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Deciphering genome-wide WRKY gene family of Triticum aestivum L. and their functional role in response to Abiotic stress

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Abstract

WRKY transcription factors (TFs) act in regulating plant growth and development as well as in response to different stress. Some earlier studies done by individual researchers reported different wheat WRKY TFs. Although, the recently released wheat genome has opened an avenue to investigate wheat WRKYs (TaWRKY) TFs. Prime objective of this study to performed genome-wide classifications of TaWRKYs and their functional annotation. The classification of 107 individual identified characterized sequences of TaWRKY (IICS-TaWRKY) and 160 uncharacterized draft sequences of TaWRKY (UDS-TaWRKY), along with their gene structures and motifs analysis was performed. Along with comparative sequence analysis and microarray analysis was performed to mimic out TaWRKYs functions in response to different abiotic stresses, accompanied by in-vitro validation. The comparative phylogenetic analysis and estimation of Ka/Ks ratio with Triticum urartu, illustrate group based clasifications of TaWRKYs and evolutionary divergences. Furthermore, motif-based and protein-DNA interaction analysis of TaWRKYs helps to identify, their putative function in target DNA recognition sites. Subsequently, results of microarray and comparative sequence analysis provides the evidence of TaWRKYs involved in heat and/or drought stress. Further, in-vitro results validates that TaWRKY014, TaWRKY090 are found to participate in response of drought stress, whereas TaWRKY008, TaWRKY122, and WRKY45 are involved in response of heat and drought stress. These findings can be utilized in developing novel heat and drought-tolerant wheat cultivars using marker-assisted breeding and transgenic development.

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References

  • Agarwal P, Reddy MP, Chikara J (2011) WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol Biol Rep 38(6):3883–3896

    Article  CAS  PubMed  Google Scholar 

  • Bakshi M, Oelmüller R (2014) WRKY transcription factors: Jack of many trades in plants. Plant Signal Behav, 9(2), e27700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res, 42:W252–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brand LH, Fischer NM, Harter K, Kohlbacher O, Wanke D (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res 41(21):9764–9778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4(1):1

    Article  Google Scholar 

  • Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14(3):559–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. BBA 1819(2):120–128

    CAS  PubMed  Google Scholar 

  • Clarke JD (2009) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb Protoc 2009(3):pdb-prot5177

    Article  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Cvetkovska M, Rampitsch C, Bykova N, Xing T (2005) Genomic analysis of MAP kinase cascades in Arabidopsis defense responses. Plant Mol Biol Rep 23(4):331–343

    Article  CAS  Google Scholar 

  • Dai X, Wang Y, Zhang WH (2015) OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Exp Bot 67:erv515

    Google Scholar 

  • de Pater S, Greco V, Pham K, Memelink J, Kijne J (1996) Characterization of a zinc-dependent transcriptional activator from Arabidopsis. Nucleic Acids Res 24(23):4624–4631

    Article  PubMed  PubMed Central  Google Scholar 

  • Diao WP, Snyder JC, Wang SB, Liu JB, Pan BG, Guo GJ, Wei G (2016) Genome-wide identification and expression analysis of WRKY gene family in Capsicum annuum L. Front Plant Sci 7:1727

    Article  Google Scholar 

  • Ding M, Chen J, Jiang Y, Lin L, Cao Y, Wang M, Zhang Y, Rong J, Ye W (2015) Genome-wide investigation and transcriptome analysis of the WRKY gene family in Gossypium. Mol Genet Genomics 290(1):151–171

    Article  CAS  PubMed  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:gkq310

    Article  CAS  Google Scholar 

  • Duan MR, Nan J, Liang YH, Mao P, Lu L, Li L, Wei C, Lai L, Li Y, Su XD (2007) DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Res 35(4):1145–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10(4):366–371

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J 18(17):4689–4699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr Opin Plant Biol 4(4):301–308

    Article  CAS  PubMed  Google Scholar 

  • Goel R, Pandey A, Trivedi PK, Asif MH (2016) Genome-wide analysis of the Musa WRKY gene family: evolution and differential expression during development and stress. Front Plant Sci 7:299

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Jadaun A, Kumar H, Raj U, Varadwaj PK, Rao AR (2015a) Exploration of new drug-like inhibitors for serine/threonine protein phosphatase 5 of Plasmodium falciparum: a docking and simulation study. J Biomol Struct Dyn 33(11):2421–2441

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Rao AR, Varadwaj PK, De S, Mohapatra T (2015b) Extrapolation of inter domain communications and substrate binding cavity of camel HSP70 1A: a molecular modeling and dynamics simulation study. PloS ONE 10(8):e0136630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gupta S, Raj U, Kumar H, Varadwaj PK, Gupta A (2016a) Embryo and endosperm specific comparative transcriptome analysis of triticumaestivum in response to ABA and H2O2 stress. In: Bioinformatics and systems biology (BSB), international conference on IEEE. pp 1–4.

  • Gupta S, Singh Y, Kumar H, Raj U, Rao AR, Varadwaj PK (2016b) Identification of novel abiotic stress proteins in Triticumaestivum through functional annotation of hypothetical proteins. Interdiscip Sci 10:1–16

    Google Scholar 

  • Gupta S, Kumari M, Kumar H, Varadwaj PK (2017a) Genome-wide analysis of miRNAs and Tasi-RNAs in Zea mays in response to phosphate deficiency. Funct Integr Genomics 17:1–17

    Article  CAS  Google Scholar 

  • Gupta S, Yadav BS, Raj U, Freilich S, Varadwaj PK (2017b) Transcriptomic analysis of soil grown T. aestivum cv. root to reveal the changes in expression of genes in response to multiple nutrients deficiency. Front Plant Sci 8:1025

    Article  PubMed  PubMed Central  Google Scholar 

  • Gupta S, Gupta V, Singh V, Varadwaj PK (2018) Extrapolation of significant genes and transcriptional regulatory networks involved in Zea mays in response in UV-B stress. Genes Genomics 40:1–18

    Article  CAS  Google Scholar 

  • Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213(3):469–473

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. https://doi.org/10.1093/bioinformatics/btu817

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics 287(6):495–513

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Li K, Xu X, Yao Z, Jin C, Zhang S (2015) Genome-wide analysis of WRKY transcription factors in white pear (Pyrusbretschneideri) reveals evolution and patterns under drought stress. BMC Genomics 16(1):1

    Article  CAS  Google Scholar 

  • Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14(6):1359–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant Microbe Interact 16(4):295–305

    Article  CAS  PubMed  Google Scholar 

  • Lagacé M, Matton DP (2004) Characterization of a WRKY transcription factor expressed in late torpedo-stage embryos of Solanum chacoense. Planta 219(1):185–189

    Article  PubMed  CAS  Google Scholar 

  • Li MY, Xu ZS, Tian C, Huang Y, Wang F, Xiong AS (2016) Genomic identification of WRKY transcription factors in carrot (Daucuscarota) and analysis of evolution and homologous groups for plants. Sci Rep 6:23101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindemose S, O’Shea C, Jensen MK, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14(3):5842–5878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo M, Dennis ES, Berger F, Peacock WJ, Chaudhury A (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Nat Acad Sci USA 102(48):17531–17536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21(16):3448–3449

    Article  CAS  PubMed  Google Scholar 

  • Meng D, Li Y, Bai Y, Li M, Cheng L (2016) Genome-wide identification and characterization of WRKY transcriptional factor family in apple and analysis of their responses to waterlogging and drought stress. Plant Physiol Biochem 103:71–83

    Article  CAS  PubMed  Google Scholar 

  • Muthamilarasan M, Bonthala VS, Khandelwal R, Jaishankar J, Shweta S, Nawaz K, Prasad M (2015) Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Front Plant Sci 6:910

    PubMed  PubMed Central  Google Scholar 

  • Niu CF, Wei W, Zhou QY, Tian AG, Hao YJ, Zhang WK, Ma B, Lin Q, Zhang ZB, Zhang JS, Chen SY (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant cell environment 35(6):1156–1170

    Article  CAS  Google Scholar 

  • Okay S, Derelli E, Unver T (2014) Transcriptome-wide identification of bread wheat WRKY transcription factors in response to drought stress. Mol Genet Genomics 289(5):765–781

    Article  CAS  PubMed  Google Scholar 

  • Pabo CO, Sauer RT (1992) Transcription factors: structural families and principles of DNA recognition. Ann Rev Biochem 61(1):1053–1095

    Article  CAS  PubMed  Google Scholar 

  • Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150(4):1648–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760

    Article  PubMed  PubMed Central  Google Scholar 

  • Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retamaraetam. Plant J 31(3):319–330

    Article  CAS  PubMed  Google Scholar 

  • Prasad CVSS, Gupta S, Gaponenko A, Dhar M (2012) In-silico comparative study of inhibitory mechanism of plant serine proteinase inhibitors. Bioinformation 8(14):673

    Article  Google Scholar 

  • Prasad CS, Gupta S, Gaponenko A, Tiwari M (2013) Molecular dynamic and docking interaction study of Heterodera glycines serine proteinase with Vigna mungo proteinase inhibitor. Appl Biochem Biotechnol 170(8):1996–2008

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro J, Melo F, Schüller A (2015) PDIviz: analysis and visualization of protein–DNA binding interfaces. Bioinformatics 31(16):2751–2753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15(20):5690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15(5):247–258

    Article  CAS  PubMed  Google Scholar 

  • Satapathy L, Singh D, Ranjan P, Kumar D, Kumar M, Prabhu KV, Mukhopadhyay K (2014) Transcriptome-wide analysis of WRKY transcription factors in wheat and their leaf rust responsive expression profiling. Mol Genet Genomics 289(6):1289–1306

    Article  CAS  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen H, Liu C, Zhang Y, Meng X, Zhou X, Chu C, Wang X (2012) OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol 80(3):241–253

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Gao J (2014) Genome-wide analysis of WRKY gene family in Arabidopsis lyrata and comparison with Arabidopsis thaliana and Populustrichocarpa. Chin Sci Bull 59(8):754–765

    Article  CAS  Google Scholar 

  • Sun L, Wang Y, Liu LL, Wang C, Gan T, Zhang Z, Wang Y, Wang D, Niu M, Long W, Li X (2017) Isolation and characterization of a spotted leaf 32 mutant with early leaf senescence and enhanced defense response in rice. Sci Rep 7:41846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szűcs A, Jäger K, Jurca ME, Fábián A, Bottka S, Zvara Á, … Fehér A (2010) Histological and microarray analysis of the direct effect of water shortage alone or combined with heat on early grain development in wheat (Triticumaestivum). Physiologiaplantarum 140(2):174–188

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Wang F, Hou XL, Wang Z, Huang ZN (2014) Genome-wide fractionation and identification of WRKY transcription factors in Chinese cabbage (Brassica rapa ssp. pekinensis) reveals collinearity and their expression patterns under abiotic and biotic stresses. Plant Mol Biol Rep 32(4):781–795

    Article  CAS  Google Scholar 

  • Tripathi A, Tripathi DK, Chauhan DK, Kumar N, Singh GS (2016) Paradigms of climate change impacts on some major food sources of the world: A review on current knowledge and future prospects. Agr Ecosyst Environ 216:356–373

    Article  Google Scholar 

  • Tuszynska I, Magnus M, Jonak K, Dawson W, Bujnicki JM (2015) NPDock: a web server for protein–nucleic acid docking. Nucleic Acids Res 43:gkv493

    Article  CAS  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 TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco. PloS ONE 8(6):e65120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Xia EH, Gao LZ (2016) Genome-wide analysis of WRKY family of transcription factors in common bean, Phaseolus vulgaris: chromosomal localization, structure, evolution and expression divergence. Plant Gene 5:22–30

    Article  CAS  Google Scholar 

  • Wolfe D, Dudek S, Ritchie MD, Pendergrass SA (2013) Visualizing genomic information across chromosomes with PhenoGram. BioData Mining 6(1):18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12(1):9–26

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Ni Z, Yao Y, Guo G, Sun Q (2008) Cloning and expression profiles of 15 genes encoding WRKY transcription factor in wheat (Triticumaestivem L.). Prog Nat Sci 18(6):697–705

    Article  CAS  Google Scholar 

  • Yamasaki K, Kigawa T, Watanabe S, Inoue M, Yamasaki T, Seki M, Shinozaki K, Yokoyama S (2012) Structural basis for sequence-specific DNA recognition by an Arabidopsis WRKY transcription factor. J Biol Chem 287(10):7683–7691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin G, Xu H, Xiao S, Qin Y, Li Y, Yan Y, Hu Y (2013) The large soybean (Glycine max) WRKY TF family expanded by segmental duplication events and subsequent divergent selection among subgroups. BMC Plant Biol 13(1):148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H, Kaku H (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64(16):5085–5097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang CQ, Xu Y, Lu Y, Yu HX, Gu MH, Liu QQ (2011) The WRKY transcription factor OsWRKY78 regulates stem elongation and seed development in rice. Planta 234(3):541–554

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Fei Z (2014) January.iTAK–Identification and classification of plant transcription factors and protein kinases. In: Plant and animal genome XXII conference.

  • Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48(4):592–605

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, Liu S, Meng C, Qin L, Kong L, Xia G (2013) WRKY transcription factors in wheat and their induction by biotic and abiotic stress. Plant Mol Biol Rep 31(5):1053–1067

    Article  CAS  Google Scholar 

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SG and PKV conceived the work and designed the experiments. SG and SM performed all in-silico and in-vitro experiments. SG, VKM, SM, and PKV analyzed the results. SG, VKM, RR, PKV and RC contributed to writing the manuscript and discussed the results and commented on the manuscript.

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Correspondence to Pritish Kumar Varadwaj.

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This research does not perform any experiment on human and animals. Data used in this work were collected from open sources and all in-vitro data were generated at the Plant Genetics Lab, Banaras Hindu University-Varanasi, India. Hence, the authors declare that there is no compliance with ethical standards.

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Gupta, S., Mishra, V.K., Kumari, S. et al. Deciphering genome-wide WRKY gene family of Triticum aestivum L. and their functional role in response to Abiotic stress. Genes Genom 41, 79–94 (2019). https://doi.org/10.1007/s13258-018-0742-9

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