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Molecular characterization and expression analysis of WRKY family genes in Dendrobium officinale

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Abstract

The WRKY family of transcription factors is one of the most important families of plant transcriptional regulators, and the members regulate multiple biological processes. However, there is limited information on WRKYs in Dendrobium officinale. In this study, 52 WRKY family genes of D. officinale were surveyed for the first time. Conserved domain, phylogenetic, exon–intron construction, and expression analyses were performed for the DoWRKY genes. Two major types of intron splicing (PR and VQR introns) were found, and the intron insertion position was observed to be relatively conserved in the conserved DoWRKY domains. The expression profiles of nine DoWRKYs were analyzed in cold- and methyl jasmonate (MeJA)-treated D. officinale seedlings; the DoWRKYs showed significant expression changes at different levels, which suggested their vital roles in stress tolerance. Moreover, the expression trends of most of the DoWRKYs after the simultaneous cold stress and MeJA treatment were the opposite of those of DoWRKYs after the individual cold stress and MeJA treatments, suggesting that the two stresses might have antagonistic effects and affect the adaptive capacity of the plants to stresses. Twelve DoWRKY genes were differentially expressed between symbiotic and asymbiotic germinated seeds; all were upregulated in the symbiotic germinated seeds except DoWRKY16. These differences in expression of DoWRKYs might be involved in promoting in vitro symbiotic germination of seeds with Tulasnella-like fungi. Our findings will be useful for further studies on the WRKY family genes in orchids.

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References

  • An Y, Hen Y, Wu L, Zhang Z (2006) A change of phenolic acids content in poplar leaves induced by methyl salicylate and methyl jasmonate. J Forest Res 17:107–110

    Article  CAS  Google Scholar 

  • Bencke-Malato M, Cabreira C, Wiebke-Strohm B, Bücker-Neto L, Mancini E, Osorio MB, Homrich MS, Turchetto-Zolet AC, De Carvalho MC, Stolf R et al (2014) Genome-wide annotation of the soybean WRKY family and functional characterization of genes involved in response to Phakopsora pachyrhizi infection. BMC Plant Biol 14:236

    Article  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 41:1–15

    Article  Google Scholar 

  • Consortium TIBG (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–717

    Google Scholar 

  • Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PLoS ONE 11:e111988

    Article  Google Scholar 

  • Diao W, Snyder J, Wang SB, Liu JB, Pan BG, Guo G, Wei G (2016) Genome-wide identification and expression analysis of WRKY gene family in Capsicum annuum L. Front Plant Sci 7:1–15

    Article  Google Scholar 

  • Dou F, Xuan W, Huang Z, Deng F, Tan X (2009) Effects of MeJA on cold tolerance of banana seedlings. J Fruit Sci 26:390–393

    Google Scholar 

  • Dou L, Zhang X, Pang C, Song M, Wei H, Fan S, Yu S (2014) Genome-wide analysis of the WRKY gene family in cotton. Mol Genet Genomics 289:1103–1121

    Article  CAS  PubMed  Google Scholar 

  • Duan X, Deng Z, Bin J (2009) Efects of Methyl Jasmonate on cold resistance of rice (Oryza sativa L.) seedlings. Plant Physiol Commun 45:881–884

    CAS  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 

  • Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F (2012) Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo a massive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69:510–528

    Article  CAS  PubMed  Google Scholar 

  • Guan L, Chi W, Xiao W, Chen L, He S (2014) Analysis of hypoxia-inducible factor alpha polyploidization reveals adaptation to Tibetan plateau in the evolution of schizothoracine fish. BMC Evol Biol 14:192

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo X, Li Y, Li C, Luo H, Wang L, Qian J, Luo X, Xiang L, Song J, Sun C, Xu H, Yao H, Chen S (2013) Analysis of the Dendrobium officinale transcriptome reveals putative alkaloid biosynthetic. Gene 527:131–138

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Liu Y (2013) Genome-wide analysis of WRKY transcription factors in Solanum tuberosum. Chin J Appl Environ Biol 19:205–214

    Article  CAS  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 287:495–513

    Article  CAS  PubMed  Google Scholar 

  • Hung KT, Hsu YT, Kao CH (2006) Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol Plantarum 127:293–303

    Article  CAS  Google Scholar 

  • Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Di Fan, Luo K (2014) Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot 65:1–16

    Article  Google Scholar 

  • Jiang Y, Zhu Y, Gao Y, Si J (2016) Cloning and expression analysis of WRKY5 gene in Dendrobium officinale. Chin Tradit Herbal Drugs 47:301–308

    CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucl Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Zhang L, Guo D, Li C, Peng S (2012) Identification and expression profiles of the WRKY transcription factor family in Ricinus communis. Gene 503:248–253

    Article  CAS  PubMed  Google Scholar 

  • Li X, Luo J, Yan T, Xiang L, Jin F, Qin D, Sun C, Xie M (2013) Deep sequencing-based analysis of the Cymbidium ensifolium floral transcriptome. PLoS ONE 12:e85480

    Article  Google Scholar 

  • Li H, Guo D, Yang Z, Tang X, Peng S (2014) Genome-wide identification and characterization of WRKY gene family in Hevea brasiliensis. Genomics 104:14–23

    Article  CAS  PubMed  Google Scholar 

  • Ling J, Jiang W, Zhang Y, Yu H, Mao Z, Gu X, Huang S, Xie B (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics 12:471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XQ, Zhu JJ, Wei CJ, Guo Q, Bian CK, Xing ZH, Zhao AC (2015) Genome-wide identification and characterization of the DREB transcription factor gene family in mulberry. Biol Plantarum 59:253–265

    Article  CAS  Google Scholar 

  • Ma J, Lu J, Xu J, Duan B, He X, Liu J (2015) Genome-wide identification of WRKY genes in the desert poplar Populus euphratica and adaptive evolution of the genes in response to salt stress. Evol Bioinform 11:47–55

    Article  Google Scholar 

  • Mangelsen E, Kilian J, Berendzen KW, Kolukisaoglu ÜH, 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  PubMed  PubMed Central  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 

  • Park CY, Lee JH, Yoo JH, Moon BC, Choi MS, Kang YH, Lee SM, Kim HS, Kang KY, Chung WS, Lima CO, Cho MJ (2005) WRKY group IId transcription factors interact with calmodulin. FEBS 579:1545–1550

    Article  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time PCR. Nucl Acids Res 29(9):e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi F, Li J, Duan L, Li Z (2006) Inductions of coronatine and MeJA to low-temperature resistance of wheat seedlings. Acta Bot Boreal-Occident Sin 26:1776–1780

    CAS  Google Scholar 

  • Rao G, Sui J, Zhang J (2015) In silico genome-wide analysis of the WRKY gene family in Salix Arbutifolia. Plant Omics 4:353–360

    Google Scholar 

  • Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 6:827–842

    Article  Google Scholar 

  • Rossberg M, Theres K, Acarkan A, Herrero R, Schmitt T, Schumacher K, Schmitz G, Schmidt R (2001) Comparative sequence analysis reveals extensive microcolinearity in the lateral suppressor regions of the tomato, Arabidopsis, and Capsella genomes. Plant cell 13:979–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savkur RS, Burris TP (2004) The coactivator LXXLL nuclear receptor recognition motif. J Pept Res 63:207–212

    Article  CAS  PubMed  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Stewart S, Zetter L (2002) Symbiotic germination of three semiaquatic rein orchids (Habenaria repens, H. quinquiseta, H. macroceratitis) from florida. Aquat Bot 72:25–35

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony. Mol Biol Evol 11:2731–2739

    Article  Google Scholar 

  • Tang J, Wang F, Hou X, Wang Z, Huang Z (2013) 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 32:781–795

    Article  Google Scholar 

  • Tripathi P, Rabara RC, Langum TJ, Boken AK, Rushton DL, Boomsma DD, Rinerson CI, Rabara J, Reese RN, Chen X, Rohila JS, Rushton PJ (2012) The WRKY transcription factor family in Brachypodium distachyon. BMC Genomics 13:270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verger A, Perdomo J, Crossley M (2003) Modification with SUMO, a role in transcriptional regulation. EMBO Rep 4:137–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C (2013) Cloning and preliminary function analysis of DnWRKY29 gene. Dissertation, Hangzhou Normal University

  • Wang L, Zhu W, Fang LC, Sun XM, Su LY, Liang ZC, Wang N, Londo JP, Li SH, Xin HP (2014) Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biol 14:103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Jina M, Paek K, Piao X, Lian M (2016) An efficient strategy for enhancement of bioactive compounds by protocorm-like body culture of Dendrobium candidum. Ind Crop Prod 84:121–130

    Article  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot-London 100:681–697

    Article  CAS  Google Scholar 

  • Wasternack C (2014) Action of jasmonates in plant stress responses and development applied aspects. Biotechnol Adv 32:31

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C, Strnad M (2015) Jasmonate signaling in plant stress responses and development-active and inactive compounds. New Biotechnol 33:604–613

    Article  Google Scholar 

  • Wei K, Chen J, Chen Y, Wu L, Xie D (2012) Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize. DNA Res 15:153–164

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Zhang Z, 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 W, Xu X, Zhang L, Wu P, Chen Y, Li M, Jiang H, Wu G (2013) Genome wide analysis of the WRKY gene family in physic nut (Jatropha carcas). Gene 524:124–132

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Pan Y, Wang C, Ying Q, Song H, Wang H (2014) Overexpression of DnWRKY11 enhanced salt and drought stress tolerance of transgenic tobacco. Biologia 69:994–1000

    Article  CAS  Google Scholar 

  • Xu L, Tian JN, Wang T, Li LB (2017) Symbiosis established between orchid and Tulasnella spp. Fungi. China J Nucl Agric Sci 31:0876–0883

    Google Scholar 

  • Yan L, Wang X, Liu H, Tian Y, Lian J, Yang R, Hao S, Wang X, Yang S, Li Q et al (2015) The genome of Dendrobium officinale illuminates the biology of the important traditional Chinese orchid herb. Mol Plant 8:922–934

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Galanis A, Witty J, Sharrocks AD (2006) An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J 25:5083–5093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Feng JC (2014) Identification and characterization of the grape WRKY Family. Biomed Res Int 2014:1–14

    Google Scholar 

  • Zhang G, Zhao MM, Zhang Dw, Guo SX (2013) Reference gene selection for real-time quantitative PCR analysis of Dendrobium officinale. Chin Pharm J 48:1664–1668

    CAS  Google Scholar 

  • Zhang G, Xu Q, Bian C, Tsai W, Yeh C, Liu K, Yoshida K, Zhang L, Chang S, Chen F (2016a) The Dendrobium catenatum Lindl. genome sequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Scientific Rep 6:19029

    Article  CAS  Google Scholar 

  • Zhang J, He C, Wu K, Silva JATD, Zeng S, Zhang X, Yu Z, Xia H, Duan J (2016b) Transcriptome analysis of Dendrobium officinale and its application to the identification of genes associated with polysaccharide synthesis. Front Plant Sci 5:1–14

    Google Scholar 

  • Zhao MM, Zhang G, Zhang DW, HsiaoYY, Guo SX (2013) ESTs analysis reveals putative genes involved in symbiotic seed germination in Dendrobium officinale. PLoS ONE 8:e72705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X, Yang J, Liu S, Chen C, Zhu H, Cao J (2014a) The colonization patterns of different fungi on roots of Cymbidium hybridum plantlets and their respective inoculation effects on growth and nutrient uptake of orchid plantlet. World J Microb Biot 30:1993–2003

    Article  CAS  Google Scholar 

  • Zhao XL, Zhang JX, Chen CL, Yang JZ, Zhu HY, Liu M, Lv FB (2014b) Deep sequencing-based comparative transcriptional profiles of Cymbidium hybridum roots in response to mycorrhizal and non-mycorrhizal beneficial fungi. BMC Genomics 15:747

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Meng CC, Zhao YF, Wang CX, Fan HH, Jin Q, Li DH, Lin Y, Cai YP (2015a) Cloning and expression analysis of transcription factor gene (DoWRKY2) in Dendrobium officinal. J Agr Biotechnol 23:1049–1057

    CAS  Google Scholar 

  • Zhao J, Sun SW, Meng CC, Jin Q, Fan HH, Lin Y, Cai YP (2015b) Cloning and expression analysis of transcription factor gene DoWRKY1 in Dendrobium officinal. China J Chin Materia Med 40:2807–2813

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zou Q, Zhu K, Liu H, Zhou J, Ma G (2011) Effect of exogenous Methyl Jasmonate on chlorophyll fluorescence and antioxidant characteristics in the leaves of phalaenopsis amabilis under abiotic stress. J Plant Physiol 47:913–917

    CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the National High Technology Research and Development Program of China (863 Program) (No. 2013AA102607).

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Correspondence to Lubin Li.

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The authors declare that they have no conflict of interest. Tao Wang declares that she has no conflict of interest. Zheng Song declares that he has no conflict of interest. Li Wei declares that she has no conflict of interest. Lubin Li declares that he has no conflict of interest.

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Wang, T., Song, Z., Wei, L. et al. Molecular characterization and expression analysis of WRKY family genes in Dendrobium officinale . Genes Genom 40, 265–279 (2018). https://doi.org/10.1007/s13258-017-0602-z

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