Molecular responses to drought and cold stress

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<ul><li><p>161 </p><p>Molecular responses to drought and cold stress Kazuo Shinozaki* and Kazuko Yamaguchi-Shinozakif </p><p>A variety of plant genes are induced by drought and cold stress, and they are thought to be involved in the stress tolerance of the plant. At least five signal transduction pathways control these genes: two are dependent on abscisic acid (ABA), and the others are ABA-independent. A novel cis-acting element involved in one of the ABA-independent signal transduction pathways has been identified. In addition, a number of genes for protein kinases and transcription factors thought to be involved in the stress signal transduction cascades have been shown to be induced by environmental stresses. </p><p>Addresses *Laboratory of Plant Molecular Biology, The Institute of Physical and Chemical Research (RIKEN), Tsukuba Life Science Center, 3-1-1 Koyadai, Tsukuba, Ibaraki 305, Japan; e-maih sinozaki@rtc.riken.go.jp tBiological Resources Division, Japan International Research Center for Agricultural Sciences (JIRCAS), Ministry of Agriculture, Forestry and Fisheries, 2-10hwashi, Tsukuba, Ibaraki 305, Japan </p><p>Current Opinion in Biotechnology 1996, 7:161-167 </p><p> Current Biology Ltd ISSN 0958-1669 </p><p>Abbreviations ABA abscisic acid ABRE ABA-responsive element bZlP basic region leucine zipper CDPK Ca2+-dependent protein kinase DRE dehydration-responsive element LTRE low temperature responsive element MAPK mitogen-activated protein kinase MAPKK MAPK kinase MAPKKK MAPKK kinase P5C A 1 -pyrrolin e-5-carboxylate SH Src-homology </p><p>I n t roduct ion Plants respond to conditions of drought or cold stress through a number of physiological and developmental changes. Many genes that respond to drought or cold stress at the transcriptional level have been described recently [1-3]. The majority have been shown to be induced by both drought and cold stress, but some are responsive only to drought and others only to cold stress [2,3]. The molecular responses of plant genes to drought or cold stress raise several interesting questions. How do plant cells sense the loss of water or the decrease of temperature? How are the stress signals transduced into cellular signals and transmitted to the nucleus? How is gene transcription affected by these stress signals? And, finally, how do the gene products function in stress tole rance ? </p><p>Abscisic acid (ABA) is produced under such environmental stresses, and it is important in the tolerance of plants </p><p>to drought, high salinity, and cold [4]. Many genes that respond to drought and/or cold stress are also induced by the exogenous application of ABA [1,2,4,5]. It appears that dehydration triggers the production of ABA, which, in turn, induces various genes. Cis-acting and trans-acting factors involved in ABA-induced gene expression have been extensively analyzed [2,5,6]. </p><p>Several reports have described genes that are induced by drought and cold stress, but are not responsive to exoge- nous ABA treatments [2,3,5]. These findings suggest the existence of both ABA-independent and ABA-dependent signal-transduction cascades between the initial signal of drought or cold stress and the expression of specific genes. Analyses of the promoters of drought-inducible and cold-inducible genes have revealed a novel cis-acting element that is involved in the ABA-independent response to conditions of dehydration, low temperature, or high salt [7]. </p><p>Several genes encoding factors involved in signal transduc- tion cascades, such as protein kinases, transcription factors, and phospholipase C, are induced by drought and cold stress; this suggests that these factors may function in the signal transduction pathways between initial water stress signals and gene expression. The present review focuses both on recent progress in the study of the expression of drought-inducible and cold-inducible genes and on the signal transduction cascades under such environmental stresses. </p><p>Funct ion o f d rought /co ld s t ress induc ib le genes Many genes have been demonstrated to respond to drought and/or cold stress in various plant species. Functions for a lot of the encoded products have been predicted from sequence homology with known functional proteins. Genes induced under stress conditions are thought to function in protecting cells from water deficit or temperature change by the production of several different gene products: water channel proteins involved in altering cellular water potential [2,8-12]; the enzymes required for the biosynthesis of various osmoprotectants such as sugars, proline and betaine [2,11-13,14",15,16]; lipid desaturases for membrane modification [2,3,11,12]; protective proteins such as late embryogenesis abundant (LEA) proteins, osmotin, antifreeze proteins, chaperones, and mRNA-binding proteins [2,3,11,12,17,18]; thiol pro- teases, Clp protease, and ubiquitin, which are required for protein turnover [2,11,12,18,19,20]; the detoxifica- tion proteins, such as glutathione S-transferase, soluble epoxide hydrolase, catalase, and ascorbate peroxidase [2,11,12,21,22",23"]; and protein kinases, phospholipase C, and transcription factors, which are involved in further </p></li><li><p>162 Plant biotechnology </p><p>regulation of signal transduction and gene expression [2,11,24",25,26,27,28-30,31"]. Some stress-inducible genes have been over-expressed in transgenic plants, pro- ducing a stress-tolerant phenotype of the plant, indicating that the gene products function in stress tolerance. Some stress-inducible genes do not always function in stress tolerance, however. The functions of the genes induced by drought, high salinity and cold stress have been reviewed [2,3,11-13]. Original reports that have appeared in 1994 and 1995 are cited in this review. </p><p>Regulation of gene expression by drought and cold stress Most of the drought-inducible genes also respond to high-salinity stress, but some of them do not respond to cold stress, and vice versa [2,3]. The expression patterns of genes induced by drought and cold stress were analyzed by northern blot analysis. Results indicate broad variations in the timing of induction of these genes and that some genes respond to ABA, whereas others do not [32-34]. ABA-deficient mutants were used to analyze cold-inducible and drought-inducible genes that respond to ABA [2,3]. Several genes were induced by exogenous ABA treatment, but they were also induced by cold or drought in ABA-deficient (aba) or ABA-insensitive (abt) Arabidopsis mutants. These observations indicate that these genes do not require an accumulation of endogenous ABA under cold or drought conditions, but do respond to ABA [2,3,19,34-37]. Analysis of the expression of ABA-inducible genes showed that several </p><p>Figure 1 </p><p>genes require protein biosynthesis for their induction by ABA, suggesting that at least two independent pathways exist between the production of endogenous ABA and gene expression under stress conditions [38]. </p><p>As shown in Figure 1, at least three independent signal pathways function under drought conditions [39]: two are ABA-dependent (pathways II and III) and one is ABA-independent (pathway IV). There are also at least two independent cold stress signal transduction pathways [19,34-36]: one is ABA-dependent (pathway III) and the other is ABA-independent (pathway IV). These pathways overlap with those of the drought response [5,19,34-36]. In addition, two other signal transduction pathways may function only in drought response (pathway I) or in cold response (pathway V) [40,41]. Therefore, at least five independent signal transduction pathways mediate drought or cold responses (Fig. 1). The existence of complex signal transduction pathways in the responses of plants to drought and cold stress is strong evidence of a molecular basis for these complex physiological responses. </p><p>Absc is ic acid respons ive gene express ion under drought and cold st ress The levels of endogenous ABA increase significantly in many plants under drought and high-salinity conditions [4]. ABA levels also increase, at least transiently, in response to low-temperature stress [3,42]. Many drought- inducible and cold-inducible genes are induced by ex- ogenous ABA treatment. These genes contain potential </p><p>Signal transduction pathways between initial drought-stress and/or cold-stress signals and gene expression. At least five signal transduction pathways exist (I-V): two are ABA-dependent (11 and III), and three are ABA-independent (I, IV and V). Protein synthesis is required in one of the ABA-dependent pathways (11). There are at least four signaling pathways (I, II, III and IV) that function under drought conditions (indicated by solid arrows), and three pathways (111, IV and V) that function under cold stress (indicated by dashed arrows). ABRE is involved in one of the ABA-dependent pathways (111), and DRE is involved in one of the ABA-independent pathways (IV). (See text for further details.) </p><p>ii i" </p><p>~i i i i i ~ iii~ III </p><p>? </p><p>0 [l </p><p>ABRE DRE Gene expression </p><p>Temperature change </p><p>D D D D B </p><p>? </p><p>D </p><p> t 996 Current Opinion in Biotechnology </p></li><li><p>Molecular responses to drought and cold stress $hinozaki and Yamaguchi-Shinozaki 163 </p><p>ABA-responsive elements (ABREs) in their promoter regions [2,3]. The ABRE (PyACGTGGC, where Py is a pyrimidine) functions as a c/s-acting DNA element involved in ABA-regulated gene expression [5,6]. The G box resembles the ABRE motif and functions in the regulation of plant genes in a variety of environmental conditions, such as red light, UV light, anaerobiosis, and wounding. Recently, nucleotides around the ACGT core motif have been shown to be involved in determining the binding specificity of basic region leucine zipper (bZIP) protein [5,6]. Furthermore, a coupling element is required to specify the function of the ABRE, constituting an ABA-responsive complex [43**]. </p><p>The induction of an Arabidopsis drought-inducible gene, rd22, is mediated by ABA, but requires protein biosynthe- sis for its ABA-dependent expression [38]. A 67 bp region of the rd22 promoter is essential for its ABA-responsive expression and contains several conserved motifs of DNA-binding proteins, such as MYC and MYB, but no ABREs [39*]. Recently, a cDNA for a transcription factor MYC homolog has been cloned by the south-western method, using the 67 bp DNA as a probe. This suggests that a drought-inducible MYC homolog may function in the ABA-inducible expression of rd22 (H Abe, K Yamaguchi-Shinozaki, K Shinozaki, unpublished data). A promoter region has been identified that functions in ABA-inducible expression of the CDeT27-45 gene in Craterostigma plantagineum [44*]. In addition, an ABA- inducible DNA-binding activity to this region was de- tected in nuclear extracts. These results indicate that drought-inducible or ABA-inducible transcription factors may function in the ABA-responsive gene expression un- der drought stress and that two independent transcription systems mediate ABA-responsive gene expression: one is controlled by ABA directly through ABRE, and the other may require de novo synthesis of ABA-inducible transcription factors. </p><p>Abscisic acid independent gene expression under drought and cold stress Several genes are induced by both cold and drought in aba or abi Arabidopsis mutants. This suggests that these genes do not require ABA for their expression under cold or drought conditions, but do respond to ABA [19,34-37]. These genes include rd29A (also termed lti78 and cor78), kin1, cor6.6 (kin2), and cor47 (rd17) [3]. Among these genes, the expression of a drought-inducible gene for rd29A/lti78/cor78 was analyzed [36,45,46]. Two genes, rd29A and rd29B/lti65, were found to be located in tandem in an 8 kbp region of the Arabidopsis genome and encode hydrophilic proteins [36,45]. The transcription of rd29A in Arabidopsis abil and abal mutants suggests that cold-regulated and drought-regulated expression does not require ABA. These observations indicate that at least two separate regulatory systems function in gene expression during drought and cold stress. One of the cis-acting elements responsible for the dehydration-induced and </p><p>cold-induced expression of rd29A was identified at the nucleotide sequence level in transgenic plants [7**]. </p><p>A 9bp conserved sequence, TACCGACAT, termed the dehydration-responsive element (DRE), is essential for the regulation of the induction of rd29A under drought, low-temperature, and high-salt stress conditions, but does not function as an ABRE. The DRE sequence is not found in the rd29B promoter, which responds to ABA treatment, but not to cold stress [7*]. Nordin et al. [451 reported conserved motifs (ACCGACA), including the DRE, as putative low-temperature responsive elements. DRE-related motifs have been reported in the promoter regions of cold-inducible and drought-inducible genes such as kinl, cor6.6, and cor47/rdl 7 [7,47]. Baker et al. [48] also reported a similar motif (C-repeat; TGGCCGAC) in the promoter region of cold-inducible cor15a [48]. The 5bp CCGAC core sequence was found in the promoter regions of the cold-inducible Brassica gene, BNllS, and designated the low temperature responsive element (LTRE) [49]. These results suggest that DRE- related motifs are involved in drought-responsive and cold-responsive, but ABA-independent, gene expression. A protein factor that specifically interacts with the 9bp DRE sequence was detected in nuclear extract prepared from either dehydrated or untreated Arabidopsis plants [7]. Cloning of the cDNA for a DRE-binding protein is in progress; this should provide a better understanding of the regulation of drought-inducible and cold-inducible genes. </p><p>Genes for transcription factors that are induced by drought or cold stress In higher plants, genes for several transcription factors have been shown to be induced by environmental stresses or signals. These include genes encoding MYB-related and bZIP-related transcription factors. A cDNA, designated Atmyb2, that encodes an MYB-related protein was cloned by screening a cDNA library prepared from dehydrated Arabidopsis plants [29]. The Atmyb2 gene is rapidly induced by dehydration stress. High-salt conditions and the application of exogenous ABA also result in the induction of Atmyb2, although Atmyb2 does not respond to cold or heat stress. Bacterially expressed ATMYB2 protein binds to the MYB recognition sequence, which suggests that the drought-inducible MYB homolog can also control drought-inducible and ABA-inducible gene expression. </p><p>Kusano and colleagues [30,31 ] have isolated a cold- inducible gene encoding a bZIP transcription factor from rice (lipl9) and maize (mliplS) plants. These genes also respond to high salt and to exogenous ABA treatment. The mLipl5 protein can bind to the hexamer sequence, ACGTCA, and to a G-box-like sequence. The mLipl5 protein binds to the promoter region of the cold-inducible alcohol dehydrogenase gene in maize [31]. These stress-inducible transcription factors are thought to function in the regulation...</p></li></ul>

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