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Saturday 17 December 2016

OsWRKY80-OsWRKY4 Module as a Positive Regulatory Circuit in Rice Resistance Against Rhizoctonia solani

Published Date
9:63

Open AccessOriginal article
DOI: 10.1186/s12284-016-0137-y

Cite this article as: 
Peng, X., Wang, H., Jang, JC. et al. Rice (2016) 9: 63. doi:10.1186/s12284-016-0137-y

Author 
  • Xixu Peng
  • Haihua Wang
  • Jyan-Chyun Jang
  • Ting Xiao
  • Huanhuan He
  • Dan Jiang
  • Xinke Tang
Abstract

Background

Plant WRKY transcription factors play pivotal roles in diverse biological processes but most notably in plant defense response to pathogens. Sheath blight represents one of the predominant diseases in rice. However, our knowledge about the functions of WRKY proteins in rice defense against sheath blight is rather limited.

Results

Here we demonstrate that the expression of Oryza sativa WRKY80 gene (OsWRKY80) is rapidly and strongly induced upon infection of Rhizoctonia solani, the causal agent of rice sheath blight disease. OsWRKY80 expression is also induced by exogenous jasmonic acid (JA) and ethylene (ET), but not by salicylic acid (SA). OsWRKY80-GFP is localized in the nuclei of onion epidermal cells in a transient expression assay. Consistently, OsWRKY80 exhibits transcriptional activation activity in a GAL4 assay in yeast cells. Overexpression of OsWRKY80 in rice plants significantly enhanced disease resistance to R. solani, concomitant with elevated expression of OsWRKY4, another positive regulator in rice defense against R. solani. Suppression of OsWRKY80 by RNA interference (RNAi), on the other hand, compromised disease resistance to R. solani. Results of yeast one-hybrid assay and transient expression assay in tobacco cells have revealed that OsWRKY80 specifically binds to the promoter regions of OsWRKY4, which contain W-box (TTGAC[C/T]) or W-box like (TGAC[C/T]) cis-elements.

Conclusions

We propose that OsWRKY80 functions upstream of OsWRKY4 as an important positive regulatory circuit that is implicated in rice defense response to sheath blight pathogen R. solani.
References

  1. Agrawal GK, Rakwal R, Jwa NS (2001) Differential induction of three pathogenesis-related genes, PR10PR1b and PR5 by the ethylene generator ethephon under light and dark in rice (Oryza sativa L.) seedlings. J Plant Physiol 158:133–137CrossRefGoogle Scholar
  2. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983CrossRefPubMedGoogle Scholar
  3. Bagnaresi P, Biselli C, Orrù L, Urso S, Crispino L, Abbruscato P, Piffanelli P, Lupotto E, Cattivelli L, Valè G (2012) Comparative transcriptome profiling of the early response to Magnaporthe oryzae in durable resistant vs susceptible rice (Oryza sativa L.) genotypes. PLoS One 7:e51609CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bari R, Jones JD (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69:473–488CrossRefPubMedGoogle Scholar
  5. Cheng H, Li H, Deng Y, Xiao J, Li X, Wang S (2015) The WRKY45-2–WRKY13–WRKY42 transcriptional regulatory cascade is required for rice resistance to fungal pathogen. Plant Physiol 167:1087–1099CrossRefPubMedPubMedCentralGoogle Scholar
  6. Choi C, Hwang SH, Fang IR, Kwon SI, Park SR, Ahn I, Kim JB, Hwang DJ (2015) Molecular characterization of Oryza sativa WRKY6, which bindsto W-box-like element 1 of the Oryza sativa pathogenesis-related (PR10a promoter and confers reduced susceptibility to pathogens. New Phytol 208:846–859CrossRefPubMedGoogle Scholar
  7. Chujo T, Miyamoto K, Shimogawa T, Shimizu T, Otake Y, Yokotani N, Nishizawa Y, Shibuya N, Nojiri H, Yamane H, Minami E, Okada K (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol Biol 82:23–37CrossRefPubMedGoogle Scholar
  8. Delteil A, Blein M, Faivre-Rampant O, Guellim A, Estevan J, Hirsch J, Bevitori R, Michel C, Morel JB (2012) Building a mutant resource for the study of disease resistance in rice reveals the pivotal role of several genes involved in defence. Mol Plant Pathol 13:72–82CrossRefPubMedGoogle Scholar
  9. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37CrossRefPubMedGoogle Scholar
  10. Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10(2):71–78CrossRefPubMedGoogle Scholar
  11. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206CrossRefPubMedGoogle Scholar
  12. Hammond-Kosack KE, Parker JE (2003) Deciphering plant pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193CrossRefPubMedGoogle Scholar
  13. Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Laing WA (2005) Transient plant expression vectors for functional genomics, quantification of promoter activity and RNA silencing. Plant Methods 1:13CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativaL.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282CrossRefPubMedGoogle Scholar
  15. Hwang SH, Kwon SI, Jang JY, Fang IL, Lee H, Choi C, Park S, Ahn I, Bae SC, Hwang DJ (2016) OsWRKY51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas oryzae pv. oryzae. Plant Cell Rep 35(9):1975–1985CrossRefPubMedGoogle Scholar
  16. Jiang YJ, Yu DQ (2015) WRKY transcription factors: links between phytohormones and plant processes. Sci Chin Life Sci 58(5):501–502CrossRefGoogle Scholar
  17. Jimmy JL, Babu S (2015) Role of OsWRKY transcription factors in rice disease resistance. Trop plant pathol 40:355–361CrossRefGoogle Scholar
  18. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329CrossRefPubMedGoogle Scholar
  19. Kim KC, Fan B, Chen Z (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol 142:1180–1192CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331CrossRefPubMedGoogle Scholar
  21. Li NY, Chai RY, Guo ZJ (2009) The disease resistance of rice regulated by OsWRKY80 gene. Acta Agric Shanghai 25(3):14–18Google Scholar
  22. Liu XQ, Xian QB, Qian Q, Xiu JW, Ming SC, Cheng CC, Xiao QL, Xian QB, Qian Q, Xiu JW, Ming SC, Cheng CC (2005) OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1. Cell Res 15(8):593-603
  23. Liu X, Xianquan B, Xiujie W, Chengcai C, Xiaoqiang L, Xianquan B, Xiujie W, Chengcai C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164(8):969-979
  24. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410CrossRefPubMedGoogle Scholar
  25. Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant Microbe Interact 19:1127–1137CrossRefPubMedGoogle Scholar
  26. Mukhtar MS, Deslandes L, Auriac MC, Marco Y, Somssich IE (2008) The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum. Plant J 56:935–947CrossRefPubMedGoogle Scholar
  27. Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262CrossRefPubMedPubMedCentralGoogle Scholar
  28. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655CrossRefPubMedPubMedCentralGoogle Scholar
  29. Peng XX, Hu YJ, Tang XK, Zhou PL, Deng XB, Wang HH, Guo ZJ (2012) Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PRgene expression and resistance to fungal pathogens in rice. Planta 236:1485–1498CrossRefPubMedGoogle Scholar
  30. Peng XX, Tang XK, Zhou PL, Hu YJ, Deng XB, He Y, Wang HH (2011) Isolation and expression patterns of rice WRKY82 transcription factor gene responsive to both biotic and abiotic stresses. Agr Sci China 10:891–901CrossRefGoogle Scholar
  31. Peng Y, Bartley LE, Chen XW, Dardick C, Chern M, Ruan R, Canlas PE, Ronald PC (2008) OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 1:446–458CrossRefPubMedGoogle Scholar
  32. Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760CrossRefPubMedPubMedCentralGoogle Scholar
  33. Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 20:492–499CrossRefPubMedGoogle Scholar
  34. Qiu D, Xiao J, Xie W, Liu H, Li X, Xiong L, Wang S (2008) Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant 1:538–551PubMedGoogle Scholar
  35. 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 37:3735–3745CrossRefPubMedGoogle Scholar
  36. Rice WRKY Working Group (2012) Nomenclature report on rice WRKY’s. -Conflict regarding gene names and its solution. Rice 5:3CrossRefGoogle Scholar
  37. Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842CrossRefGoogle Scholar
  38. Rush MC, Hoff BJ, Mcllrath WO (1976) A uniform disease rating system for rice disease in the United States. In: Proceedings of the 16th Rice Technical Working Group, Lake Charles, Louisiana, USA., p 64Google Scholar
  39. 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 25:836–847CrossRefPubMedGoogle Scholar
  40. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  41. Sayler RJ, Yang Y (2007) Detection and quantification of Rhizoctonia solani AG-1 IA, the rice sheath blight pathogen, in rice using real-time PCR. Plant Dis 91:1663–1668CrossRefGoogle Scholar
  42. Schwechheimer C, Bevan M (1998) The regulation of transcription factor activity in plants. Trends Plant Sci 3:378–383CrossRefGoogle Scholar
  43. 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 13:83–94CrossRefPubMedGoogle Scholar
  44. 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 19:2064–2076CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 151:936–948CrossRefPubMedPubMedCentralGoogle Scholar
  46. Triezenberg SJ (1995) Structure and function of transcriptional activation domains. Curr Opin Genet Dev 5:190–196CrossRefPubMedGoogle Scholar
  47. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet 5:e1000772CrossRefPubMedPubMedCentralGoogle Scholar
  48. Turck F, Zhou A, Somssich IE (2004) Stimulus-Dependent, promoter-specific binding of transcription factor WRKY1 to its native promoter and the defense-related gene PcPR1-1 in parsley. Plant Cell 16:2573–2585CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ülker B, Somssich IE (2004) WRKY transcription factors: From DNA binding towards biological function. Curr Opin Plant Biol 7:491–498CrossRefPubMedGoogle Scholar
  50. Wang HH, Hao JJ, Chen XJ, Hao ZZ, Wang X, Lou YG, Peng YL, Guo ZJ (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol 65:799–815CrossRefPubMedGoogle Scholar
  51. Wang HH, Meng J, Peng XX, Tang XK, Zhou PL, Xiang JH, Deng XB (2015) Rice WRKY4 acts as a transcriptional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight. Plant Mol Biol 89:157–171CrossRefPubMedGoogle Scholar
  52. Wang J, Jiang J, Oard JH (2000) Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.). Plant Sci 156:201–211CrossRefPubMedGoogle Scholar
  53. Wang ZB, Zuo SM, Li G, Chen XJ, Chen ZX, Zhang YF, Pan XB (2009) Rapid identification technology of resistance to rice sheath blight in seedling stage. Acta Phytopathol Sin 39:174–182Google Scholar
  54. Wei T, Ou B, Li J, Zhao Y, Guo D, Zhu Y, Chen Z, Gu H, Li C, Qin G, Qu LJ (2013) Transcriptional profiling of rice early response to Magnaporthe oryzae identified OsWRKYs as important regulators in rice blast resistance. PLoS One 8:e59720CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY Family of transcription factors in rice and Arabidopsis and their Origins. DNA Res 12:9–26CrossRefPubMedGoogle Scholar
  56. Xie C, Zhang JS, Zhou HL, Li J, Zhang ZG, Wang DW, Chen SY (2003) Serine/threonine kinase activity in the putative histidine kinase-like ethylene receptor NTHK1 from tobacco. Plant J 33:385–393CrossRefPubMedGoogle Scholar
  57. Yang Y, Li R, Qi M (2000) In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J 22:543–551CrossRefPubMedGoogle Scholar
  58. Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H, Kaku H, Minami E, Nishizawa Y (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64:5085–5097CrossRefPubMedPubMedCentralGoogle Scholar
  59. Zhang YJ, Wang LJ (2005) The WRKY transcription factor superfamily : It s origin in eukaryotes and expansion in plants. BMC Evol Biol 5(1):1–12CrossRefPubMedPubMedCentralGoogle Scholar
  60. 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 134:1500–1513CrossRefPubMedPubMedCentralGoogle Scholar
  61. Zhao CJ, Wang AR, Shi YJ, Wang LQ, Liu WD, Wang ZH, Lu GD (2008) Identification of defense-related genes in rice responding to challenge by Rhizoctonia solani. Theor Appl Genet 116:501–516
  62. Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605CrossRefPubMedGoogle Scholar

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