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The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat

Kazuo Nakashima, Kazuko Yamaguchi-Shinozaki, Kazuo Shinozaki

Frontiers in Plant Science · 2014 · Review

doi:10.3389/fpls.2014.00170

Abstract

Drought negatively impacts plant growth and the productivity of crops around the world. Understanding the molecular mechanisms in the drought response is important for improvement of drought tolerance using molecular techniques. In plants, abscisic acid (ABA) is accumulated under osmotic stress conditions caused by drought, and has a key role in stress responses and tolerance. Comprehensive molecular analyses have shown that ABA regulates the expression of many genes under osmotic stress conditions, and the ABA-responsive element (ABRE) is the major cis-element for ABA-responsive gene expression. Transcription factors (TFs) are master regulators of gene expression. ABRE-binding protein and ABRE-binding factor TFs control gene expression in an ABA-dependent manner. SNF1-related protein kinases 2, group A 2C-type protein phosphatases, and ABA receptors were shown to control the ABA signaling pathway. ABA-independent signaling pathways such as dehydration-responsive element-binding protein TFs and NAC TFs are also involved in stress responses including drought, heat, and cold. Recent studies have suggested that there are interactions between the major ABA signaling pathway and other signaling factors in stress responses. The important roles of these TFs in crosstalk among abiotic stress responses will be discussed. Control of ABA or stress signaling factor expression can improve tolerance to environmental stresses. Recent studies using crops have shown that stress-specific overexpression of TFs improves drought tolerance and grain yield compared with controls in the field.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 17, 2026. Paragraph numbers are ours, so an answer can point at one.

INTRODUCTION

The world population is expected to reach nine billion by 2050. Considering this population increase, crop yields need to be improved by 40% in areas where drought is likely to occur by 2025. In addition, frequent occurrences of drought and abnormal weather events have lately been observed all over the world. Drought negatively impacts plant growth and crop production. Almost every year, some region of the earth is hit by drought, damaging crops, and disrupting agricultural production. Severe drought affected the central and south of the US Corn Belt during 2012. Drought also causes great damage to the production of other crops such as rice, wheat, and soybean. The southern states of Brazil, which account for 40% of the soybean production by the second leading producer worldwide, lost more than 20% of their production because of drought during the 2003/2004 and 2004/2005 seasons. The development of stress-tolerant crops will be significantly advantageous in areas where such stresses occur frequently. Recently, some progress has been made toward identification of stress-related genes potentially capable of increasing the tolerance of plants to abiotic stress. Understanding the molecular mechanisms in the drought response is important to improve drought tolerance using molecular techniques. ABA accumulates under osmotic stress caused by drought, but also by other water limiting conditions, and plays an important role in stress responses and tolerance in plants (reviewed in;;; Figure 1). Molecular studies have revealed that ABA-independent gene expression is also important in stress tolerance in plants (Figure 1). In this review, we summarize some of the most important TFs in drought responses and discuss their regulatory networks and crosstalk in abiotic stress responses. By applying current knowledge of stress-regulated TFs and their target genes, improvement of drought stress tolerance is in progress in various crops using transgenic technology.

AREB/ABF TFs FOR ABA-DEPENDENT GENE EXPRESSION

The promoter regions of ABA-responsive genes contain a conserved cis-element, named the ABRE (PyACGTGG/TC), which controls gene expression (Figure 1). Studies have revealed that expression of ABA-responsive genes requires more than one ABRE or a combination of an ABRE and a CE for a functional promoter (reviewed in,; ). Comprehensive and molecular analyses showed that ABA regulates the expression of many genes under osmotic stress conditions, and that the ABRE is the major cis-element for ABA-responsive gene expression. AREB/ABFs are bZIP TFs that regulate ABA-dependent gene expression, acting as major TFs under abiotic stress conditions in Arabidopsis (reviewed in,; Figure 1). Among the nine members of the AREB/ABF TF family identified in Arabidopsis, AREB1/ABF2 has been reported to control ABA signaling and environmental stress responses during the vegetative growth stage. The AREB/ABF TFs are induced by abiotic stress and their transcriptional activities are controlled by ABA-dependent phosphorylation. ABA is required for full activation of AREB1 and its activity is regulated by the ABA-dependent phosphorylation of multiple sites within conserved domains. Transgenic Arabidopsis plants overexpressing deleted and active forms of AREB1 showed enhanced drought tolerance and ABA hypersensitivity. Overexpression of AREB1 also improved drought tolerance in rice and soybean. Progress in understanding ABA perception and signal transduction has been made recently (reviewed in;;;; ). It was revealed that SnRK2, group A PP2Cs, and RCAR/PYR/PYL ABA receptors control the ABA signaling pathway including AREB/ABFs in land plants (reviewed in;; ). The phosphorylation of AREB/ABFs by SnRK2s is critical in the ABA-dependent signaling network. Recent studies have indicated that group A PP2Cs evolved early in land plants as key regulators of intrinsic desiccation tolerance, such as in the moss Physcomitrella patens. Perception and signaling factors such as PYL4 can also be used to improve stress tolerance.

DREB1/CBF TFs FOR COLD-RESPONSIVE GENE EXPRESSION TO IMPROVE DROUGHT TOLERANCE

Analysis of the promoter regions of genes showing ABA-independent expression in stress responses and tolerance has shown a cis-element with the sequence A/GCCGAC, designated the DRE/CRT (Figure 1). Two groups of AP2/ERF TFs were identified as DREB; DREB1/CBF and DREB2 in Arabidopsis. DREB1/CBF TFs specifically interact with the DRE/CRT and control the expression of a large number of stress-responsive genes in Arabidopsis. Improvements in tolerance to drought, salinity and freezing stresses have been reported in transgenic Arabidopsis overexpressing DREB1/CBF TFs, although their constitutive expression causes growth defects. However, overexpression of DREB1 under the control of the Arabidopsis stress-responsive RD29A promoter improved stress tolerance in Arabidopsis without growth defects. Cold-inducible DREB1/CBF genes have also been isolated from a number of plant species, such as maize, oilseed rape, rye (Secale cereale), rice, tomato, and wheat (Triticum aestivum; reviewed in ). Interestingly, the major QTLs for tolerance to frost in Arabidopsis, diploid wheat (T. monococcum) and barley map to DREB1/CBF genes, and the expression levels of DREB1/CBF genes are correlated with frost tolerance. Thus, the function of the DREB1/CBF regulon in the regulation of cold stress responses is widely conserved in angiosperms. Overexpression of DREB/CBF TFs has been reported to enhance drought tolerance in transgenic crops including chrysanthemum, peanut, potato, rice, soybean, tobacco, tomato, and wheat. For example, rice DREB1/CBF-type TFs involved in cold-responsive gene expression also conferred improved tolerance to drought in transgenic rice. The rice DREB1/CBF-type genes, OsDREB1A and OsDREB1B, are induced by cold stress. Transgenic Arabidopsis and rice plants overexpressing rice OsDREB1 or Arabidopsis DREB1 genes showed improved tolerance to drought, high-salt and cold stresses but defective growth under normal growth conditions. Elevated contents of osmoprotectants including free proline and soluble sugars were detected in the transgenic rice. These results indicate that the DREB1/CBF regulon is conserved in rice, and that DREB1/CBF-type genes may be useful for improvement of tolerance to different environmental stresses in various kinds of transgenic monocot plants as well as dicot plants.

DREB2 TFs FOR OSMOTIC- AND HEAT-RESPONSIVE GENE EXPRESSION TO IMPROVE DROUGHT TOLERANCE

The DREB2 gene encoding a DRE/CRT-binding protein is induced by osmotic stress (; Figure 1). However, transgenic plants overexpressing DREB2A did not show any changes in phenotype. Domain analysis of DREB2A using Arabidopsis protoplasts showed that deletion of the central region makes DREB2A constitutively active (DREB2Aca), indicating that this region contains a negative regulatory domain (NRD; ). Overexpression of DREB2Aca induced growth defects, up-regulation of stress-inducible genes, and enhanced drought tolerance. Stress-inducible overexpression of DREB2ca improved drought tolerance in Arabidopsis and soybean without growth defects. The NRD region of DREB2A is required for regulation of DREB2A protein stability. As mentioned above, overexpression of DREB1A improves freezing and dehydration stress tolerance in transgenic plants. By contrast, overexpression of DREB2Aca improves dehydration stress tolerance but only slightly improves freezing stress tolerance in transgenic plants. Integrated analysis of transcripts and metabolites was conducted to see the difference in the downstream gene products of DREB1A and DREB2A in Arabidopsis. Microarray analysis indicated that the downstream gene products of DREB1A and those of DREB2A have similar putative functions, but the expression of genes for carbohydrate metabolism in DREB1A and DREB2A transgenic plants is very different. Under dehydration and cold conditions, expression of genes for starch-degradation, sucrose metabolism and sugar alcohol synthesis changes dynamically. As a result, many kinds of mono-, di-, and trisaccharides, and sugar alcohols accumulate in plants. Overexpression of DREB1A caused similar changes in these metabolic processes, and these changes might improve dehydration and freezing stress tolerance in transgenic plants. By contrast, overexpression of DREB2Aca did not increase the level of these metabolites in transgenic plants. In addition, degradation of DREB2A is mediated by DRIPs, which are C3HC4 RING domain-containing proteins. DRIPs bind to DREB2A and function as E3 ubiquitin ligases mediating ubiquitination of DREB2A. Overexpression of DREB2Aca also induced expression of genes related to heat shock stress and improved thermotolerance in transgenic plants. These results indicate that DREB2s function in both dehydration and heat shock stress responses. DREB2-type proteins have been isolated from a number of other plant species such as barley, rice, sunflower, maize, and wheat. GmDREB2A;2 is a DREB2A ortholog in soybean, but there are differences between DREB2A and GmDREB2A;2 in the NRD sequence. The effects on gene expression in transgenic plants overexpressing GmDREB2A;2 are different from those in transgenic plants overexpressing DREB2A. This suggests that specialization in DREB2 regulons has occurred, although their basic functions are conserved between Arabidopsis and soybean. Recently, GWAS of ZmDREB2 and natural variations in the drought tolerance of maize (Zea mays) indicated that natural variation in the promoter region of ZmDREB2.7 contributes to drought tolerance in maize. The favorable ZmDREB2.7 allele may be a good resource for improving drought tolerance in maize. Recent studies suggest that DREB2 has important functions in drought tolerance, and that it can be used for improvement of drought tolerance in crops.

NAC TFs FOR DROUGHT-RESPONSIVE GENE EXPRESSION TO IMPROVE DROUGHT TOLERANCE

NAM, ATAF, and CUC TF proteins are plant-specific TFs. More than 100 NAC genes have been identified in Arabidopsis and rice (reviewed in ). Phylogenetic analyses indicate that six groups were established in an ancient moss. NAC TFs have a variety of important functions in development and stress responses. The genes in the SNAC group have important roles in the control of environmental stress tolerance (reviewed in; Figure 1), and can bind to the NACR (NAC recognition sequence; CACG core). Stress-responsive Arabidopsis SNAC genes such as RD26 and ATAF1, and rice SNAC genes such as SNAC1, OsNAC6/SNAC2, and OsNAC5 can improve drought and/or high-salt stress tolerance when overexpressed (;;;; reviewed in ). Stress-responsive overexpression of NACs utilizing rice stress-responsive LIP9, OsNAC6, or OsHox24 promoters is effective in inducing stress tolerance without the inhibitory effects of NAC on plant growth. Recent studies have suggested that the root-specific promoter RCc3 is useful for the overexpression of SNACs such as SNAC1 and OsNAC10 to enhance the abiotic stress tolerance of rice in field conditions. These results indicate that SNACs have important roles in the control of abiotic stress responses and tolerance and that it is possible to improve stress tolerance by overexpressing SNACs using suitable promoters in the field. The many kinds of drought-responsive or tissue/organ-specific promoters reported for roots and stomata might be effective tools to control the expression of drought-responsive factors that cause growth defects at the right time and right position.

INTERACTIONS BETWEEN MULTIPLE TFs IN DROUGHT RESPONSES

Evidence for interaction between the AREB/ABFs and DREB/CBFs has been reported. The DRE/CRT motif in the promoters of drought-responsive genes is a binding region for an ABA-independent DREB/CBF TF and functions as a CE for ABRE in ABA-dependent gene expression. showed that the DREB1A/CBF3, DREB2A, and DREB2C proteins interact physically with AREB/ABF proteins. These data suggest crosstalk between elements of the ABA-dependent and -independent response pathways. Moreover, interactions in the signaling pathways have also been indicated. reported that an ABRE promoter sequence, AREB/ABF TFs, and SnRK2s are involved in expression of the DREB2A gene under osmotic stress conditions, suggesting complex interaction between the AREB and DREB regulons at the gene expression level as well as the protein level.

Interaction between the AREB/ABFs and NACs has also been indicated at the gene expression level. reported that Arabidopsis SNAC TF ATAF1 directly regulates the ABA biosynthetic gene NCED3 in Arabidopsis, suggesting that SNAC TFs may regulate ABA-dependent gene expression of ABRE regulons. On the other hand, the promoters of SNAC genes contain ABRE sequences. Recently, reported that Arabidopsis ANAC096 cooperates with AREB/ABF factors (ABF2/AREB1 and ABF4/AREB2) in dehydration and osmotic stress responses. These results indicate complex interaction between the AREB/ABF and NAC regulons.

Finally, interaction between DREB/CBFs and other kinds of AP2/ERFs at the gene expression level has also been suggested. reported that the Arabidopsis ERF1 regulates gene expression by binding to two kinds of cis-elements, the GCC box and DRE/CRT, in response to different stress signals. ERF1 is an upstream TF in both ethylene and jasmonate signaling and is involved in resistance to pathogens. Their results suggested that ERF1 bound to the GCC box but not the DRE/CRT in response to biotic stress, and to the DRE/CRT under abiotic stress. These results suggest that ERF1 may integrate ethylene, jasmonate, and ABA signaling and play an important role in biotic and abiotic stress responses.

CONCLUSION

Molecular analysis has suggested that drought-responsive TFs such as DREB1/CBF, DREB2, AREB/ABF, and NAC TFs function in drought responses and tolerance (Figure 1). These TFs also function in crosstalk in abiotic stress responses, such as drought, cold, and heat. As mentioned above, these factors can be used to improve drought tolerance in a variety of crops. Our group has utilized these key TFs for the improvement of drought tolerance in crops including rice, wheat, and soybean in collaboration with international and domestic institutes. Some results using crops including rice and peanut have shown that stress-specific overexpression of DREB1A improves drought tolerance and grain yield compared with controls in the field. These results suggest that overexpression of key TFs under the control of suitable promoters can improve stress tolerance, although the regulatory network in the plant response is complex in water limiting environments (Figure 1). Since TFs function in balanced crosstalk in abiotic stress responses, overexpression of a certain TF may affect other signaling pathways. Thus, we should examine the molecular effects of overexpressing TFs in addition to conducting stress tolerance assays. In addition, the effects of a transgene may depend on the genetic background of the species or cultivar used for transformation. Furthermore, since the degree of drought varies in actual fields (strength, timing, and period of stress, complex stresses such as drought with heat stress etc.), the effect of a transgene may differ depending on environmental conditions. Continuous field experiments might be necessary to see the effects of transgene-encoded TFs in the field using a variety of genotypes and environments. Recently, QTL analyses have revealed novel genes involved in drought resistance. DEEPER ROOTING 1 (DRO1), a QTL controlling root growth angle in rice, was cloned and characterized. This study revealed that changes in root system architecture can improve drought avoidance. Other drought resistant QTLs have also been reported in rice. Multiple QTLs were reported in the rice mega-variety IR64 that enhance the yield under drought conditions. Combinations/pyramiding of transgenic plants and QTL drought resistant varieties by marker-assist selection (MAS) may promote drought tolerance.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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  44. 44.

    Mizoi J. Shinozaki K. Yamaguchi-Shinozaki K. (2012 ). AP2/ERF family transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819 86–96

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    Nakashima K. Fujita Y. Kanamori N. Katagiri T. Umezawa T. Kidokoro S. (2009a ). Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol. 50 1345–1363.

    Not in our library10.1093/pcp/pcp083

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    Nakashima K. Ito Y. Yamaguchi-Shinozaki K. (2009b ). Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 149 88–95

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    Nakashima K. Jan A. Todaka D. Maruyama K. Goto S. Shinozaki K. (2014 ). Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239 47–60

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    Nakashima K. Takasaki H. Mizoi J. Shinozaki K. Yamaguchi-Shinozaki K. (2012 ). NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819 97–103

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    Nakashima K. Tran L. S. Van Nguyen D. Fujita M. Maruyama K. Todaka D. (2007 ). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51 617–630

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    Nakashima K. Yamaguchi-Shinozaki K. (2013 ). ABA signaling in stress-response and seed development. Plant Cell Rep. 32 959–970

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    Narusaka Y. Nakashima K. Shinwari Z. K. Sakuma Y. Furihata T. Abe H. (2003 ). Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 34 137–148

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    Oh S. J. Song S. I. Kim Y. S. Jang H. J. Kim S. Y. Kim M. (2005 ). Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol. 138 341–351

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    Pellegrineschi A. Reynolds M. Pacheco M. Brito R. M. Almeraya R. Yamaguchi-Shinozaki K. (2004 ). Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47 493–500

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    Pennisi E. (2008 ). Plant genetics. The blue revolution, drop by drop, gene by gene. Science 320 171–173

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    Pizzio G. A. Rodriguez L. Antoni R. Gonzalez-Guzman M. Yunta C. Merilo E. (2013 ). The PYL4 A194T mutant uncovers a key role of PYR1-LIKE4/PROTEIN PHOSPHATASE 2CA interaction for abscisic acid signaling and plant drought resistance. Plant Physiol. 163 441–455

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    Polizel A. M. Medri M. E. Nakashima K. Yamanaka N. Farias J. R. De Oliveira M. C. (2011 ). Molecular, anatomical and physiological properties of a genetically modified soybean line transformed with rd29A:AtDREB1A for the improvement of drought tolerance. Genet. Mol. Res. 10 3641–3656

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    Qin F. Sakuma Y. Tran L. S. Maruyama K. Kidokoro S. Fujita Y. (2008 ). Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20 1693–1707

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    Raghavendra A. S. Gonugunta V. K. Christmann A. Grill E. (2010 ). ABA perception and signalling. Trends Plant Sci. 15 395–401

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    Rai M. He C. Wu R. (2009 ). Comparative functional analysis of three abiotic stress-inducible promoters in transgenic rice. Transgenic Res. 18 787–799

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    Redillas M. C. Jeong J. S. Kim Y. S. Jung H. Bang S. W. Choi Y. D. (2012 ). The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol. J. 10 792–805

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  61. 61.

    Rusconi F. Simeoni F. Francia P. Cominelli E. Conti L. Riboni M. (2013 ). The Arabidopsis thaliana MYB60 promoter provides a tool for the spatio-temporal control of gene expression in stomatal guard cells. J. Exp. Bot. 64 3361–3371

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    Saint Pierre C. Crossa J. L. Bonnett D. Yamaguchi-Shinozaki K. Reynolds M. P. (2012 ). Phenotyping transgenic wheat for drought resistance. J. Exp. Bot. 63 1799–1808

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    Sakuma Y. Maruyama K. Osakabe Y. Qin F. Seki M. Shinozaki K. (2006a ). Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18 1292–1309

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    Sakuma Y. Maruyama K. Qin F. Osakabe Y. Shinozaki K. Yamaguchi-Shinozaki K. (2006b ). Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl. Acad. Sci. U.S.A. 103 18822–18827

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    Tran L. S. Nakashima K. Sakuma Y. Simpson S. D. Fujita Y. Maruyama K. (2004 ). Isolation 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. Plant Cell 16 2481–2498

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    Vágújfalvi A. Galiba G. Cattivelli L. Dubcovsky J. (2003 ). The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol. Genet. Genomics 269 60–67

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    Weiner J. J. Peterson F. C. Volkman B. F. Cutler S. R. (2010 ). Structural and functional insights into core ABA signaling. Curr. Opin. Plant Biol. 13 495–502

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    Yamaguchi-Shinozaki K. Shinozaki K. (2006 ). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57 781–803

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    Yang M. Xiong L. (2011 ). Isolation and characterization of a drought-inducible promoter Oshox24P in rice. J. Huazhong Agric. Univ. 30 525–531

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    Yi N. Kim Y. S. Jeong M. H. Oh S. J. Jeong J. S. Park S. H. (2010 ). Functional analysis of six drought-inducible promoters in transgenic rice plants throughout all stages of plant growth. Planta 232 743–754

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    Yoshida T. Fujita Y. Sayama H. Kidokoro S. Maruyama K. Mizoi J. (2010 ). AREB1, 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. Plant J. 61 672–685

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