Open access

Role of Plant Transcription Factors in Abiotic Stress Tolerance

Written By

Charu Lata, Amita Yadav and Manoj Prasad

Submitted: November 24th, 2010 Published: August 29th, 2011

DOI: 10.5772/23172

Chapter metrics overview

8,924 Chapter Downloads

View Full Metrics

1. Introduction

Plants are constantly exposed to a wide range of environmental stresses such as drought, high salt, heat and extremes of temperature. Growth constraints due to these abiotic stresses result in reduced productivity and significant crop losses globally. Drought and salinity affect more than 10% of arable land, which results in more than 50% decline in the average yields of important crops worldwide (Bray et al., 2000). Tolerance or susceptibility to these stresses is also a very intricate event as stress may affect multiple stages of plant development and often several stresses concurrently affect the plants (Chinnusamy et al., 2004). Therefore, the basic mechanisms of abiotic stress tolerance and adaptation have been the area of comprehensive research.

Plants counter adverse environmental conditions in a complex, integrated way depending on the timing and length that allows them to respond and adapt to the existing constraints present at a given time. Plant stress tolerance involves changes at whole-plant, tissue, cellular, physiological and molecular levels. Exhibition of a distinct or a combination of intrinsic changes ascertains the capacity of a plant to sustain itself under unfavorable environmental conditions (Farooq et al., 2009). This comprises a range of physiological and biochemical adjustments in plants including leaf wilting, leaf area reduction, leaf abscission, root growth stimulation, alterations in relative water content (RWC), electrolytic leakage (EL), production of reactive oxygen species (ROS) and accumulation of free radicals which disturb cellular homeostasis ensuing lipid peroxidation, membrane damage, and inactivation of enzymes thus influencing cell viability (Bartels and Sunkar, 2005). Other than these, abscissa acid (ABA), a plant stress hormone, induces leaf stomata closure, thus reducing transpirational water loss and photosynthetic rate which improves the water-use efficiency (WUE) of the plant. Molecular responses to abiotic stress on the other hand include perception, signal transduction, gene expression and ultimately metabolic changes in the plant thus providing stress tolerance (Agarwal et al., 2006).

Several genes are activated in response to abiotic stresses at the transcriptional level, and their products are contemplated to provide stress tolerance by the production of vital metabolic proteins and also in regulating the downstream genes (Kavar et al., 2007). Transcript profiling can be a significant tool for the characterization of stress-responsive genes. Extensive transcriptome analyses have divulged that these gene products can largely be classified into two groups (Bohnert et al., 2001; Seki et al., 2002; Fowler and Thomashow, 2002). First group comprises of genes that encode for proteins that defend the cells from the effects of water-deficit. These genes mainly include those that regulate the accumulation of compatible solutes (enzymes for osmolyte biosynthesis like proline, betaine, sugars, etc.); passive and active transport systems across membranes (water channel proteins and membrane transporters); and protection and stabilization of cell structures from damage by ROS (the detoxification enzymes such as glutathione S-transferase, catalase, superoxide dismutase, ascorbate peroxidase, etc.); fatty acid metabolism enzymes, proteinase inhibitors, ferritin and lipid-transfer proteins; and other proteins for the protection of macromolecules (LEA protein, osmotin, chaperons, etc.). Another group of genes stimulated by abiotic stresses includes regulatory proteins that further regulate the stress signal transduction and alter gene expression and hence possibly function in stress response. They comprise several transcription factors (TFs) emphasizing the role of various transcriptional regulatory mechanisms in the stress signal transduction pathways; protein kinases (MAP kinase, CDP kinase, receptor protein kinase, etc.); protein phosphatases and proteinases implicated in the regulation of stress signaling and gene expression (Seki et al., 2003; Shinozaki and Yamaguchi- Shinozaki, 2007).


2. Role of transcription factors in abiotic stress responses

Transcription factors (TFs) are proteins that act together with other transcriptional regulators, including chromatin remodeling/modifying proteins, to employ or obstruct RNA polymerases to the DNA template (Udvardi et al., 2007). Plant genomes assign approximately 7% of their coding sequence to TFs, which proves the complexity of transcriptional regulation (Udvardi et al., 2007). The TFs interact with cis-elements in the promoter regions of several stress-related genes and thus up-regulate the expression of many downstream genes resulting in imparting abiotic stress tolerance (Agarwal and Jha, 2010). In Arabidopsis thaliana genome about 1500 TFs are described which are considered to be involved in stress responsive gene expression (Riechmann et al., 2000). Transcriptome data in Arabidopsis and in numerous other plants suggest that there are several pathways that independently respond to environmental stresses (in both ABA dependent- and independent- manner), suggesting that stress tolerance or susceptibility is controlled at the transcriptional level by an extremely intricate gene regulatory network. (Fig.1) (Fowler and Thomashow, 2002; Umezawa et al., 2006).

The phytohormone ABA is the central regulator of abiotic stress particularly drought resistance in plants, and coordinates a complex gene regulatory network enabling plants to cope with decreased water availability (Cutler et al., 2010; Kim et al., 2010). ABA-dependent signaling systems have been illustrated as pathways that mediate stress adaptation by induction of atleast two separate regulons (a group of genes controlled by a certain TF): (1) the AREB/ABF (ABA-responsive element-binding protein/ ABA-binding factor) regulon; and (2) the MYC (myelocytomatosis oncogene)/MYB (myeloblastosis oncogene) regulon (Abe et al., 1997; Busk and Pagés, 1998; Saibo et al., 2009). While ABA-independent regulons are: (1) the CBF/DREB regulon; and (2) the NAC (NAM, ATAF and CUC) and ZF-HD (zinc-finger homeodomain) regulon (Nakashima et al. 2009; Saibo et al., 2009). However in addition, several studies have identified the existence of both ABA-dependent and –independent pathways of stress response that function through AP2/EREBP (ERF) family members (Yamaguchi-Shinozaki and Shinozaki, 1994; Kizis and Pagés, 2002). In addition to these well-known regulons, a large number of other TFs are also involved in abiotic stress responses, thereby playing a crucial role in imparting stress endurance to plants. Although

Figure 1.

A schematic representation of transcriptional regulatory networks of cis-acting elements and transcription factors involved in abiotic-stress-responses. Transcription factors are shown in ellipses; cis-acting elements are shown in boxes; and target stress inducible genes are shown in long rectangular box at the bottom.

these different stress responsive TFs usually function independently, it is undoubtedly possible that some level of cross-talk exists between them.

This chapter focuses on these TFs and their role in regulating abiotic stress responses in plants (Table 1) as well as their utility in engineering stress tolerance for crop improvement programs (Table 2).

Table 1.

Response of transcription factors to various stresses.

Table 2.

Stress response of overexpressing transcription factors in transgenic plants.


3. The AREB/ABF regulon

A conserved cis-element named as ABA-responsive element (ABRE; PyACGTGG/TC) was identified from the promoters of ABA-inducible genes (Bray, 1994; Giraudat et al., 1994; Busk and Page`s, 1998). Subsequently it was revealed that ABA-responsive gene expression needs multiple ABREs or the combination of an ABRE with a coupling element (CE) as a functional promoter (Yoshida et al., 2010). For example, ABRE and coupling elements, including coupling element 1 (CE1) and coupling element 3 (CE3), constitute an ABA-responsive complex in the regulation of wheat HVA1 and HVA22 genes (Shen et al., 1996). For the expression of RD29B in seeds and vegetative tissues of Arabidopsis, two ABRE cis-acting elements are required (Uno et al., 2000; Nakashima and Yamaguchi-Shinozaki, 2006).

The AREB or ABFs are bZIP (basic leucine zipper) TFs that bind to the ABRE motif and activate ABA-dependent gene expression were first isolated in a yeast one-hybrid screening (Choi et al., 2000; Uno et al., 2000). It was reported that in the ABA-deficient aba2 and ABA-insensitive abi1 mutants, the AREB/ABF proteins have less activity while they show an enhanced activity in the ABA hypersensitive era1 mutant of Arabidopsis suggesting that these TFs require an ABA-mediated signal for their activation (Uno et al., 2000). The reason possibly may be an ABA-dependent phosphorylation of the AREB/ABF proteins (Shinozaki and Yamaguchi-Shinozaki, 2007). The 75 AtbZIPs have been divided into 11 groups, and the ABFs/AREBs are classified to group A (Jakoby et al., 2002) which usually act in ABA signaling during seed maturation or stress conditions. Several studies have suggested that ABFs function in different stress response pathways; i.e. ABF1 in cold; ABF2 in salt, drought, heat and glucose; ABF3 in salt; ABF4 in cold, salt, and drought signaling pathways (Kim et al., 2004; Fujita et al., 2005). AREB/ABFs are phosphorylated by ABA-responsive 42-kDa kinases which suggest that ABA-dependent phosphorylation may be involved in activation of AREB subfamily proteins (Uno et al., 2000). These kinases (SnRK2-type) such as OST1/SRK2E in Arabidopsis phosphorylate Ser/Thr residues of R-X-X-S/T sites in the conserved regions of AREB1 (Mustilli et al., 2002; Yoshida et al., 2002; Furihata et al., 2006).

AREB/ABF genes are mostly redundant in tissue-specific expression either in vegetative tissues or seeds (Choi et al., 2000; Uno et al., 2000). AREB1/ABF2, AREB2/ABF4, and ABF3 were mainly expressed in vegetative tissues, whereas ABI5 and EEL were expressed during seed maturation and/or germination (Choi et al., 2000; Uno et al., 2000; Bensmihen et al., 2002; Fujita et al., 2005; Nakashima and Yamaguchi-Shinozaki, 2006). Rice homolog TRAB1 and barley homolog HvABI5 activated ABA-responsive gene expression in seeds (Hobo et al., 1999; Casaretto and Ho, 2003). Expression of OsABI5 was stimulated by ABA and high salinity, but was down-regulated by drought and cold stress in seedlings, and its overexpression also improved salinity tolerance in rice (Zou et al., 2008; Nakashima at al., 2009). ZmbZIP17 was up-regulated by drought, heat, ABA and NaCl stress in maize seedlings (Jia et al., 2009).

Overexpression of ABF3 and ABF4 resulted in reduced transpiration and improved drought tolerance (Kang et al., 2002). AREB1/ABF2 was found to be a crucial component of glucose signaling, and its over-expression improved drought stress tolerance (Kim et al., 2004). Overexpressing OsbZIP23, a member of AREB/ABF subfamily can also significantly improve drought and high salinity resistance of transgenic rice at the reproductive stage (Xiang et al., 2008). Enhanced tolerance to drought and heat was also observed in 35S-OsAREB1 transgenic Arabidopsis plants (Jin et al. 2010). The over-expression of the constitutively active form of AREB1 in transgenic Arabidopsis plants showed ABA hypersensitivity and enhanced drought tolerance, and LEA-class genes and ABA- and dehydration-stress-inducible regulatory genes such as linker histone H1 and AAA ATPase were upregulated. Over-expressing SRK2C caused hypersensivity to ABA, improved drought tolerance and lowered transpiration rate (Umezawa et al., 2004). Overexpression of AtbZIP60 led to improved salt tolerance (Fujita et al., 2007).


4. The MYC /MYB regulon

The MYC/MYB families of proteins are universally found in both plants and animals and known to have varied functions. Both MYC/MYB TFs participate in the ABA-dependent pathway of stress signaling for the upregulation of the abiotic stress responsive genes. The first MYB gene identified was the v-MYB gene of avian myeloblastosis virus (AMV) (Klempnauer et al., 1982). The first plant MYB gene, C1, was identified in Zea mays. It encodes a c-MYB-like TF that is involved in anthocyanin biosynthesis (Paz-Ares et al., 1987). Wide existence of MYB genes indicates that these are very ancient evolutionarily. A MYB domain is usually composed of one to three imperfect repeats, each with about 52 amino acid residues that adopt a helix-turn-helix conformation intercalating in the major groove of the DNA (Yanhui et al. 2006). Plant MYB proteins are categorized into three major groups: (i) R2R3-MYB having two adjacent repeats; (ii) R1R2R3-MYB having three adjacent repeats; and (iii) MYB-related proteins, usually containing a single MYB repeat (Rosinski and Atchley, 1998; Jin and Martin, 1999; Stracke et al., 2001). The R2R3 family contains the largest number of MYB genes. Yanhui et al. (2006) have reported that there are 198 and 183 MYB genes in the Arabidopsis and rice genomes, respectively.

MYB TFs play important roles in many physiological processes under normal or unfavorable growth conditions (Jin and Martin, 1999; Chen et al., 2006; Yanhui et al., 2006) and also in secondary metabolism (Paz-Ares et al., 1987), cell morphogenesis (Higginson et al., 2003), meristem formation and floral and seed development (Kirik et al., 1998), cell cycle control (Araki et al., 2004), defense and stress responses (Abe et al., 2003), and hormone signaling (Newman et al., 2004). MYC and MYB TFs accumulate only after ABA accumulation. AtMYB4 (At1g22640), AtMYB6 (At4g09460), AtMYB7 (At2g16720), AtMYB44 (At5g67300), AtMYB73 (At4g37260), AtMYB77 (At3g50060), and AtMYBCDC5 (At1g09770) were found to be constitutively expressed in all organs and during all stress treatments (Yanhui et al., 2006). AtMYB2 and AtMYC2 function cooperatively as transcriptional activators in the dehydration- and ABA-inducible rd22 expression (Urao et al., 1993; Abe et al., 2003). According to Denekamp and Smeekens (2003), AtMYB102 integrates dehydration, osmotic, or salinity stress, ABA application, and wound-signaling pathways. AtMYB60 and AtMYB61are involved in light-induced opening of stomata (Cominelli et al., 2005) and dark-induced closure of stomata, respectively (Liang et al., 2005). AtMYB44, AtMYB73, and AtMYB77 are activated by wounding (Cheong et al., 2002), white-light (Ma et al., 2005), cold stress (Fowler and Thomashow, 2002), and salt stress (Kamei et al., 2005). AtMYB44 and AtMYB77 expression is reduced in fus3 (fusca3), lec1 (leafy cotyledon1), and abi3 (ABA-insensitive3) mutants that are defective in development of dormancy and drought tolerance during late embryogenesis and seed maturation (Kirik et al., 1998). AtMYB44 TF confers abiotic stress tolerance through enhancing stomatal closure in an ABA-independent manner (Jung et al., 2008). Recent studies have shown that AtMYB15 expression is detectable in both vegetative and reproductive organs and is up-regulated by cold and salt stresses (Agarwal et al., 2006). AtMYB15 has been found to negatively regulate freezing tolerance in Arabidopsis with its ability to repress the expression levels of CBF genes (Agarwal et al., 2006). AtMyb41 from Arabidopsis is transcriptionally regulated in response to salinity, drought, cold, and ABA (Lippold et al., 2009). Liao et al. (2008c) identified 156 GmMYB genes of which the expression of 43 genes changed on treatment with ABA, salt, drought and/or cold stress.

Overexpression of MYB15 results in improved drought and salt tolerance in Arabidopsis (Ding et al., 2009). Increased expression levels of AtMYB2, AtMYC2 or both enhance ABA sensitivity and improve osmotic tolerance (Abe et al., 2003). Overexpression of 35S:AtMYC2 and 35S:AtMYB2 and 35S:AtMYC2+AtMYB2 in Arabidopsis induced ABA responsive stress genes and showed an ABA-hypersensitive phenotype with increased osmotic stress tolerance (Abe et al., 2003). Transgenic plants overexpressing AtMyb41 showed dwarf phenotype due to alterations of cell expansion and cuticle integrity and enhanced drought sensitivity (Cominelli et al., 2008). Overexpression of AtMyb75 and AtMyb90 led to increased anthocyanin levels (Borevitz et al., 2000; Xie et al., 2006), while Met-derived glucosinolate content of Arabidopsis increased with overexpression of AtMyb28 (Gigolashvili et al., 2007). In contrast, OsMYB3R-2 transgenic plants showed enhanced tolerance to freezing, drought and salt stress and decreased sensitivity to ABA (Dai et al., 2007). Different level of tolerance was imparted by overexpression of OsMYB4 depending on the nature of the host plants. Arabidopsis transgenic plants overexpressing OsMYB4 showed increased chilling and freezing tolerance with a dwarf phenotype (Vannini et al., 2004), the tomato transgenic showed higher tolerance to drought stress (Vannini et al., 2007), whereas increased drought and cold tolerance was observed in the apple transgenic (Pasquali et al., 2008). Overexpression of a StMYB1R-1 transgene in potato plants improved plant tolerance to drought stress while having no significant effects on other agricultural traits (Shin et al. 2011).


5. The CBF/DREB regulon

The dehydration responsive element binding proteins (DREBs) are important AP2/ERF plant TFs that induce a set of abiotic stress-related genes, thus imparting stress tolerance to plants. These play an important role in the ABA-independent pathways that activates stress responsive genes. The first isolated cDNAs encoding DRE binding proteins, CBF1 (CRT binding factor1), DREB1A and DREB2A were identified through yeast one-hybrid screening from Arabidopsis (Stockinger et al., 1997; Liu et al., 1998). Since then, many DREBs have been isolated from various plants. These proteins specifically bind to and activate the expression of genes regulated by the DRE sequence (5'-TACCGACAT-3') and were first identified in the promoter of the drought-responsive gene rd29A (Yamaguchi-Shinozaki and Shinozaki 1993). DREB1 and DREB2 are two main subgroups of DREB subfamily, involved in two different signal transduction pathways under cold and dehydration respectively. DREB1B/CBF1, DREB1A/CBF3 and DREB1C/CBF2 genes are positioned in consonance on chromosome 4 of Arabidopsis (Gilmour et al., 1998; Liu et al., 1998). Arabidopsis also contains major DREB2 proteins namely, DREB2A and DREB2B (Liu et al., 1998). DREB1/DREB2-homologous genes have also been identified in various cereals and millet crops (Nakashima et al., 2009; Lata et al., 2011).

The DREB TFs contain an extremely conserved AP2/ERF DNA-binding domain throughout plant kingdom. The domain consists of a three-stranded β-sheet and one α -helix running almost parallel to it that contacts DNA via Arg and Trp residues located in the β-sheet (Magnani et al., 2004). Two conserved functional amino acids (valine and glutamic acid) at 14th and 19th residues respectively, exist in the DNA binding domain, which are crucial sites for the binding of DREBs and DRE core sequences (Liu et al., 1998). An alkaline N-terminal amino acid region that serve as a nuclear localization signal (NLS) and a conserved Ser/Thr-rich region responsible for phosphorylation near the AP2/ERF DNA binding domain are also mostly present (Liu et al., 1998; Agarwal et al., 2006).The proteins contain an acidic C-terminal region which might be functional in trans-activation activity (Stockinger et al., 1997).

The activation of these transcripts is organ-specific and comparative to the extent of the stress given. When exposed to salt stress, AhDREB1 was highly expressed in roots but less significantly in stems and leaves (Shen et al., 2003b). It was observed that OsDREB1F was constitutively expressed throughout the plant with highest expression in panicles and callus than in the other tissues (Wang et al., 2008). AtDREB2A accumulated in roots, stems and leaves under control conditions (Liu et al., 1998). DREB2C expressed in mature embryo and the cotyledons of germinating seedlings (Lee et al., 2010). Almoguera et al. (2009) reported that sunflower HaDREB2 expresses in all vegetative tissues. Chrysanthemum DvDREB2A was expressed in all organs under normal conditions (Liu et al., 2008). SiDREB2, a DREB2 gene accumulated in leaves, roots, young and mature spikelets of foxtail millet indicating its function in developmental pathways also (Lata et al., 2011).

AtDREB1 was induced within 10 min at 4 0C (Liu et al., 1998). The transcript of CBF genes was detectable after 30 min at 40C with highest accumulation at 1 h (Medina et al., 1999). HvDREB1 gene in barley leaves significantly accumulated on salt, drought, and low-temperature treatments (Xu et al., 2009). OsDREB1A and Os-DREB1B were induced early (within 40 min) after cold exposure but not on ABA treatment. OsDREB1A was induced within 5 h of salinity stress whereas OsDREB1C showed constitutive expression (Dubouzet et al., 2003). PNDREB1 strongly responded to low temperature and dehydration (Mei et al., 2009). However, hot pepper Ca-DREBLP1 was quickly activated by dehydration, high salinity and mechanical wounding but not at all by cold stress (Hong and Kim, 2005). The expression of Arabidopsis DREB2A and its homolog DREB2B were stimulated by dehydration and high salinity, but not by cold and ABA (Liu et al., 1998; Nakashima et al., 2000). Similarly, ABA, mannitol and cold treatments had minimal effect on DREB2C expression (Lee et al., 2010). A detailed study of all five rice OsDREB2s showed that OsDREB2A expressed to the highest levels under the control condition, and its expression was increased to some extent by high temperature, drought and high salinity, but not by low temperature treatments. Expression of OsDREB2B was markedly increased after 20 min of high and 24 h of low temperature stress. While the transcript levels of OsDREB2C, OsDREB2E and OsABI4 were low under the control condition and were transiently induced by the abiotic stresses (Matsukura et al., 2010). Wheat TaDREB1and WDREB2, maize ZmDREB2A, and pearl millet PgDREB2 are responsive to cold stress while foxtail millet SiDREB2 was not (Shen et al., 2003a; Egawa et al., 2006; Agarwal et al., 2007; Qin et al., 2007; Lata et al., 2011). Expression of chickpea CAP2 was induced by dehydration, NaCl, ABA and auxin treatments but not by low temperature, salicylic acid and jasmonic acid (Shukla et al., 2006). The transcript expression of Salicornia brachiata SbDREB2A was stimulated by NaCl, drought and heat stress (Gupta et al., 2010).

Transgenic Arabidopsis plants over-expressing DREB1B/CBF1 or DREB1A/CBF3 show strong tolerance to freezing, drought, and high salinity stresses implying that DREBs/CBFs affect multiple genes (Jaglo-Ottosen et al., 1998; Liu et al., 1998; Kasuga et al., 1999). DREB1A/CBF3 overexpressing transgenics accumulated proline and various sugars under non-stress conditions (Gilmour et al., 2000). Transgenic Arabidopsis and rice plants overexpressing OsDREB1A too displayed tolerance to low temperatures, high salinity and drought (Dubouzet et al., 2003; Ito et al., 2006). The rd29A:DREB1A/CBF3 wheat transgeneic showed improved drought stress tolerance (Pellegrineschi et al., 2004). Likewise, the constitutively overexpressing CBF3/DREB1A and ABF3 transgenic rice showed better drought and salinity tolerance without any growth inhibition or phenotypic anomalies (Oh et al., 2005). The overexpression of AhDREB1 accumulated putative downstream target genes and also conferred improved survival rate to transgenic tobacco plants under salt stress as compared to the wild-type plants (Shen et al., 2003b). The over-expression of OsDREB1F greatly enhanced tolerance of plants to high salinity, drought, and low-temperature both in rice and Arabidopsis, thus playing a significant role in plant stress signal transduction (Wang et al., 2008). Microarray analysis of transgenic Arabidopsis plants suggested that over-expression of DREB2A-CA induced drought-, salt-responsive and heat-shock (HS)-related genes. These transgenic plants also exhibited enhanced thermotolerance which was significantly decreased in DREB2A knockout plants (Sakuma et al., 2006). Overexpression of DREB2C was also found to activate the expression of many HS responsive genes (Lim et al., 2007). Transgenic Arabidopsis plants overexpressing maize ZmDREB2A were dwarf and also displayed improved drought and heat stress tolerance. Transgenic Arabidopsis plants overexpressing OsDREB2B showed enhanced expression of DREB2A target genes and improved drought and heat-shock stress tolerance (Matsukura et al., 2010). Transgenic tobacco plants overexpressing PgDREB2A showed better tolerance to both hyperionic and hyperosmotic stresses (Agarwal et al. 2010). Transgenic tobacco plants overexpressing CAP2 showed improved growth and development, and tolerance to dehydration and salt stress (Shukla et al., 2006). While its expression in yeast (Saccharomyces cerevisae) enhanced heat tolerance, with increased expression of heat shock factor 1 (Hsf1) and its target yeast heat shock protein 104 (Hsp 104) suggesting strong evolutionary conservation of the stress response mechanisms (Shukla et al., 2009). In another remarkable study it was described that the recombinant E. coli cells expressing SbDREB2A exhibited better growth in basal LB medium as well as if supplemented with NaCl, PEG and mannitol (Gupta et al., 2010).

These studies indicate that the DREB proteins are important TFs in regulating abiotic stress-related genes and play a critical role in imparting stress endurance to plants.


6. The NAC (NAM, ATAF and CUC) and ZF-HD (zinc-finger homeodomain) regulon

The NAC family of plant-specific TFs is one of the largest in the plant genome, with 106 and 149 members in Arabidopsis and rice, respectively (Gong et al., 2004, Xiong et al., 2005). NAC family TFs contains a highly conserved N-terminal DNA-binding domain and a diversified C-terminal domain (Hu et al., 2008). NAC was derived from the names of the first three described TFs containing NAC domain, namely NAM (no apical meristem), ATAF1-2 and CUC2 (cup-shaped cotyledon) (Souer et al., 1996; Aida et al., 1997). The cis-element of NAC TF [NAC recognized sequence (NACRS)] was also identified in Arabidopsis (Tran et al., 2004).

Numerous studies have examined the involvement of several types of NAC TFs in plant developmental programs (Sablowski and Meyerowitz 1998; Xie et al. 2000; Weir et al. 2004), and disease resistance (Collinge and Boller, 2001; Oh et al., 2005; Nakashima et al., 2007). A few NAC genes were found to be involved in response to various environmental stresses also such as ANAC019, ANAC055, and ANAC072 from Arabidopsis (Tran et al., 2004), and BnNAC from Brassica (Hegedus et al., 2003). SNAC1 is activated mainly in guard cells under dehydration (Hu et al., 2006). AtNAP and its homologs play an important role in leaf senescence in Arabidopsis (Guo and Gan et al., 2006). ERD1 promoter analysis showed that TFs belonging to the NAC family and ZF-HD are important for the activation of the ERD1 (early responsive to dehydration stress 1) gene (Tran et al., 2007). XND1 is expressed in xylem and associated with stress, ABA response and leaf senescence in Arabidopsis (Zhao et al., 2008). In soybean 101 NAC domain containing proteins, identified as functionally non-redundant were involved in response to abiotic stresses and in cell death events whereas GmNAC2, GmNAC3 and GmNAC4 were strongly induced by osmotic stress (Pinheiro et al., 2009). Soybean NACs GmNAC3 andGmNAC4 were also induced by ABA, JA and salinity but differed in their response to cold. GmNAC1, GmNAC5 and GmNAC6 transiently expressed in tobacco leaves, resulting in cell death and enhanced expression of senescence markers. Flavonoid biosynthesis is regulated by ANAC078 under high-light (Morishita et al., 2009). A rice NAC gene, ONAC045 was induced by drought, high salt, low temperature, and ABA treatment in leaves and roots (Zheng et al., 2009). The transcription level of CaNAC1 could be elevated by exogenous SA, ET, and MeJA treatment (Oh et al., 2005). A novel wheat NAC TF, TaNAC4 was found to be induced in response to cold, salt, wounding, ABA, ethylene and MeJA, suggesting a significant cross-talk between abiotic and biotic stress conditions (Xia et al., 2010). Kim et al. (2008) reported that a salt-inducible NTL8 (membrane associated NAC) regulates gibberellic acid -mediated salt signaling in seed germination. Very recently a membrane associated NAC TF from foxtail millet was found to be up-regulated in drought, salinity, ethephone and MeJA treatments (Puranik et al., 2011).

Several target genes of the ANAC019, ANAC055, and ANAC072 transcriptional activators were identified in the Arabidopsis transgenic plants using cDNA microarray. These transgenic plants also exhibited improved drought tolerance (Tran et al., 2004). The SNAC1-overexpressing transgenic rice seedlings showed significantly higher survival rate than wild type under drought treatment and significantly enhanced salinity tolerance as well (Hu et al., 2006). A rice R2R3-MYB gene (UGS5) containing putative NACRS in the promoter region was also induced in the SNAC1-overexpressing plants (Hu et al., 2006). Many abiotic and biotic stress responsive genes were upregulated in the OsNAC6 transgenic plants, and the transgenics were tolerant to dehydration, high salt stresses (Nakashima et al., 2007). ONAC045 overexpressing rice plants showed enhanced tolerance to drought and salt treatments (Zheng et al., 2009). XND1overexpressing showed severe stunting, premature death, and repression of TE differentiation (Zhao et al., 2008). Hence NAC TFs play an indispensable role in physiological adaptation for successful plant propagation under abiotic stress conditions.


7. Other TFs in abiotic stress response and tolerance

There are a number of TFs which are involved in abiotic stress responses other than the TFs belonging to the well known regulons described above. A new class of homeodomain TF known as HIGHER EXPRESSION OF OSMOTICALLY RESPONSIVE GENE 9 (HOS 9) and a R2R3-type MYB protein HOS 10 have been identified recently which are found to be associated with cold stress (Zhu et al., 2004, 2005). hos9 and hos 10 mutants show freezing hypersensitivity but at the same time enhance expression of RD29A and other cold responsive genes without changes in the CBF/DREB1 regulon implicating their role as negative regulators of cold stress-responsive genes. Another homeodomain TF, HDG11 which codes for HD-START TF plays a significant role in drought tolerance by enhancing the water homeostasis of the plants (Yu et al., 2008).

HARDY (HRD), an AP2-EREBP IIIc TF gene is expressed in inflorescence tissue to protect it from desiccation (Nakano et al., 2006). Rice plants overexpressing HRD exhibited drought and salinity tolerance as well as improved WUE (Karaba et al., 2007). ERFs (ethylene responsive factors) also belong to the AP2-EREBP TF and have been found to be involved in growth, development, metabolic regulation and biotic and abiotic stress responses (Hussain et al., 2011). Transgenic tobacco plants expressing SodERF3 exhibited extremely improved drought and salt tolerance (Trujillo et al., 2008). Zhang et al., (2009) reported that transgenic tobacco plants overexpressing soybean GmERF3 exhibited tolerance not only to high salinity and drought stresses but also to various pathogens, suggesting its crucial role in both abiotic and biotic stresses.

WRKYs are another important class of plant TFs which have shown to possess multiple functions in plants including abiotic stress responses. OsWRKY45 in rice was up-regulated by dehydration, cold, heat and salt (Qiu and Yu, 2009). Arabidopsis overexpressing OsWRKY45 also showed improved drought tolerance. They have suggested that OsWRKY45 may be involved in ABA synthesis that induces a signaling cascade resulting in lowered transpiration and enhanced tolerance to drought. Overexpression of the OsWRKY89 in rice led to growth inhibition at early stages of plant development, but showed increased tolerance to UV irradiation and fungal infection (Wang et al., 2007). GmWRKY13, GmWRKY21 and GmWRKY54 were found to be differentially expressed under abiotic stresses (Zhou et al., 2008). Transgenic Arabidopsis plants overexpressing GmWRKY21were tolerant to cold stress, whereas GmWRKY54 conferred salt and drought tolerance, possibly through the regulation of DREB2A and STZ/Zat10. However, transgenic plants over-expressing GmWRKY13 showed increased sensitivity to salt and mannitol stress, decreased sensitivity to ABA, and an increase in lateral roots. Archana et al., (2009) reported that down-regulation of NbWRKY; an abiotic stress related WRKY TF, by virus-induced gene silencing produced chlorosis and senescing phenotype in tobacco plants.

Zinc finger proteins (ZFPs) are one of the important TFs found abundantly in plants and animals. They contain sequence motifs in which cysteines and/or histidines coordinate zinc atom(s) forming local peptide structures required for their specific functions (Singh et al., 2010). Cys2/His2 (C2H2)-type ZFPs containing the EAR transcriptional repressor domain, play a key role in regulating the defense responses of plants to biotic and abiotic stress conditions (Singh et al., 2010). Over-expression of Alfin1, a novel member of the ZFP family confers salt tolerance to the transgenic Alfalfa plants (Winicov and Bastola, 1999). The constitutive over-expression of soybean SCOF-1 induced cold-regulated (COR) gene expression and transgenic Arabidopsis and tobacco plants (Kim et al., 2001). ZPT2-3, a C2H2-type Petunia ZFP, when constitutively over-expressed in petunia, resulted in dehydration tolerance of transgenic plants (Sugano et al. 2003). OSISAP1 from rice was inducible by cold, desiccation, salt, submergence, heavy metals and wounding, and its overexpression in tobacco exhibited cold, dehydration and salt tolerance at the seed germination/seedling stages (Mukhopadhyay et al., 2004). Constitutive expression of Zat12 in Arabidopsis resulted in the increased expression of oxidative- and light stress responsive genes (Davletova et al., 2005). Transgenic Arabidopsis plants constitutively expressing the Zat7 exhibited suppressed growth and were more tolerant to salinity stress (Ciftci-Yilmaz et al., 2007). CaZF, a C2H2 ZFP provided salinity-tolerance in transgenic tobacco (Jain et al., 2009). Interestingly, heterologous expression of CaZF provided osmotolerance in S. cerevisiae through Hog1p and calcineurin dependent as well as independent pathways (Jain et al., 2009).


8. Conclusion and future perspectives

In response to abiotic stresses such as, drought, salinity, heat, cold and mechanical wounding many genes are regulated, and their gene products function in providing stress tolerance to plants. Understanding the molecular mechanisms of plant responses to abiotic stresses is very important as it facilitates in exploiting them to improve stress tolerance and productivity. This review summarizes the role of important plant TFs namely; ABRE, MYC/MYB, CBF/DREBs and NAC that regulate various stress responsive gene expression. They play a crucial role in providing tolerance to multiple stresses generally in both ABA-dependent and -independent manner and through respective cis-elements and DNA binding domains. These TFs can be genetically engineered to produce transgenics with higher tolerance to drought, salinity, heat and cold using different promoters. Functional analysis of these TFs will thus provide more information on the intricate regulatory networks involved in abiotic stress responses and the cross-talk between different signaling pathways during stress adaptation. Further, considering TFs as candidate genes in breeding and other crop improvement programs will give us a clear understanding of abiotic stress related signal transduction events and eventually will lead us to develop crop varieties superior in stress tolerance by genetic manipulation.



This study was supported by the Department of Biotechnology, Govt. of India, New Delhi and core grant from the National Institute of Plant Genome Research (NIPGR). Ms Charu Lata acknowledges the award of SRF from the UGC, New Delhi. We are thankful to Prof. A. K. Tyagi (Director, NIPGR) for support and encouragement.


  1. 1. AbeH.Yamaguchi-ShinozakiK.UraoT.IwasakiT.HosokawaD.ShinozakiK.1997Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. The Plant Cell 918591868
  2. 2. AbeH.UraoT.ItoT.SekiM.ShinozakiK.Yamaguchi-ShinozakiK.2003Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell 156378
  3. 3. AgarwalM.HaoY.KapoorA.DongC. H.FujiH.ZhengX.ZhuJ. K.2006A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. Journal of Biological Chemistry 2813763637645
  4. 4. AgarwalP. K.AgarwalP.ReddyM. K.SoporyS. K.2006Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Reports 2512631274
  5. 5. AgarwalP.AgarwalP. K.NairS.SoporyS. K.ReddyM. K.2007Stress inducible DREB2A transcription factor from Pennisetum glaucum is a phosphoprotein and its phosphorylation negatively regulates its DNA binding activity. Molecular Genetics and Genomics 277189198
  6. 6. AgarwalP.AgarwalP. K.JoshiA. J.SoporyS. K.ReddyM. K.2010Overexpression of PgDREB2A transcription factor enhances abiotic stress tolerance and activates downstream stress-responsive genes. Molecular Biology Reports 3711251135
  7. 7. AgarwalP. K.JhaB.2010Transcription factors in plants and ABA dependent and independent abiotic stress signaling. Biologia Plantarum 54201212
  8. 8. AidaM.IshidaT.FukakiH.FujisawaH.TasakaM.1997Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell 9841857
  9. 9. AlmogueraC.Prieto-DapenaP.Díaz-MartínJ.EspinosaJ. M.CarrancoR.JordanoJ.2009The HaDREB2 transcription factor enhances basal thermotolerance and longevity of seeds through functional interaction with HaHSFA9. BMC Plant Biology 9:75 doi:
  10. 10. ArakiS.ItoM.SoyanoT.NishihamaR.MachidaY.2004Mitotic cyclins stimulate the activity of c-Myb-like factors for transactivation of G2/M phase-specific genes in tobacco. Journal of Biological Chemistry 2793297988
  11. 11. ArchanaK.RamaN.MamruthaH. M.NatarajaK. N.2009Down-regulation of an abiotic stress regulated Nicotiana benthamiana WRKY transcription factor induces physiological abnormalities. Indian Journal of Biotechnology 85360
  12. 12. BartelsD.SunkarR.2005Drought and salt tolerance in plants. Critical Reviews in Plant Science 21136
  13. 13. BehnamB.KikuchiA.Celebi-ToprakF.YamanakaS.KasugaM.Yamaguchi-ShinozakiK.WatanabeK. N.2006The Arabidopsis DREB1A gene driven by the stress-inducible rd29A promoter increases salt-stress tolerance in proportion to its copy number in tetrasomic tetraploid potato (Solanum tuberosum). Plant Biotechnology 23169177
  14. 14. BensmihenS.RippaS.LambertG.JublotD.PautotV.GranierF.GiraudatJ.ParcyF.2002The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 1413911403
  15. 15. Bhatnagar-MathurP.DeviM. J.DSReddyVadez. V.Yamaguchi-ShinozakiK.SharmaK. K.2006Overexpression of Arabidopsis thaliana DREB1A in transgenic peanut (Arachis hypogaea L.) for improving tolerance to drought stress (poster presentation). In: Arthur M. Sackler Colloquia on ‘‘From Functional Genomics of Model Organisms to Crop Plants for Global Health’’, April 35National Academy of Sciences, Washington, DC.
  16. 16. BihaniP.CharB.BhargavaS.2011Transgenic expression of sorghum DREB2 in rice improves tolerance and yield under water limitation. The Journal of Agricultural Science 14995101
  17. 17. BohnertH. J.AyoubiP.BorchertC.BressanR. A.BurnapR. L.CushmanJ. C.MACushmanDeyholos. M.FisherR.GalbraithD. W.HasegawaP. M.JenksM.KawasakiS.KoiwaH.Kore-edaS.Lee-HB.MichalowskiC. B.MisawaE.NomuraM.OzturkN.PostierB.PradeR.Song-PC.TanakaY.WangH.ZhuJ. K.2001A genomic approach towards salt stress tolerance. Plant Physiology and Biochemistry 39295311
  18. 18. BorevitzJ. O.XiaY. J.BlountJ.DixonR. A.LambC.2000Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. The Plant Cell 1223832393
  19. 19. BrayE. A.Bailey-SerresJ.WeretilnykE.2000Responses to abiotic stresses. In Biochemistry and Molecular Biology of Plants, Buchanan BB, Gruissem W, and Jones RL, eds (Rockville, MD: American Society of Plant Biologists), 11581203
  20. 20. Bray EA1994Alterations in gene expression in response to water deficit. In Stress-Induced Gene Expression in Plants (Basra, A.S., ed.). Amsterdam: Harwood Academic, 123
  21. 21. BuskP. K.PagèsM.1998Regulation of abscisic acid-induced transcription. Plant Molecular Biology 37425435
  22. 22. CasarettoJ.HoT. H.2003The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15271284
  23. 23. ChenJ.XiaX.YinW.2009Expression profiling and functional characterization of a DREB2-type gene from Populus euphratica. Biochemical and Biophysical Research Communications 378483487
  24. 24. ChenJ. Q.MengX. P.ZhangY.XiaM.WangX. P.2008Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnology Letter 3021912198
  25. 25. ChenM.WangQ. Y.ChengX. G.XuZ. S.LiL. C.YeX. G.XiaL. Q.MaY. Z.2007GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochemical and Biophysical Research Communications 353299305
  26. 26. ChenY.YangX.HeK.LiuM.LiJ.GaoZ.LinZ.ZhangY.WangX.QiuX.ShenY.LiZ.DengX.LuoJ.Deng-WX.ChenZ.GuH.Qu-JL.2006The MYB transcription factor superfamily of Arabidopsis: Expression analysis and phylogenetic comparison with the rice MYB family. Plant Molecular Biology 60107124
  27. 27. CheongY. H.ChangH. S.GuptaR.WangX.ZhuT.LuanS.2002Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129661677
  28. 28. ChinnusamyV.SchumakerK.ZhuJ.2004Molecular genetic perspectives on cross-talk and specificity in abiotic stress signaling in plants. Journal of Experimental Botany 55225236
  29. 29. ChoiH.HongJ.HaJ.KangJ.KimS. Y.2000ABFs, a family of ABA responsive element binding factors. Journal of Biological Chemistry 27517231730
  30. 30. Ciftci-YilmazS.MorsyM. R.SongL.CoutuA.BAKrizekLewis. M. W.WarrenD.CushmanJ.ConnollyE. L.MittlerR.2007The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. Journal of Biological Chemistry 28292609268
  31. 31. CollingeM.BollerT.2001Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Molecular Biology 46521529
  32. 32. CominelliE.GalbiatiM.VavasseurA.ContiL.SalaT.VuylstekeM.LeonhardtN.DellaportaS. L.TonelliC.2005A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Current Biology 1511961200
  33. 33. CominelliE.SalaT.CalviD.GusmaroliG.TonelliC.2008Overexpression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. The Plant Journal 535364
  34. 34. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR2010Abscisic acid: Emergence of a core signaling network. Annual Reviews in Plant Biology 61651679
  35. 35. DaiX.XuY.MaXuQ.WangW.XueT.ChongY.K.2007Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiology 14317391751
  36. 36. DavletovaS.SchlauchK.CoutuJ.MittlerR.2005The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiology 139847856
  37. 37. DenekampM.SmeekensS. C.2003Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene. Plant Physiology 13214151423
  38. 38. DingZ.LiS.AnX.LiuX.QinH.WangD.2009Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. Journal of Genetics & Genomics 361729
  39. 39. DubouzetJ. G.SakumaY.ItoY.KasugaM.DubouzetE. G.MiuraS.SekiM.ShinozakiK.Yamaguchi-ShinozakiK.2003OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. The Plant Journal 33751763
  40. 40. EgawaC.KobayashiF.IshibashiM.NakamuraT.NakamuraC.TakumiS.2006Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes & Genetic Systems 817791
  41. 41. FarooqM.WahidA.KobayashiN.FujitaD.BasraS. M. A.2009Plant drought stress: effects, mechanisms and management. Agronomy of Sustainable Development 29185212
  42. 42. FowlerS.ThomashowM. F.2002Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. The Plant Cell 1416751690
  43. 43. FujitaM.MizukadoS.FujitaY.IchikawaT.NakazawaM.SekiM.MatsuiM.Yamaguch-ShinozakiK.ShinozakiK.2007Identification of stress-tolerance-related transcription-factor genes via mini-scale full length cDNA over-eXpressor (FOX) gene hunting system. Biochemical and Biophysical Research Communications 364250257
  44. 44. FujitaY.FujitaM.SatohR.MaruyamaK.MMParvezSeki. M.HiratsuK.MasaruO. T.KazuoS.KazukoY. S.2005AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. The Plant Cell 1734703488
  45. 45. FurihataT.MaruyamaK.FujitaY.UmezawaT.YoshidaR.ShinozakiK.Yamaguchi-ShinozakiK.2006Abscisic acid dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proceedings of the National Academy of Sciences USA 10319881993
  46. 46. GigolashviliT.YatusevichR.BergerB.MullerC.FluggeU. I.2007The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine derived glucosinolate biosynthesis in Arabidopsis thaliana. The Plant Journal 51247261
  47. 47. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF2000Overexpression of Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiology 12418541865
  48. 48. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF1998Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. The Plant Journal 16433442
  49. 49. GiraudatJ.ParcyF.BertaucheN.GostiF.LeungJ.MorrisP.Bouvier-DurandM.VartanianN.1994Current advances in abscisic acid action and signaling. Plant Molecular Biology 2615571577
  50. 50. GongW.ShenY. P.MaPanL. G.DuY.WangY. L.YangD. H.HuJ. Y. L. D.LiuX. F.DongC. X.MaChenL.YangY. H.GaoX. Y.ZhuY.TanD.MuX.ZhangJ. Y.LiuD. B.Dinesh-KumarY. L.LiS. P.WangY.GuX. P.QuH. Y.BaiL. J.LuS. N.LiY. T.ZhaoJ. Y.JDZuoJ.HuangH.DengX. W.ZhuY. X.2004Genome-wide ORFeome cloning and analysis of Arabidopsis transcription factor genes. Plant Physiology 135773782
  51. 51. GuoY.GanS.2006AtNAP, a NAC family transcription factor, has an important role in leaf senescence The Plant Journal 46601612
  52. 52. GuptaK.AgarwalP. K.ReddyM. K.JhaB.2010SbDREB2A, an A-2 type DREB transcription factor from extreme halophyte Salicornia brachiata confers abiotic stress tolerance in Escherichia coli. Plant Cell Reports 2911311137
  53. 53. HaakeV.CookD.RiechmannJ. L.PinedaO.ThomashowM. F.ZhangJ. Z.2002Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiology 130639648
  54. 54. He X-J, Mu R-L, Cao W-H, Zhang Z-G, Zhang J-S, ChenS-Y(2005AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. The Plant Journal 44903916
  55. 55. HegedusD.YuM.BaldwinD.GruberM.SharpeA.ParkinI.WhitwillS.LydiateD.2003Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Molecular Biology 53383397
  56. 56. Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT2002Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiology 12910861094
  57. 57. HigginsonT.LiS. F.ParishR. W.2003AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. The Plant Journal 35177192
  58. 58. HoboT.KowyamaY.HattoriT.1999A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proceedings of the National Academy of Sciences USA 961534815353
  59. 59. Hong JP, Kim WT2005Isolation and functional characterization of the Ca-DREBLP1gene encoding a dehydration-responsive element binding-factor-like protein 1 in hot pepper (Capsicum annuum L. cv Pukang). Planta 220875888
  60. 60. HuH.DaiM.YaoJ.XiaoB.LiXianghua.ZhangQ.XiongL.2006Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proceedings of the National Academy of Sciences, USA 1031298712992
  61. 61. HuH.YouJ.FangY.ZhuX.QiZ.XiongL.2008Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Molecular Biology 67169181
  62. 62. HussainS. S.MAKayaniAmjad. M.2011Transcription factors as tools to engineer enhanced drought tolerance in plants. American Institute of Chemical Engineers DOI:btpr.514.
  63. 63. ItoY.KatsuraK.MaruyamaK.TajiT.KobayashiM.ShinozakiK.Yamaguchi-ShinozakiK.2006Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiology 47141153
  64. 64. Jaglo-OttosenK. R.GilmourS. J.ZarkaD. G.SchabenbergerO.ThomashowM. F.1998Arabidopsis CBF1 overexpression induces cor genes and enhances freezing tolerance. Science 280104106
  65. 65. JainD.RoyN.ChattopadhyayD.2009CaZF, a plant transcription factor functions through and parallel to HOG and calcineurin pathways in Saccharomyces cerevisiae to provide osmotolerance. PLoS One 4: e5154
  66. 66. JakobyM.WeisshaarB.Dröge-LaserW.Vicente-CarbajosaJ.TiedemannJ.KrojT.ParcyF.2002bZIP transcription factors in Arabidopsis. Trends in Plant Science 7106111
  67. 67. JiaZ.LianY.ZhuY.HeJ.CaoZ.WangG.2009Cloning and characterization of a putative transcription factor induced by abiotic stress in Zea mays. African Journal of Biotechnology 867646771
  68. 68. JinH.MartinC.1999Multifunctionality and diversity within the plant MYB-gene family. Plant Molecular Biology 41577585
  69. 69. Jin-FX.Jiong-SA.Peng-HR.Liu-GJ.GaoF.Chen-MJ.Yao-HQ.2010OsAREB1, an ABRE-binding protein responding to ABA and glucose, has multiple functions in Arabidopsis. BMB Reports 433439
  70. 70. JungC.SeoJ. S.HanS. W.KooY. J.KimC. H.SongS. I.NahmB. H.ChoiY. D.Cheong-JJ.2008Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiology 146623635
  71. 71. KameiA.SekiM.UmezawaT.IshidaJ.SatouM.AkiyamaK.ZhuJ. K.ShinozakiK.2005Analysis of gene expression profiles in Arabidopsis salt overly sensitive mutants sos2-1 and sos3-1. Plant, Cell & Environment 2812671275
  72. 72. Kang JY, Choi HI, Im MY, Kim SY2002Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. The Plant Cell 14343357
  73. 73. KarabaA.DixitS.GrecoR.AharoniA.TrijatmikoK. R.Marsch-MartinezN.KrishnanA.NatarajaK. A.UdayakumarM.PereiraA.2007Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proceedings of the National Academy of Sciences USA 1041527015275
  74. 74. KasugaM.LiuQ.MiuraS.Yamaguchi-ShinozakiK.ShinozakiK.1999Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17287291
  75. 75. KasugaM.MiuraS.ShinozakiK.Yamaguchi-ShinozakiK.2004A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiology 45346350
  76. 76. KavarT.MarasM.KidricM.Sustar-VozlicJ.MeglicV.2007Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Molecular Breeding 21159172
  77. 77. Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO, Cho MJ2001A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. The Plant Journal 25247259
  78. 78. KimS.KangJ. Y.ChoD. I.ParkJ. H.KimS. Y.2004ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant Journal 407587
  79. 79. Kim SG, Lee AK, Yoon HK, Park CM2008A membrane bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. The Plant Journal 557788
  80. 80. Kim-HT.Bo°hmerM.HuH.NishimuraN.SchroederJ. I.2010Guard cell signal transduction network: Advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annual Reviews in Plant Biology 61561591
  81. 81. KirikV.Ko°lleK.Mise´raS.Ba°umleinH.1998Two novel MYB homologues with changed expression in late embryogenesis-defective Arabidopsis mutants. Plant Molecular Biology 37819827
  82. 82. KizisD.PagèsM.2002Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. The Plant Journal 30679689
  83. 83. Klempnauer K.-H, TJ Gonda, JM Bishop1982Nucleo- tide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: The architecture of a transduced oncogene. The Cell 31453463
  84. 84. KobayashiF.MaetaE.TerashimaA.KawauraK.OgiharaY.TakumiS.2008Development of abiotic stress tolerance via bZIP-type transcription factor LIP19 in common wheat. Journal of Experimental Botany 59891905
  85. 85. LataC.BhuttyS.BahadurR. P.MajeeM.PrasadM.2011Association of a SNP in a novel DREB2like gene SiDREB2 with stress tolerance in foxtail millet [Setaria italica (L.)]. Journal of Experimental Botany DOI:jxb/err016.
  86. 86. Lee SJ, Kang JY, Park HJ, Kim MD, Bae MS, Choi HI, Kim SY2010DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiology 153716727
  87. 87. Li XP, Tian AG, Luo GZ, Gong ZZ, Zhang JS, Chen SY2005Soybean DRE-binding transcription factors that are responsive to abiotic stresses. Theoretical and Applied Genetics 11013551362
  88. 88. LiangY. K.DubosC.DoddI. C.HolroydG. H.HetheringtonA. M.MMCampbell2005AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Current Biology 1512011206
  89. 89. LiaoY.Zhang-SJ.Chen-YS.Zhang-KW..2008bRole of soybean GmbZip132 under abscisic acid and salt stresses. Journal of Integrative Plant Biology 50221230
  90. 90. LiaoY.ZouH.WeiW.HaoY. J.TianA. G.HuangJ.Liu-FY.Zhang-SJ.Chen-YS.2008aSoybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228225240
  91. 91. LiaoY.Zou-FH.Wang-WH.Zhang-KW.MaZhangB.-SJ.2008cSoybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants. Cell Research 1810471060
  92. 92. LimC. J.HwangJ. E.ChenH.HongJ. K.YangK. A.ChoiM. S.LeeK. O.ChungW. S.LeeS. Y.LimC. O.2007Over-expression of the Arabidopsis DRE/CRT-binding transcription factor DREB2C enhances thermotolerance. Biochemical and Biophysical Research Communications 362431436
  93. 93. LippoldF.SanchezD. H.MusialakM.SchlerethA.ScheibleW. R.HinchaD. K.UdvardiM. K.2009AtMyb41 Regulates Transcriptional and Metabolic Responses to Osmotic Stress in Arabidopsis[W][OA]. Plant Physiology 14917611772
  94. 94. DiegoH.MagdalenaMusialak.ArminSchlereth.Wolf-RuedigerScheible.DirkK.Hincha and Michael K. Udvardi
  95. 95. LiuQ.KasugaM.SakumaY.AbeH.MiuraS.GodaH.ShimadaY.YoshidaS.ShinozakiK.Yamaguchi-ShinozakiK.1998Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10391406
  96. 96. LiuL.ZhuK.YangY.WuJ.ChenF.YuD.2008Molecular cloning, expression profiling and trans-activation property studies of a DREB2-like gene from chrysanthemum (Dendranthema vestitum). Journal of Plant Research 121215226
  97. 97. Lu-LP.Chen-ZN.AnR.SuZ.Qi-SB.RenF.ChenJ.Wg-CX.2007A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Molecular Biology 63289305
  98. 98. MaSunL.LiuN.JiaoX.ZhaoY.DengH.X. W.2005Organ-specific expression of Arabidopsis genome during development. Plant Physiology 1388091
  99. 99. MagnaniE.SjölanderK.HakeS.2004From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. The Plant Cell 1622652277
  100. 100. MatsukuraS.MizoiJ.YoshidaT.TodakaD.ItoY.MaruyamaK.ShinozakiK.Yamaguch-ShinozakiK.2010Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Molecular Genetics and Genomics 283185196
  101. 101. MattanaM.BiazziE.ConsonniR.LocatelliF.VanniniC.ProveraS.CoraggioI.2005Overexpression of Osmyb4 Enhances Compatible Solute Accumulation and Increases Stress Tolerance of Arabidopsis thaliana. Physiologia Plantarum 125212223
  102. 102. MedinaJ.BarguesM.TerolJ.P´erez-AlonsoM.SalinasJ.1999The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiology 119463469
  103. 103. MeiZ.WeiL.Yu-PingB.Zi-ZhangW.2009Isolation and Identification of PNDREB1: A New DREB Transcription Factor from Peanut (Arachis hypogaea L.) Acta Agronomica Sinica 3519731980
  104. 104. MorishitaT.KojimaY.MarutaT.Nishizawa-YokoiA.YabutaY.ShigeokaS.2009Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiology 5022102222
  105. 105. MukhopadhyayA.VijS.TyagiA. K.2004Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proceedings of National Academy Sciences USA 10163096314
  106. 106. MustilliA. C.MerlotS.VavasseurA.FenziF.GiraudatJ.2002Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. The Plant Cell 1430893099
  107. 107. NakanoT.SuzukiK.FujimuraT.ShinshiH.2006Genome-Wide Analysis of the ERF Gene Family in Arabidopsis and Rice. Plant Physiology 140411432
  108. 108. NakashimaK.ItoY.Yamaguchi-ShinozakiK.2009Transcriptional Regulatory Networks in Response to Abiotic Stresses in Arabidopsis and Grasses. Plant Physiology 1498895
  109. 109. NakashimaK.ShinwarZ. K.SakumaY.SekiM.MiuraS.ShinozakiK.Yamaguchi-ShinozakiK.2000Organization and expression of two Arabidopsis DREB2genes encoding DRE-binding proteins involved in dehydration- and high salinity-responsive gene expression. Plant Molecular Biology 42657665
  110. 110. NakashimaK.Tran-SL.NguyenP.FujitaD. V.MaruyamaM.TodakaK.ItoD.HayashiY.ShinozakiN.Yamaguchi-ShinozakiK.K.2007Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. The Plant Journal 51617630
  111. 111. NakashimaK.Yamaguchi-ShinozakiK.2006Regulons involved in osmotic stress-responsive and cold stress responsive gene expression in plants. Physiologia Plantarum 1266271
  112. 112. NewmanL. J.PerazzaD. E.JudaL.MMCampbell2004Involvement of the R2R3-MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype. The Plant Journal 3723950
  113. 113. OhS. J.SongS. I.KimY. S.JangH. J.KimS. Y.KimM.KimY. K.NahmB. H.KimJ. K.2005Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiology 138341351
  114. 114. Oh-KS.LeeS.YuS. H.ChoiD.2005Expression of a novel NAC domain containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta 222876887
  115. 115. PasqualiG.BiricoltiS.LocatelliF.BaldoniE.MattanaM. .2008Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Reports 2716771686
  116. 116. Paz-AresJ.GhosalD.WienandU.PetersonP. A.SaedlerH.1987The regulatory cl locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO f. 635533558
  117. 117. PellegrineschiA.ReynoldsM.PachecoM.BritoR. M.AlmerayaR.Yamaguchi-ShinozakiK.HoisingtonD.2004Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47493500
  118. 118. PengH.ChengH. Y.YuX. W.ShiQ. H.ZhangH.LiJ. G.MaH.2009Characterization of a chickpea (Cicer arietinum L.) NAC family gene, CarNAC5, which is both developmentally- and stress-regulated. Plant Physiology & Biochemistry 47103745
  119. 119. Pinheiro GL, Marques CS, Costa MDBL, Reis PAB, Alves MS, Carvalho CM, Fietto LG, Fontes EPB2009Complete inventory of soybean NAC transcription factors: Sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 4441023
  120. 120. PuranikS.BahadurR. P.SrivastavaP. S.PrasadM.2011Molecular cloning and characterization of a membrane associated NAC family gene, SiNAC from foxtail millet [Setaria italica (L.) P. Beauv.]. Molecular Biotechnology DOI:s12033-011-9385-7.
  121. 121. QinF.KakimotoM.SakumaY.MaruyamaK.OsakabeY.TranL. S.ShinozakiK.Yamaguchi-ShinozakiK.2007Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. The Plant Journal 505469
  122. 122. QiuY.YuD.2009Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environmental and Experimental Botany 653547
  123. 123. RiechmannJ. L.HeardJ.MartinG.ReuberL.JiangC.KeddieJ.AdamL.PinedaO.RatcliffeO. J.SamahaR. R.CreelmanR.PilgrimM.BrounP.ZhangJ. Z.GhandehariD.ShermanB. K.YuG.2000Arabidopsis transcription factor: genome wide comparative analysis among eukaryotes. Science 29021052110
  124. 124. Rosinski JA, Atchley WR1998Molecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin. Journal of Molecular Evolution 467483
  125. 125. Sablowski RW, Meyerowitz EM1998A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. The Cell 9293103
  126. 126. SaiboN. J. M.Lourenc¸oT.MMOliveira2009Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Annals of Botany 103609623
  127. 127. SakumaY.MaruyamaK.QinF.OsakabeY.ShinozakiK.Yamaguchi-ShinozakiK.2006Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proceedings of National Academy of Sciences USA 1031882218827
  128. 128. SavitchL. V.AllardG.SekiM.RobertL. S.TinkerN. A.HunerN. P. A.ShinozakiK.SinghJ.2005The effect of overexpression of two Brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus. Plant Cell Physiology 4615251539
  129. 129. SekiM.NarusakaM.IshidaJ.NanjoT.FujitaM.OonoY.KamiyaA.NakajimaM.EnjuA.SakuraiT.SatouM.AkiyamaK.TajiT.Yamaguchi-ShinozakiK.CarninciP.KawaiJ.HayashizakiY.ShinozakiK.2002Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full-length cDNA microarray. The Plant Journal 31279292
  130. 130. SekiM.KameiA.SatouM.SakuraiT.FujitaM.OonoY.Yamaguch-ShinozakiK.ShinozakiK.2003Transcriptome analysis in abiotic stress conditions in higher plants. Topics Curr Genet 4271295
  131. 131. Shan-PD.Huang-GJ.Yang-TY.Guo-HY.Wu-AC.Yang-DG.GaoZ.Zheng-CC.2007Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytologist 1767081
  132. 132. ShenQ.ZhangP.HoT.1996Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 811071119
  133. 133. ShenY. G.ZhangW. K.HeS. J.ZhangJ. S.LiuQ.ChenS. Y.2003aAn EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theoretical and Applied Genetics 106923930
  134. 134. ShenY. G.ZhangW. K.YanD. Q.DuB. X.ZhangJ. S.LiuQ.ChenS. Y.2003bCharacterization of a DRE-binding transcription factor from a halophyte Atriplex hortensis. Theoretical and Applied Genetics 107155161
  135. 135. ShinD.Moon-JS.HanS.Kim-GB.ParkS. R.Lee-KS.Yoon-JH.Lee-EH.Kwon-BH.BaekD.YiB. Y.Byun-OM.2011Expression of StMYB1R-1, a novel potato single MYB-like domain transcription factor, increases drought tolerance. Plant Physiology 155421432
  136. 136. ShinozakiK.Yamaguchi-ShinozakiK.2007Gene networks involved in drought stress tolerance and response. Journal of Experimental Botany 58221227
  137. 137. ShuklaR. K.RahaS.TripathiV.ChattopadhyayD.2006Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiology 142113123
  138. 138. ShuklaR. K.TripathiV.JainD.YadavR. K.ChattopadhyayD.2009CAP2 enhances germination of transgenic tobacco seeds at high temperature and promotes heat stress tolerance in yeast. FEBS Journal 27652525262
  139. 139. SinghA. K.SoporyS. K.WuR.Singla-PareekS. L.2010Transgenic Approaches. In: Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation, A Pareek, SK Sopory, HJ Bohnert and Govindjee (eds.), 417450
  140. 140. SouerE.Van HouwelingenA.KloosD.MolJ.KoesR.1996The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordial boundaries. The Cell 85159170
  141. 141. Stockinger EJ, Gilmour SJ, Thomashow MF1997Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences USA 9410351040
  142. 142. StrackeR.WerberM.WeisshaarB.2001The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology 4447456
  143. 143. SuganoS.KaminakaH.RybkaZ.CatalaR.SalinasJ.MatsuiK.Ohme-TakagiM.TakatsujiH.2003Stress-responsive zinc finger gene ZPT2-3 plays a role in drought tolerance in petunia. The Plant Journal 36830841
  144. 144. Tran-SL.NakashimaP.SakumaK.SimpsonY.FujitaS. D.MaruyamaY.FujitaK.SekiM.ShinozakiM.Yamaguchi-ShinozakiK.K.2004Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. The Plant Cell 1624812498
  145. 145. TranL. S.NakashimaK.SakumaY.OsakabeY.QinF.SimpsonS. D.MaruyamaK.FujitaY.ShinozakiK.Yamaguchi-ShinozakiK.2007Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. The Plant Journal 494663
  146. 146. TrujilloL. E.SotolongoM.MenendezC.MEOchogavaColl. Y.HernandezI.Borras-HidalgoO.ThommaB. P. H. J.VeraP.HernandezL.2008SodERF3, a novel sugarcane ethylene responsive factor (ERF), enhances salt and drought tolerance when over-expressed in tobacco plants. Plant Cell Physiology 49512515
  147. 147. UdvardiM. K.KakarK.WandreyM.MontanriO.MurrayJ.AndraiankajaA.Zhang-YJ.BeneditoV.HoferJ. M. I.ChengF.TownC. D.2007Legume transcription factors: global regulators of plant development and response to the environment. Plant Physiology 144538549
  148. 148. UmezawaT.FujitaM.FujitaY.Yamaguchi-ShinozakiK.ShinozakiK.2006Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Current Opinion in Biotechnology 17113122
  149. 149. UmezawaT.YoshidaR.MaruyamaK.Yamaguchi-ShinozakiK.ShinozakiK.2004SRK2C. A SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 1011730617311
  150. 150. UnoY.FurihataT.AbeH.YoshidaR.ShinozakiK.Yamaguchi-ShinozakiK.2000Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proceedings of National Academy of Sciences USA 971163211637
  151. 151. UraoT.Yamaguchi-ShinozakiK.UraoS.ShinozakiK.1993An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. The Plant Cell 515291539
  152. 152. VanniniM.CampaM.IritiM.GengaA.FaoroF.CarravieriS.RotinoG. L.RossoniM.SpinardiA.BracaleM.2007Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene. Plant Science 173231239
  153. 153. VanniniC.LocatelliF.BracaleM.MagnaniE.MarsoniM.OsnatoM.MattanaM.BaldoniE.CoraggioI.2004Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. The Plant Journal 37115127
  154. 154. WangH.HaoJ.ChenX.2007Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Molecular Biology 65799815
  155. 155. WangQ.GuanY.WuY.ChenH.ChenF.ChuC.2008Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Molecular Biology 67589602
  156. 156. WeirI.LuJ.CookH.CausierB.Schwarz-SommerZ.DaviesB. .2004CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131915922
  157. 157. WinicovI.BastolaD. R.1999Transgenic overexpression of the transcription factor Alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants. Plant Physiology 120473480
  158. 158. XiaN.ZhangG.Liu-YX.DengL.Cai-LG.ZhangY.Wang-JX.ZhaoJ.Huang-LL.Kang-SZ.2010Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Molecular Biology Reports 3737033712
  159. 159. XiangY.TangN.DuH.YeH.XiongL.2008Charaterization of Osb-ZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiology 14819381952
  160. 160. XieQ.FrugisG.ColganD.ChuaN. H.2000Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes & Development 1430243036
  161. 161. XieD. Y.SharmaS. B.WrightE.WangZ. Y.DixonR. A.2006Metabolic engineering of proanthocyanidins through co-expression of anthocyanidin reductase and the PAP1 MYB transcription factor. The Plant Journal 45895907
  162. 162. XiongY.LiuT.TianC.SunS.LiJ.ChenM.2005Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Molecular Biology 59191203
  163. 163. Xu QJ, Cui CR2007Genetic transformation of OSISAP1 gene to onion (Allium cepa L.) mediated by amicroprojectile bombardment. Journal of Plant Physiology and Molecular Biology (Article in Chinese) 3318896
  164. 164. XuZ. S.NiZ. Y.LiZ. Y.LiL. C.ChenM.GaoD. Y.YuX. D.LiuP.MaY. Z.2009Isolation and functional characterization of HvDREB1-a gene encoding a dehydration-responsive element binding protein in Hordeum vulgare. Journal of Plant Research 122121130
  165. 165. Xue GP, Loveridge CW2004HvDRF1 is involved in abscisic acid mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. The Plant Journal 37326339
  166. 166. Yamaguchi-ShinozakiK.ShinozakiK.1994A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. The Plant Cell 6251264
  167. 167. Yamaguchi-ShinozakiK.ShinozakiK.1993The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration-stress in Arabidopsis thaliana. Molecular and General Genetics 2381725
  168. 168. YangY.WuJ.ZhuK.LiuL.ChenF.YuD.2009Identification and characterization of two chrysanthemum (Dendronthema × morifolium) DREB genes, belonging to the AP2/EREBP family. Molecular Biology Reports 367181
  169. 169. YanhuiC.XiaoyuanY.KunH.MeihuaL.JigangL.ZhaofengG.ZhiqiangL.YunfeiZ.XiaoxiaoW.XiaomingQ.YunpingS.XiaohuiD.JingchuL.Xing-WangD.ZhangliangC.HongyaG.Li-JiaQ.2006The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Molecular Biology 60107124
  170. 170. YoshidaT.FujitaY.SayamaH.KidokoroS.MaruyamaK.MizoiJ.ShinozakiK.Yamaguchi-ShinozakiK.2010AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. The Plant Journal 61672685
  171. 171. YoshidaR.HoboT.IchimuraK.MizoguchiT.TakahashiF.AlonsoJ.EckerJ. R.ShinozakiK.2002ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiology 4314731483
  172. 172. YuH.ChenX.Hong-YY.WangY.XuP.Ke-DS.Liu-YH.Zhu-KJ.OliverD. J.Xiang-BC.2008Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. The Plant Cell 2011341151
  173. 173. ZhangG.ChenM.LiL.XuZ.ChenX.GuoJ.MaY.2009Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought and diseases in transgenic tobacco. Journal of Experiment Botany 6037813796
  174. 174. Zhang JZ, Creelman RA, Zhu JK2004From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiology 135615621
  175. 175. ZhaoC.AvciU.GrantE. H.HaiglerC. H.BeersE. P.2008XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. The Plant Journal 53425436
  176. 176. ZhengX.ChenB.LuG.HanB.2009Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochemical and Biophysical Research Communications 379985989
  177. 177. ZhouQ. Y.TianA. G.ZouH. F.XieZ. M.LeiG.HuangJ.WangC. M.WangH. W.ZhangJ. S.ChenS. Y.2008Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal 6486503
  178. 178. ZhuJ.ShiH.LeeB. H.DamszB.ChengS.StirmV.Zhu-KJ.HasegawaP. M.BressanR. A.2004An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proceedings of the National Academy of Sciences, USA 10198739878
  179. 179. ZhuJ.VersluesP. E.ZhengX.Lee-HB.ZhanX.ManabeY.SokolchikI.ZhuY.Dong-HC.Zhu-KJ.HasegawaP. M.BressanR. A.2005HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proceedings of the National Academy of Sciences, USA 10299669971
  180. 180. ZouM.GuanY.RenH.ZhangF.ChenF.2008A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Molecular Biology 66675683

Written By

Charu Lata, Amita Yadav and Manoj Prasad

Submitted: November 24th, 2010 Published: August 29th, 2011