WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance

Journal of Experimental Botany

Volumn 64, Issue 16, 2013, Pages 5085-5097

  Yokotani, Naoki ^a   Sato, Yuko ^a   Tanabe, Shigeru ^a   Chujo, Tetsuya ^b   Shimizu, Takafumi ^b   Okada, Kazunori ^b   Yamane, Hisakazu ^c   Shimono, Masaki ^a   Sugano, Shoji ^a   Takatsuji, Hiroshi ^a   Kaku, Hisatoshi ^d   Minami, Eiichi ^a   Nishizawa, Yoko ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c TEIKYO UNIVERSITY   (Japan)

^d Sakata Seed Ibérica SLU   (Japan)

Author keywords

Blast disease resistance; Cold stress; Phytoalexin; Rice; Transcriptional repressor; WRKY

Indexed keywords

PHYTOALEXIN; REPRESSOR PROTEIN; VEGETABLE PROTEIN;

ARTICLE; BLAST DISEASE RESISTANCE; COLD; COLD STRESS; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DISEASE; RICE; TRANSCRIPTIONAL REPRESSOR; WRKY.;

BLAST DISEASE RESISTANCE; COLD STRESS; PHYTOALEXIN; RICE; TRANSCRIPTIONAL REPRESSOR; WRKY.;

COLD TEMPERATURE; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; MAGNAPORTHE; ORYZA SATIVA; PLANT DISEASES; PLANT PROTEINS; REPRESSOR PROTEINS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84891886068     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert298     Document Type: Article

References (70)

1. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. 1997. Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. The Plant Cell 9, 1859-1868
2. 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, e51609
3. Bubier J, Schläppi M. 2004. Cold induction of EARLI1, a putative Arabidopsis lipid transfer protein, is light and calcium dependent. Plant, Cell and Environment 27, 929-936
4. Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X. 2010. Roles of arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biology 10, 281
5. Chinnusamy V, Zhu J, Zhu JK. 2007. Cold stress regulation of gene expression in plants. Trends in Plant Science 12, 444-451
6. Chujo T, Kato T, Yamada K, et al. 2008. Characterization of an elicitor-induced rice WRKY gene, OsWRKY71. Bioscience, Biotechnology, and Biochemistry 72, 240-245
7. Chujo T, Miyamoto K, Shimogawa T, et al. 2013. OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Molecular Biology 82, 23-37
8. Chujo T, Takai R, Akimoto-Tomiyama C, et al. 2007. Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. Biochimica et Biophysica Acta 1769, 497-505
9. Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A. 2008. Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiology 148, 1094-1105
10. DellaPenna D, Pogson BJ. 2006. Vitamin synthesis in plants: Tocopherols and carotenoids. Annual Review of Plant Biology 57, 711-738
11. 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 defense. Molecular Plant Pathology 13, 72-82
12. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science 5, 199-206
13. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. 2006. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology 9, 436-442.
14. Hasegawa M, Mitsuhara I, Seo S, Imai T, Koga J, Okada K, Yamane H, Ohashi Y. 2010. Phytoalexin accumulation in the interaction between rice and the blast fungus. Molecular Plant- Microbe Interactions 23, 1000-1011.
15. Jain M, Nijhawan A, Tyagi AK, Khurana JP. 2006. Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochemical and Biophysical Research Communications 345, 646-651
16. Jiang CJ, Shimono M, Sugano S, Kojima M, Yazawa K, Yoshida R, Inoue H, Hayashi N, Sakakibara H, Takatsuji H. 2010. Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Molecular Plant-Microbe Interactions 23, 791-798
17. Jiang Y, Deyholos MK. 2009. Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Molecular Biology 69, 91-105
18. Kim SH, Oikawa T, Kyozuka J, Wong HL, Umemura K, Kishi-Kaboshi M, Takahashi A, Kawano Y, Kawasaki T, Shimamoto K. 2012. The bHLH Rac Immunity1 (RAI1) is activated by OsRac1 via OsMAPK3 and OsMAPK6 in rice immunity. Plant and Cell Physiology 53, 740-754
19. Kim KC, Fan B, Chen Z. 2006. Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiology 142, 1180-1192
20. Koga H, Dohi K, Mori M. 2004. Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiological and Molecular Plant Pathology 65, 3-9
21. Li S, Fu Q, Chen L, Huang W, Yu D. 2011. Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233, 1237-1252
22. Liu D, Chen X, Liu J, Ye J, Guo Z. 2012. The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. Journal of Experimental Botany 63, 3899-3911
23. Matsuyama N, Dimond AE. 1973. Effect of nitrogenous fertilizer on biochemical processes that could affect lesion size of rice blast. Phytopathology 63, 1202-1203
24. Marè C, Mazzucotelli E, Crosatti C, Francia E, Stanca AM, Cattivelli L. 2004. Hv-WRKY38: A new transcription factor involved in cold- and drought-response in barley. Plant Molecular Biology 55, 399-416
25. Mauch-Mani B, Mauch F. 2005. The role of abscisic acid in plant- pathogen interactions. Current Opinion in Plant Biology 8, 409-414
26. McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible WR, Udvardi MK, Kazan K. 2005. Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiology 139, 949-959
27. Nakashima K, Tran LS, Van Nguyen D, et al. 2007. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. The Plant Journal 51, 617-630
28. Niwa Y, Hirano T, Yoshimoto K, Shimizu M, Kobayashi H. 1999. Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. The Plant Journal 18, 455-463
29. Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M. 2001. Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. The Plant Cell 13, 1959-1968
30. Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H. 2009. OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice. Journal of Biological Chemistry 284, 26510-26518
31. Okada A, Shimizu T, Okada K, Kuzuyama T, Koga J, Shibuya N, Nojiri H, Yamane H. 2007. Elicitor induced activation of the methylerythritol phosphate pathway toward phytoalexins biosynthesis in rice. Plant Molecular Biology 65, 177-187
32. Okada K. 2011. The biosynthesis of isoprenoids and the mechanisms regulating it in plants. Bioscience, Biotechnology, and Biochemistry 75, 1219-1225
33. Pandey SP, Somssich IE. 2009. The role of WRKY transcription factors in plant immunity. Plant Physiology 150, 1648-1655
34. Pauw B, Hilliou FA, Martin VS, et al. 2004. Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus. Journal of Biological Chemistry 279, 52940-52948
35. Passardi F, Theiler G, Zamocky M, et al. 2007. PeroxiBase: The peroxidase database. Phytochemistry 68, 1605-1611
36. 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
37. Peng Y, Bartley LE, Chen X, 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. Molecular Plant 1, 446-458
38. 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. Molecular Plant 1, 538-551
39. Robert-Seilaniantz A, Navarro L, Bari R, Jones JD. 2007. Pathological hormone imbalances. Current Opinion in Plant Biology 10, 372-379
40. Ross CA, Liu Y, Shen QJ. 2007. The WRKY gene family in rice (Oryza sativa). Journal of Integrative Plant Biology 49, 827-842
41. Rushton PJ, Somssich IE, Ringler P, Shen QJ. 2010. WRKY transcription factors. Trends in Plant Science 15, 247-258
42. 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 Reports 25, 836-847
43. Schweizer P, Schlagenhauf E, Schaffrath U, Dudler R. 1999. Different patterns of host genes are induced in rice by Pseudomonas syringae, a biological inducer of resistance, and the chemical inducer benzothiadiazole (BTH). European Journal of Plant Pathology 105, 659-665.
44. Seo YS, Chern M, Bartley LE, et al. 2011. Towards establishment of a rice stress response interactome. PLoS Genetics 7, e1002020
45. Sharma R, Vleesschauwer DD, Sharma MK, Ronald PC. 2013. Elucidating stress regulatory crosstalk in rice. Molecular Plant 6, 250-260
46. Shang Y, Yan L, Liu ZQ, et al. 2010. The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. The Plant Cell 22, 1909-1935
47. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P. 2007. Nuclear activity of MLA immune receptors links isolate-specific and basal diseaseresistance responses. Science 315, 1098-1103
48. Shimizu T, Jikumaru Y, Okada A, 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
49. Shimizu T, Lin F, Hasegawa M, Okada K, Nojiri H, Yamane H. 2012. Purification and identification of naringenin 7-O-methyltransferase, a key enzyme in biosynthesis of flavonoid phytoalexin sakuranetin in rice. Journal of Biological Chemistry 287, 19315-19325
50. Shimono M, Koga H, Akagi A, et al. 2012. Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Molecular Plant Pathology 13, 83-94
51. 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. The Plant Cell 19, 2064-2076
52. Singh KB, Foley RC, Oñate-Sánchez L. 2002. Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 5, 430-436
53. Soranzo N, Sari Gorla M, Mizzi L, De Toma G, Frova C.2004. Organisation and structural evolution of the rice glutathione S-transferase gene family. Molecular Genetics and Genomics 271, 511-521
54. Talbot NJ. 2003. On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annual Review of Microbiology 57, 177-202
55. Tanabe S, Okada M, Jikumaru Y, Yamane H, Kaku H, Shibuya N, Minami E. 2006. Induction of resistance against rice blast fungus in rice plants treated with a potent elicitor, N-acetylchitooligosaccharide. Bioscience, Biotechnology, and Biochemistry 70, 1599-1605
56. Thaler JS, Humphrey PT, Whiteman NK. 2012. Evolution of jasmonate and salicylate signal crosstalk. Trends in Plant Science 17, 260-270
57. Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H. 2006. Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. The Plant Journal 47, 969-976
58. Ton J, Flors V, Mauch-Mani B. 2009. The multifaceted role of ABA in disease resistance. Trends in Plant Science 14, 310-317
59. Toyomasu T, Usui M, Sugawara C, et al. 2013. Reversegenetic approach to verify physiological roles of rice phytoalexins: Characterization of a knockdown mutant of OsCPS4 phytoalexin biosynthetic gene in rice. Physiologia Plantarum (in press)
60. Wang A, Xia Q, Xie W, Datla R, Selvaraj G. 2003. The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proceedings of the National Academy of Sciences, USA 100, 14487-14492
61. 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 Physiology 137, 176-189
62. Xiong X, James VA, Zhang H, Altpeter F. 2010. Constitutive expression of the barley HvWRKY38 transcription factor enhances drought tolerance in turf and forage grass (Paspalumnotatum Flugge). Molecular Breeding 25, 419-432.
63. Xu X, Chen C, Fan B, Chen Z. 2006. Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. The Plant Cell 18, 1310-1326
64. Xu YH, Wang JW, Wang S, Wang JY, Chen XY. 2004. Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiology 135, 507-515
65. Xu ZY, Zhang X, Schläppi M, Xu ZQ. 2011. Cold-inducible expression of AZI1 and its function in improvement of freezing tolerance of Arabidopsis thaliana and Saccharomyces cerevisiae. Journal of Plant Physiology 168, 1576-1587
66. Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781-803.
67. Yasuda M, Ishikawa A, Jikumaru Y, et al. 2008. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. The Plant Cell 20, 1678-1692.
68. Zellerhoff N, Jarosch B, Groenewald JZ, Crous PW, Schaffrath U. 2006. Nonhost resistance of barley is successfully manifested against Magnaporthe grisea and a closely related Pennisetum-infecting lineage but is overcome by Magnaporthe oryzae. Molecular Plant-Microbe Interactions 19, 1014-1022
69. Zhang J, Peng Y, Guo Z. 2008. Constitutive expression of pathogeninducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Research 18, 508-521.
70. Zheng Z, Mosher SL, Fan B, Klessig DF, Chen Z. 2007. Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biology 7, 2