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OsWRKY51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas oryzae pv. oryzae

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OsWRKY51 functions as a positive transcriptional regulator in defense signaling against Xanthomonas oryzae pv. oryzae by direct DNA binding to the promoter of defense related gene, OsPR10a.

Abstract

OsWRKY51 in rice (Oryza sativa L.) is induced by exogenous salicylic acid (SA) and inoculation with Xanthomonas oryzae pv. oryzae (Xoo). To examine the role of OsWRKY51 in the defense response of rice, we generated OsWRKY51 overexpressing and underexpressing transgenic rice plants. OsWRKY51-overexpressing transgenic rice lines were more resistant to Xoo and showed greater expression of defense-related genes than wild-type (WT) plants, while OsWRKY51-underexpressing lines were more susceptible to Xoo and showed less expression of defense-associated genes than WT plants. Transgenic lines overexpressing OsWRKY51 showed growth retardation compared to WT plants. In contrast, transgenic lines underexpressing OsWRKY51 by RNA interference showed similar plant height with WT plants. Transient expression of OsWRKY51-green fluorescent protein fusion protein in rice protoplasts revealed that OsWRKY51 was localized in the nucleus. OsWRKY51 bound to the W-box and WLE1 elements of the OsPR10a promoter. Based on these results, we suggest that OsWRKY51 is a positive transcriptional regulator of defense signaling and has direct DNA binding ability to the promoter of OsPR10a, although it is reported to be a negative regulator in GA signaling.

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References

  • Abbruscato P, Nepusz T, Mizzi L, Del Corvo M, Morandini P, Fumasoni I, Michel C, Paccanaro A, Guiderdoni E, Schaffrath U, Morel JB, Piffanelli P, Faivre-Rampant O (2012) OsWRKY22, a monocot WRKY gene, plays a role in the resistance response to blast. Mol Plant Pathol 13:828–841

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee A, Roychoudhury A (2015) WRKY proteins: signaling and regulation of expression during abiotic stress responses. Sci World J 2015:807560

    Article  Google Scholar 

  • Borun F, Yang S, Du H, Hou X, Zhang J, Liu H, Huang Y (2012) Molecular characterization and functional analysis of plant WRKY genes. Afr J Biotechnol 11:13606–13613

    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. Biochim Biophys Acta 1819:120–128

    Article  CAS  PubMed  Google Scholar 

  • Chi Y, Yang Y, Zhou Y, Zhou J, Fan B, Yu JQ, Chen Z (2013) Protein-protein interactions in the regulation of WRKY transcription factors. Mol Plant 6:287–300

    Article  CAS  PubMed  Google Scholar 

  • Choi C, Hwang SH, Fang IR, Kwon SI, Park SR, Ahn I, Kim JB, Hwang DJ (2015) Molecular characterization of Oryza sativa WRKY6, which binds to W-box-like element 1 of the Oryza sativa pathogenesis-related (PR) 10a promoter and confers reduced susceptibility to pathogens. New Phytol 208:846–859

    Article  CAS  PubMed  Google Scholar 

  • Chujo T, Takai R, Akimoto-Tomiyama C, Ando S, Minami E, Nagamura Y, Kaku H, Shibuya N, Yasuda M, Nakashita H, Umemura K, Okada A, Okada K, Nojiri H, Yamane H (2007) Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. Biochim Biophys Acta 1769:497–505

    Article  CAS  PubMed  Google Scholar 

  • Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T, Kishi-Kaboshi M, Takahashi A, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2014) Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLoS One 9:e98737

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription 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 

  • Hwang SH, Lee IA, Yie SW, Hwang DJ (2008) Identification of an OsPR10a promoter region responsive to salicylic acid. Planta 227:1141–1150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang SH, Yie SW, Hwang DJ (2011) Heterologous expression of OsWRKY6 gene in Arabidopsis activates the expression of defense related genes and enhances resistance to pathogen. Plant Sci 181:316–323

    Article  CAS  PubMed  Google Scholar 

  • Kauffman HE, Reddy APK, Hsieh SPV, Merca SD (1973) An improved technique for evaluating resistance to rice varieties of Xanthomonas oryzae. Plant Dis Rep 57:537–541

    Google Scholar 

  • Lee H, Ko YJ, Cha JY, Park SR, Ahn I, Hwang DJ (2013) The C-terminal region of OsWRKY30 is sufficient to confer enhanced resistance to pathogen and activate the expression of defense-related genes. Plant Biotechnol Rep 7:221–230

    Article  Google Scholar 

  • Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XQ, Bai XQ, Wang XJ, Chu CC (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164:969–979

    Article  CAS  PubMed  Google Scholar 

  • Maeo K, Tomiya T, Hayashi K, Akaike M, Morikami A, Ishiguro S, Nakamura K (2001) Sugar-responsible elements in the promoter of a gene for beta-amylase of sweet potato. Plant Mol Biol 46:627–637

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng X, Hu Y, Tang X, Zhou P, Deng X, Wang H, Guo Z (2012) Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236:1485–1498

    Article  CAS  PubMed  Google Scholar 

  • Ricachenevsky FK, Sperotto RA, Menguer PK, Fett JP (2010) Identification of Fe-excess-induced genes in rice shoots reveals a WRKY transcription factor responsive to Fe, drought and senescence. Mol Biol Rep 37:3735–3745

    Article  CAS  PubMed  Google Scholar 

  • Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842

    Article  CAS  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 

  • Ryu HS, Han M, Lee SK, Cho JI, Ryoo N, Heu S, Lee YH, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836–847

    Article  CAS  PubMed  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19:2064–2076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimono M, Koga H, Akagi A, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang CJ, Kaku H, Inoue H, Takatsuji H (2012) Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol 13:83–94

    Article  CAS  PubMed  Google Scholar 

  • Tao Z, Liu H, Qiu D, Zhou Y, Li X, Xu C, Wang S (2009) A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol 151:936–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao Z, Kou Y, Liu H, Li X, Xia J, Wang S (2011) OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J Exp Bot 62:4863–4874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wang H, Hao J, Chen X, Hao Z, Wang X, Lou Y, Peng Y, Guo Z (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol 65:799–815

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Meng J, Peng X, Tang X, Zhou P, Xiang J, Deng X (2015) Rice WRKY4 acts as a transcriptional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight. Plant Mol Biol 89:157–171

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28:21–30

    Article  CAS  PubMed  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 

  • Xie Z, Zhang ZL, Zou X, Yang G, Komatsu S, Shen QJ (2006) Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant J 46:231–242

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NN (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9:68

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu S, Ligang C, Liping Z, Diqiu Y (2010) Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis. J Biosci 35:459–471

    Article  PubMed  Google Scholar 

  • Zhang ZL, Xie Z, Zou X, Casaretto J, Ho TH, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZL, Shin M, Zou X, Huang J, Ho TH, Shen QJ (2009) A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol 70:139–151

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Su J, Duan S, Ao Y, Dai J, Liu J, Wang P, Li Y, Liu B, Feng D, Wang J, Wang H (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7:30

    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 genes, GmWRKY13, GmWRKY21 and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6(5):486–503

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by Grant PJ01087001 from the National Institute of Agricultural Sciences and Grant PJ01109104 from the Next-Generation BioGreen21 Program to Dr. Duk-Ju Hwang.

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  1. Soon Il Kwon

    Present address: Convergence Research Center for Functional Plant Products, Advanced Institutes of Convergence Technology (AICT), Suwon, 443-270, Korea

Authors and Affiliations

  1. National Institute of Agricultural Science, Rural Development Administration, Jeonju, 560-500, Korea

    Seon-Hee Hwang, Soon Il Kwon, Ji-Young Jang, Il Lan Fang, Heyoung Lee, Changhyun Choi, Sangryeol Park, Ilpyung Ahn, Shin-chul Bae & Duk-Ju Hwang

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  1. Seon-Hee Hwang
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Correspondence to Duk-Ju Hwang.

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Additional information

Communicated by H. S. Judelson.

S.-H. Hwang and S. I. Kwon contributed equally to this study.

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Hwang, SH., Kwon, S.I., Jang, JY. et al. OsWRKY51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas oryzae pv. oryzae . Plant Cell Rep 35, 1975–1985 (2016). https://doi.org/10.1007/s00299-016-2012-0

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