Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Chujo, Tetsuya ^a,d   Miyamoto, Koji ^a,c   Ogawa, Satoshi ^a   Masuda, Yuka ^a   Shimizu, Takafumi ^a,e   Kishi Kaboshi, Mitsuko ^b   Takahashi, Akira ^b   Nishizawa, Yoko ^b   Minami, Eiichi ^b   Nojiri, Hideaki ^a   Yamane, Hisakazu ^a,c   Okada, Kazunori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c TEIKYO UNIVERSITY   (Japan)

^d MASSEY UNIVERSITY   (New Zealand)

^e RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROLINE; RECOMBINANT PROTEIN; SERINE; TRANSCRIPTOME; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; FUNGAL STRAIN; FUNGUS; GENE CLUSTER; GENE OVEREXPRESSION; IN VITRO STUDY; INFECTION RESISTANCE; MAGNAPORTHE ORYZAE; MKK4 GENE; MPK3 GENE; MPK6 GENE; MUTANT; NONHUMAN; PHOSPHOMIMIC MUTANT; PLANT GENE; PROTEIN PROCESSING; REACTOR CASCADE; REPORTER GENE; RICE; RICE BLAST; STEADY STATE; TRANSACTIVATION; TRANSGENIC PLANT; UPREGULATION; VIRULENCE; WRKY53 GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PLANT DISEASE;

GENE EXPRESSION REGULATION, PLANT; ORYZA SATIVA; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TRANSCRIPTION FACTORS;

EID: 84902449771     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098737     Document Type: Article

References (55)

1. Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6: 973-979.
2. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814. (Pubitemid 43261453)
3. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329. (Pubitemid 44764102)
4. Zipfel C, Robatzek S (2010) Pathogen-associated molecular pattern-triggered immunity: veni, vidi? Plant Physiol 154: 551-554.
5. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15: 247-258.
6. Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, et al. (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7: 301-308. (Pubitemid 36726514)
7. Seo S, Okamoto M, Seto H, Ishizuka K, Sano H, et al. (1995) Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270: 1988-1992. (Pubitemid 26097188)
8. Zhang S, Klessig DF (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9: 809-824. (Pubitemid 28104509)
9. Zhang S, Klessig DF (1998) The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc Natl Acad Sci U S A 95: 7225-7230. (Pubitemid 28278135)
10. Romeis T, Piedras P, Zhang S, Klessig DF, Hirt H, et al. (1999) Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11: 273-287.
11. Jin H, Liu Y, Yang KY, Kim CY, Baker B, et al. (2003) Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J 33: 719-731. (Pubitemid 36325914)
12. Tanaka S, Ishihama N, Yoshioka H, Huser A, O'Connell R, et al. (2009) The Colletotrichum orbiculare SSD1 mutant enhances Nicotiana benthamiana basal resistance by activating a mitogen-activated protein kinase pathway. Plant Cell 21: 2517-2526.
13. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983. (Pubitemid 34193435)
14. Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277: 559-565. (Pubitemid 34952092)
15. Kroj T, Rudd JJ, Nurnberger T, Gabler Y, Lee J, et al. (2003) Mitogen-activated protein kinases play an essential role in oxidative burst-independent expression of pathogenesis-related genes in parsley. J Biol Chem 278: 2256-2264. (Pubitemid 36801294)
16. Kim CY, Zhang S (2004) Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J 38: 142-151. (Pubitemid 38448451)
17. Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, et al. (2007) Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51: 941-954. (Pubitemid 47376640)
18. Ren D, Liu Y, Yang KY, Han L, Mao G, et al. (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105: 5638-5643. (Pubitemid 351753915)
19. Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, et al. (2010) A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J 63: 599-612.
20. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10: 366-371. (Pubitemid 47126955)
21. Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49: 827-842. (Pubitemid 46993133)
22. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150: 1648-1655.
23. Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, et al. (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15: 5690-5670.
24. 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: 4689-4699. (Pubitemid 29415523)
25. 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.
26. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199-206. (Pubitemid 30300843)
27. Cohen P (1997) The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol 7: 353-361.
28. Sharrocks AD, Yang SH, Galanis A (2000) Docking domains and substrate-specificity determination for MAP kinases. Trends Biochem Sci 25: 448-453. (Pubitemid 30662413)
29. Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H (2011) Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell 23: 1153-1170.
30. Ishihama N, Yoshioka H (2012) Post-translational regulation of WRKY transcription facrors in plant immunity. Curr Opin Plant Biol 15: 431-437.
31. Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, et al. (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24: 2579-2589. (Pubitemid 41076314)
32. Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, et al. (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27: 2214-2221.
33. Mao GH, Meng XZ, Liu YD, Zheng ZY, Chen ZX, et al. (2011) Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis. Plant Cell 23: 1639-1653.
34. Menke FL, Kang HG, Chen Z, Park JM, Kumar D, et al. (2005) Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol Plant Microbe Interact 18: 1027-1034. (Pubitemid 41356406)
35. Koo SC, Moon BC, Kim JK, Kim CY, Sung SJ, et al. (2009) OsBWMK1 mediates SA-dependent defense responses by activating the transcription factor OsWRKY33. Biochem Biophys Res Commun 387: 365-370.
36. Chujo T, Takai R, Akimoto-Tomiyama C, Ando S, Minami E, et al. (2007) Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. Biochim Biophys Acta 1769: 497-505. (Pubitemid 47082525)
37. Chujo T, Sugioka N, Masuda Y, Shibuya N, Takemura T, et al. (2009) Promoter analysis of the elicitor-induced WRKY gene OsWRKY53, which is involved in defense responses in rice. Biosci Biotechnol Biochem 73: 1901-1904.
38. Ando S, Sato Y, Shigemori H, Shimizu T, Okada K, et al. (2011) Identification and characterization of 2′-deoxyuridine from the supernatant of conidial suspensions of rice blast fungus as an infection-promoting factor in rice plants. Mol Plant Microbe Interact 24: 519-532.
39. Toki S, Hara N, Ono K, Onodera H, Tagiri A, et al. (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47: 969-976. (Pubitemid 44326445)
40. Hiratsu K, Mitsuda N, Matsui K, Ohme-Takagi M (2004) Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem Biophys Res Commun 321: 172-178. (Pubitemid 39055620)
41. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, et al. (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19: 2064-2076. (Pubitemid 47218859)
42. Kitagawa K, Kurinami S, Oki K, Abe Y, Ando T, et al. (2010) A Novel Kinesin 13 Protein Regulating Rice Seed Length. Plant Cell Physiol 51: 1315-1329.
43. Ando S, Tanabe S, Akimoto-Tomiyama C, Nishizawa Y, Minami E (2009) The Supernatant of a Conidial Suspension of Magnaporthe oryzae Contains a Factor that Promotes the Infection of Rice Plants. J Phytopathol 157: 420-426.
44. Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, et al. (2013) OsWRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64: 5085-5097.
45. Shimizu T, Jikumaru Y, Okada A, Okada K, Koga J, et al. (2008) Effects of a bile acid elicitor, cholic acid, on the biosynthesis of diterpenoid phytoalexins in suspension-cultured rice cells. Phytochemistry 69: 973-981. (Pubitemid 351222598)
46. Shimura K, Okada A, Okada K, Jikumaru Y, Ko KW, et al. (2007) Identification of a biosynthetic gene cluster in rice for momilactones. J Biol Chem 282: 34013-34018. (Pubitemid 350159470)
47. Wang Q, Hillwig ML, Peters RJ (2011) CYP99A3: functional identification of a diterpene oxidase from the momilactone biosynthetic gene cluster in rice. Plant J 65: 87-95.
48. Lai ZB, Li Y, Wang F, Cheng Y, Fan BF, et al. (2011) Arabidopsis Sigma Factor Binding Proteins Are Activators of the WRKY33 Transcription Factor in Plant Defense. Plant Cell 23: 3824-3841.
49. Cheng Y, Zhou Y, Yang Y, Chi YJ, Zhou J, et al. (2012) Structural and Functional Analysis of VQ Motif-Containing Proteins in Arabidopsis as Interacting Proteins of WRKY Transcription Factors. Plant Physiol 159: 810-825.
50. Chujo T, Miyamoto K, Shimogawa T, Shimizu T, Otake Y, et al. (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol Biol 82: 23-37.
51. Mayr B, Montminy M (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Bio 2: 599-609. (Pubitemid 33674011)
52. Yang SH, Sharrocks AD, Whitmarsh AJ (2003) Transcriptional regulation by the MAP kinase signaling cascades. Gene 320: 3-21. (Pubitemid 37352751)
53. Toyomasu T, Usui M, Sugawara C, Otomo K, Hirose Y, et al. (2014) Reverse-genetic approach to verify physiological roles of rice phytoalexins: characterization of a knockdown mutant of OsCPS4 phytoalexin biosynthetic gene in rice. Physiol Plant 150: 55-62.
54. Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, et al. (2009) OsTGAP1, a bZIP Transcription Factor, Coordinately Regulates the Inductive Production of Diterpenoid Phytoalexins in Rice. J Biol Chem 284: 26510-26518.
55. Kishi-Kaboshi M, Takahashi A, Hirochika H (2010) MAMP-responsive MAPK cascades regulate phytoalexin biosynthesis. Plant Signal Behav 5: 1653-1656.