a subset of GH3

OsNAC10 expressed in roots significantly, and be

genes encoding auxin-conjugating enzymes. MYB96

induced by drought, high salinity, and ABA. In

over-expression in Arabidopsis exhibited enhanced

transgenic rice, OsNAC10 over-expression increased

drought resistance with reduced lateral roots. On the

drought tolerance. Under the control of root-specific

other hand, a T-DNA insertional knockout mutant was

promoter RCc3, root diameter of OsNAC10 plants

more susceptible to drought. Taken together, MYB96

was thicker by 1.25-fold than that of the constitutive

was a molecular link that mediated ABA-auxin cross

promoter GOS2 and non-transgenic plants grain

talk in drought stress response and lateral root growth

yield added by 17% in drought stress condition, 9%

(Seo et al., 2009). By a cDNA microarray approach

in normal condition (Jeong et al., 2010). In soybean,

to monitor the expression profile of rice under cold

101 NAC domain-containing proteins were divided

stress, OsMYB3R-2 was identified. Unlike most plant

into 15 different subgroups, in which six previously

R2R3 MYB transcription factors, OsMYB3R-2 has

described GmNAC proteins (GmNAC1 to GmNAC6)

three imperfect repeats in the DNA-binding domain.

were located in the nucleus and responded to

Expression of OsMYB3R- 2 was induced by cold,

various stress. GmNAC 2-5 acted as transactivators.

drought, and salt stress. Over-expressing OsMYB3R-2

GmNAC2-4 were significantly induced by osmotic

in Arabidopsis showed increased tolerance to cold,

stress. GmNAC3-4 were also induced by ABA, JA

drought, and salt stress (Dai et al., 2007). A putative

E-mail: [email protected]

Chen Li-miao et al. Regulatory Network of Transcription Factors in Response to Drought in Arabidopsis and Crops

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R1-type MYB-like transcription factor, StMYB1R-1,

that regulated gene expression in both plant defense

was also isolated as a putative stress-response gene

and stress responses by acting as either transcription

using reverse northern-blot analysis under abiotic

activator or repressor (Chen et al., 2010). The ABO3, a

environmental stress conditions. StMYB1R-1 located

WRKY transcription factor, regulated plant responses

to the nucleus and bound to the DNA sequence

to abscisic acid and drought tolerance in Arabidopsis.

/AGATAA. StMYB1R-1 over-expression in potato

The ABA sensitive mutant, abo3, was hypersensitive

plants improved plant tolerance to drought stress while

to ABA in both seedling establishment and seedling

having no significant effects on other agricultural

growth. However, stomatal closure was less sensitive

traits. In addition, over-expression of StMYB1R-1

to ABA, and the abo3 mutant was less drought tolerant

enhanced the expression of drought-regulated genes

than the wild type. Northern blot analysis showed that

such as AtHB-7, RD28, ALDH22a1, and ERD1-like.

the expression of the ABA-responsive transcription

These results demonstrated that StMYB1R-1 functions

factor ABF2/AREB1 was markedly lower in the

as a transcription factor involved in the activation of

abo3 mutant than in the wild type. The abo3 mutation

drought-related genes (Shin et al., 2011).

also reduced the expression of stress-inducible genes RD29A and COR47, especially early during the ABA

WRKY regulated pathway

treatment. The ABO3 was able to bind the W-box in

Like MYB family, the WRKY gene family also

the promoter of ABF2 in vitro. These results indicated

encoded a large group of TFs. Proteins of this family

that ABO3 played an important role as a WRKY

contained one or two highly conserved WRKY

transcription factor in plant responses to ABA and

domains and a zinc finger motif in the C-terminal

drought stress (Ren et al., 2010). In addition, the

region (Eulgem et al., 2000). The WRKY domain

expression of OsWRKY45 found in rice markedly

bound to the W box or SURE (sugar-responsive cis-

induced by abscisic acid (ABA) and various stress

element) found in promoters of target genes and

factors in Arabidopsis, including NaCl, PEG, mannitol

regulated its transcription (Rushton et al., 1995;

or dehydration, treatment with 0℃ and 42℃ as well as

Sun et al., 2003). WRKY transcription factors were

infection by Pyricularia oryzae Cav. and Xanthomonas

involved in plant responses to both biotic and abiotic

oryzae pv. oryzae. Together, these results indicated

stresses such as WRKY18, WRKY40, and WRKY60.

that the OsWRKY45 may be involved in the signal

WRKY18 and WRKY60 had a positive effect on plant

pathways of both biotic and abiotic stress responses

ABA sensitivity for inhibition of seed germination

(Qiu and Yu, 2009). Besides, in other plants, including

and root growth. And the two WRKY genes also

soybean and barely, there were also some WRKY TFs

enhanced plant sensitivity to salt and drought stress.

responding to drought and other stresses. Soybean

In contrast, WRKY40 repressed WRKY18 and

WRKY-type transcription factor, GmWRKY13,

WRKY60 in the effect on plant sensitivity to ABA

GmWRKY21, and GmWRKY54, conferred differential

and abiotic stress in germination and growth. Both

tolerance to abiotic stresses in transgenic Arabidopsis

WRKY18 and WRKY40 were rapidly induced by

plants. GmWRKY21-transgenic Arabidopsis plants

ABA, while induction of WRKY60 by ABA was

were tolerant to cold stress, whereas GmWRKY54

delayed. ABA-inducible expression of was almost

conferred salt and drought tolerance, possibly through

completely abolished in the WRKY18 and WRKY40

the regulation of DREB2A and STZ/Zat10. Transgenic

mutants. Thus, WRKY60 might be a direct target gene

plants over-expressing GmWRKY13 showed

of WRKY18 and WRKY40 in ABA signaling. Taken

increased sensitivity to salt and mannitol stress, but

together, these three related WRKY transcription

decreased sensitivity to ABA, when compared with

factors formed a highly interacting regulatory network

wild-type plants. In addition, GmWRKY13-transgenic http: //publish.neau.edu.cn

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Journal of Northeast Agricultural University (English Edition)

Vol. 19 No. 3 2012

plants showed an increase in lateral roots. These

vascular tissues and guard cells, and NFYA5 contained

results indicated that these three GmWRKY genes

a target site for miR169, which was down-regulated

played differential roles in abiotic stress tolerance

by drought stress also by an ABA-dependent pathway.

(Zhou et al., 2008). Constitutive expression of the

Analysis of the expression of miR169 precursors

barley HvWRKY38 transcription factor also enhanced

showed that miR169a and miR169c were substantially

drought tolerance in turf and forage grass (Paspalum

down-regulated by drought stress. Co-expression of

notatum Flugge). Transgenic plants retained water

miR169 and NFYA5 suggested that miR169a was

better during dehydration, recovered faster and

more efficient than miR169c at repressing the NFYA5

produced more biomass following rehydration and

mRNA level. nfya5 knockout plants and plants over-

survived severe dehydration stress under controlled

expressing miR169a showed enhanced leaf water

environment conditions in contrast to non-transgenic

loss and were more sensitive to drought stress than

plants. They indicated that HvWRKY38 played the

wild-type plants. By contrast, transgenic Arabidopsis

regulatory role in dehydration tolerance (Xiong et al.,

plants over-expressing NFYA5 displayed reduced

2010).

leaf water loss and were more resistant to drought stress than the wild type. Microarray analysis indicated

NF-Y regulated pathway

that NFYA5 was an important regulator for the

NF-Y transcription factors existd ubiquitous in all

expression of a number of drought stress-responsive

eukaryotes and have roles in the regulation of various

genes. Therefore, NFYA5 was crucial for drought

genes (McNabb et al., 1995; Edwards et al., 1998;

tolerance, and its induction by drought stress occurred

Maity and Crombrugghe, 1998; Mantovani, 1999).

at both the transcriptional and posttranscriptional

The NF-Y transcription factor complex was composed

levels.

of three unique subunits: NF-YA, NF-YB, and NFYC. The subunits NF-YB and NF-YC formed a

HD-Zip regulated pathway

heterodimer in the cytoplasm, and then translocated

The HD-Zip (Homeodomain-Leucine Zipper)

to the nucleus, where they combined with the third

family of transcription factors is unique to the plant

subunit, NF-YA, heterotrimeric NF-Y transcription

kingdom. They are made up of four subfamilies in

factor (Frontini et al., 2004; Kahle et al., 2005). NF-Y

Arabidopsis, including HD-ZipⅠ, Ⅱ, Ⅲ, and Ⅳ.

transcription factor combined to CCAAT box, the

Some HD-Zip proteins participate in plant growth

core sequence in the promoter of regulative genes.

and development, while, others involve the action

Plant NF-Y TFs function appears to be important

of hormones or are apt to respond to environmental

for responses to drought stress. Although a specific

stress. Here, we mainly reviewed recent studies for

mechanism remains unknown. Over-expression of

transcription factors of this family playing crucial

AtNF-YB1 and its ortholog in maize (Zea mays),

role in environment stress, especially in drought.

ZmNF-YB2 improved drought tolerance (Nelson and

In 1999, ATHB6 (HD-ZipⅠ) was reported to be

Repetti, 2007). However, no loss-of-function data were

induced by water deficit, osmotic stress or exogenous

provided to study and indicated the function of drought

treatment with abscisic acid (ABA), and the ATHB6

in Arabidopsis. On the other hand, a publication

induction was impaired in the two ABA-insensitive

provided both over-expression and loss-of-function

mutants, abi1 and abi2. It demonstrated that ATHB6

data for NFYA5 (Li et al., 2008). The Arabidopsis

might act downstream to both ABI1 and ABI2 in

thaliana NFYA5 transcript was strongly induced by

a signal transduction pathway mediating a drought

drought stress in an abscisic acid (ABA)-dependent

stress response (Söderman et al., 1999). In contrast,

signal pathway. NFYA5 was highly expressed in

the Arabidopsis thaliana homeodomain leucine-

E-mail: [email protected]

·9·

Chen Li-miao et al. Regulatory Network of Transcription Factors in Response to Drought in Arabidopsis and Crops

zipper gene ATHB7 and ATHB12 (HD-ZipⅠ) acted

dehydration responsive dehydrin gene. CpHB-7

to mediate a response to water deficit as a negative

over-expression in transgenic desiccation-tolerant

regulator of growth (Söderman et al., 1996; Hjellstrom

plant Craterostigma plantagineum reduced sensitivity

et al., 2003; Olsson et al., 2004). The dehydration-

towards ABA during seed germination and stomatal

inducible expression of the Arabidopsis thaliana

closure. CpHB-7 regulated ABA-responsive gene

EARLY RESP O N S I V E T O D E H Y D R A T I O N

expression as a negative regulator, which was func-

STRESS 1 (ERD1) gene depended on the action

tionally similar to the Arabidopsis transcription factor,

together of zinc finger homeodomain ZFHD1 and

ATHB-6 (Deng et al., 2006). Brassica napus L. Hom-

NAC transcription factors. Using the yeast one-hybrid

eodomain Leucine-Zipper Gene BnHB6 was reported

system, ZFHD1 transcriptional activator was isolated.

to be induced by several stress and phytohormones

The expression of ZFHD1 was induced by drought,

including mannitol, NaCl, cold treatment, anaerobic

high salinity and abscisic acid. The DNA-binding

culture, wounding, H2O2, abscisic acid (ABA), and

and activation domains of ZFHD1 were localized on

salicylic acid (SA) treatments, but not by ultraviolet

the C-terminal homeodomain and N-terminal zinc

treatment (Yu et al., 2005). Hahb-4, a sunflower

finger domain, respectively. Microarray analysis of

homeobox-leucine zipper gene, can be induced by

transgenic plants over-expressing ZFHD1 revealed

drought and ABA. Its over-expression also increased

that several stress-inducible genes were up-regulated

drought tolerance. It showed that it might participate

in the transgenic plants. Using the yeast two-hybrid

in the regulation of the expression of genes involved

system, both ZFHD1 and NAC proteins were detected.

in developmental responses of plants to desiccation

Moreover, co-overexpression of the ZFHD1 and NAC

(Dezar et al., 2005). Besides, the TF was a new

genes restored the morphological phenotype of the

component of ethylene signaling pathways, and that

transgenic plants to a near wild-type state and increase

it induced a marked delay in senescence. Plants over-

expression of ERD1 in transgenic Arabidopsis

expressing Hahb-4 were less sensitive to external

plants (Tran et al., 2006). Activated expression of

ethylene, entered the senescence pathway later.

an Arabidopsis HD-START Protein, HDG11(HD-

Expression of this TF had a major repressive effect

Zip Ⅳ) enhanced drought tolerance with improved

on genes related to ethylene synthesis, such as the

root system and reduced stomatal density (Yu et al.,

ACO and the SAM, and on genes related to ethylene

2008). And HDG11 over-expression in transgenic

signaling, such as ERF2 and ERF5. Taken together,

Arabidopsis, tobacco and tall fescue all increased

we proposed that Hahb-4 was involved in a novel

drought tolerance (Yu et al., 2008; Cao et al., 2009).

conserved mechanism related to ethylene-mediated

HIPP26 from Arabidopsis thaliana belonged to the

senescence that improved desiccation tolerance

HIPP family of plant proteins, characterized by a

(Manavella et al., 2006). Nicotiana attenuata NaHD20

heavy metal associated domain and an additional

enhanced leaf ABA accumulation during water stress,

isoprenylation motif. It was induced during cold, salt

and NaHD20 played a positive role in the expression

and drought stress. By a yeast-two-hybrid approach,

of some dehydration-responsive genes including ABA

a strong interaction of HIPP26 with the zinc finger

biosynthetic genes (Re et al., 2011).

homeodomain transcription factor ATHB29 existed, which was known to play a role in dehydration stress response could be detected (Barth et al., 2009). A dehydration responsive nuclear-targeted HD-ZIP

Crosstalk of Stress-responsive Gene Regulatory Network

transcriptional regulator, CpHB-7 could combine

The crosstalk exists not only in different regulatory

with its target gene CDeT6-19, a known ABA and

systems, such as ABA-dependent or not, but also in http: //publish.neau.edu.cn

·10·

Journal of Northeast Agricultural University (English Edition)

Vol. 19 No. 3 2012

different stresses-responsive gene expressions. Most drought-inducible genes are also induced by high-

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