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Wheat WRKY Type Transcription Factor Gene TaWRKY1 is Essential in Mediating Drought Tolerance Associated with an ABA-Dependent Pathway

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Abstract

WRKY-type transcription factors (TFs) are important regulators in plant growth, development and responses to diverse biotic and abiotic stresses. In this study, we characterized the function of TaWRKY1, a wheat (Triticum aestivum) WRKY family gene, in mediating plant tolerance to drought. TaWRKY1 bears a conserved WRKY motif and a C2H2 domain and targets onto the nucleus under both normal and simulated drought conditions. On exposure to simulated drought and ABA, the TaWRKY1 expression levels were significantly up-regulated. Ectopic overexpression of TaWRKY1 in tobacco conferred improved tolerance to drought; the transgenic plants exhibited more biomass, slower leaf water loss rate (WLR), more osmolyte accumulation, and higher antioxidant enzyme activities than wild type (WT) plants after drought treatments. In addition, the stomata closure rate was promoted in the transgenic plants upon exposure to drought and -exogenous ABA with respect to that in WT plants, suggesting that TaWRKY1 mediates the stomata movement and impacts the leaf water retention capacity. The transcripts of NtPYL8, an ABA receptor gene in tobacco, were shown to be induced in the TaWRKY1-overexpressing plants under drought and ABA stresses. Moreover, overexpression and knockdown of NtPYL8 modified the stomata movement characterization, leaf WLR, and phenotype of the seedlings upon exposure to the drought stress. These findings suggest that NtPYL8 acts as one of the critical players in transducing ABA signaling initiated by osmotic stress, contributing to the TaWRKY1-mediated drought tolerance via regulating stomata movement and plant water retention capacity. Our findings together reveal that TaWRKY1 plays an important role in mediating the plant tolerance to drought through modification of a set of osmotic stress-defensive processes connecting an ABA-dependent pathway. NtPYL8 and its homolog in wheat are crucial members in transducing the drought-initiated ABA signaling and are functional in modulating stomata movement.

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References

  • Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21:3554–3366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174

    Article  CAS  PubMed  Google Scholar 

  • Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structure clues into WRKY-domain function. Plant Mol Biol 68:81–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the reces-sive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci U S A 99:2404–2409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du X, Zhao X, Liu X, Guo C, Lu W, Gu J, Xiao K (2013) Overexpression of TaSRK2C1, wheat SNF1-related protein kinase gene, increases tolerance to dehydration, salt, and low temperature in transgenic tobacco. Plant Mol Biol Rep 31:810–821

    Article  CAS  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcrip-tion factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Feng L, Gao Z, Xiao G, Huang R, Zhang H (2014) Leucine-rich repeat receptor-like kinase FON1 regulated drought stress and seed germination by activating the expression of ABA-responsive genes in rice. Plant Mol Biol Rep 32:1158–1168

    Article  CAS  Google Scholar 

  • Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391

    Article  CAS  PubMed  Google Scholar 

  • Guo C, Zhao X, Liu X, Zhang L, Gu J, Li X, Lu W, Xiao K (2013) Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237:1163–1178

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert H (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and beta-amylase from sweet potato. Mol Gen Genet 244:563–571

    Article  CAS  PubMed  Google Scholar 

  • Jia H, Wang C, Wang F, Liu S, Li G, Guo X (2015) GhWRKY68 reduces resistance to salt and drought in transgenic Nicotiana benthamiana. Plos ONE. doi:10.1371/journal.pone.0120646

    Google Scholar 

  • Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105

    Article  CAS  PubMed  Google Scholar 

  • Kim T, Bohmer M, Hu H, Nishimura N, Schroeder J (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kline KG, Sussman MR, Jones AM (2010) Abscisic acid receptors. Plant Physiol 154:479–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee BH, Henderson DA, Zhu JK (2005) TheArabidopsis cold responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Fu Q, Huang W, Yu D (2009) Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Rep 28:683–693

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Liu Z, Wang J, Li X, Yang Y (2015) The Arabidopsis Kelch Repeat F-box E3 ligase APKP1 plays a positive role for the regulation of abscisic acid signaling. Plant Mol Biol Rep. doi:10.1007/s11105-015-0942-2

    PubMed  Google Scholar 

  • Liang YC, Chen Q, Liu Q, Zhang W, Ding R (2003) Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). J Plant Physiol 160:1157–1164

    Article  CAS  PubMed  Google Scholar 

  • Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • Mangelsen E, Kilian J, Berendzen KW, Kolukisaoglu UH, Harter K, Jansson C, Wanke D (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics 9:194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu C, Wei W, Zhou Q, Tian A, Hao Y, Zhang W, Ma B, Lin Q, Zhang Z, Zhang J, Che S (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Environ 35:1156–1170

    Article  CAS  PubMed  Google Scholar 

  • Pandey SP, Somssich IE (2009) The role of WRKY tran-scription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder I (1997) Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 9:409–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Proietti S, Bertini L, Vander Ent S, Leon-Reyes A, Pieterse CMJ (2011) Cross activity of orthologous WRKY transcription factors in wheat and Arabidopsis. J Exp Bot 62:1975–1990

    Article  CAS  PubMed  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  CAS  PubMed  Google Scholar 

  • Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ram-achandran S (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 49:865–879

    Article  CAS  PubMed  Google Scholar 

  • Rushton PJ, Macdonald H, Huttly AK, Lazarus CM, Hooley R (1995) Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of alpha-Amy 2 genes. Plant Mol Biol 29:691–702

    Article  CAS  PubMed  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shionzaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Yu D (2015) Activated expression of AtWRKY53 negatively regulates drought tolerance by mediating stomatal movement. Plant Cell Rep 34:1295–1306

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Ding C, Li X, Xiao K (2012) Molecular characterization and expression analysis of TaZFP15, a C2H2- type zinc finger transcription factor gene in wheat (Triticum aestivum L.). J Integr Agric 11:31–42

    Article  CAS  Google Scholar 

  • Thu NBA, Hoang XLT, Nguyen TH (2015) Differential expression of two-component system-related drought-responsive gens in two contrasting drought-tolerant soybean cultivars DT51 and MTD720 under well-watered and drought conditions. Plant Mol Biol Rep 33:1599–1610

    Article  CAS  Google Scholar 

  • Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Verk MC, Pappaioannou D, Neeleman L, Bol JF, Linthorst HJM (2008) A novel WRKY transcription factor is required for induction of PR-1a gene expression by salicylic acid and bacterial elicitors. Plant Physiol 146:1983–1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vavasseur A, Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytol 165:65–682

    Article  CAS  Google Scholar 

  • Vlad F, Rubio S, Rodrigues A, Sirichandra C, Belin C, Robert N, Leung J, Rodriguez PL, Laurière C, Merlot S (2009) Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21:3170–3184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Deng P, Chen L, Wang X, Ma H, Hu W, Yao N, Feng Y, Chai R, Yang G, He G (2013) A wheat WRKY transcription factor TaWRKY1 0 confers tolerance to multiple abiotic stresses in transgenic tobacco. Plos ONE 8(6), e65120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiang Y, Huang Y, Xiong L (2007) Characterization of stress responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137:176–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165–S183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XP, Chen CH, Fan BF, Chen ZX (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang PZ, Chen CH, Wang ZP, Fan BF, Chen ZX (1999) A pathogen- and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J 18:141–149

    Article  CAS  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu QS, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20:1134–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YJ, Wang LJ (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6:486–503

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31371618 and 31201674) the National Transgenic Major Program (No. 2011ZX08008) and the Key Laboratory of Crop Growth Regulation of Hebei Province.

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    Authors and Affiliations

    1. College of Life Sciences, Agricultural University of Hebei, Baoding, China, 071001

      Weiwei Ding, Weibo Fang & Xiaojuan Li

    2. College of Agronomy, Agricultural University of Hebei, Baoding, China, 071001

      Shuya Shi, Yuanyuan Zhao & Kai Xiao

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    1. Weiwei Ding
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    Weiwei Ding and Weibo Fang contributed equally to this work.

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    Ding, W., Fang, W., Shi, S. et al. Wheat WRKY Type Transcription Factor Gene TaWRKY1 is Essential in Mediating Drought Tolerance Associated with an ABA-Dependent Pathway. Plant Mol Biol Rep 34, 1111–1126 (2016). https://doi.org/10.1007/s11105-016-0991-1

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