Genome-wide identification of WRKY45-regulated genes that mediate benzothiadiazole-induced defense responses in rice

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Nakayama, Akira ^a,b   Fukushima, Setsuko ^a   Goto, Shingo ^a   Matsushita, Akane ^a,c   Shimono, Masaki ^a,d   Sugano, Shoji ^a   Jiang, Chang Jie ^a   Akagi, Aya ^a,e   Yamazaki, Muneo ^a   Inoue, Haruhiko ^a   Takatsuji, Hiroshi ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b MAEBASHI INSTITUTE OF TECHNOLOGY   (Japan)

^c Du Pont Kabushiki Kaisha   (Japan)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e BAYER AG   (Germany)

Author keywords

Benzothiadiazole; Magnaporthe oryzae; OsNPR1; Salicylic acid; WRKY

Indexed keywords

VEGETABLE PROTEIN;

ARTICLE; DNA MICROARRAY; GENETICS; METABOLISM; MICROBIOLOGY; PLANT DISEASE; PLANT GENOME; RICE; TRANSGENIC PLANT;

GENOME, PLANT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORYZA SATIVA; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED;

EID: 84885057190     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-150     Document Type: Article

References (56)

1. Cao H, Bowling SA, Gordon AS, Dong X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 1994, 6(11):1583-1592. 160545, 12244227.
2. Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC. Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant-Microbe Interact 2005, 18(6):511-520. 10.1094/MPMI-18-0511, 15986920.
3. Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Li Q, Yang D, et al. Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 2007, 5(2):313-324. 10.1111/j.1467-7652.2007.00243.x, 17309686.
4. Yoshioka K, Nakashita H, Klessig DF, Yamaguchi I. Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. Plant J 2001, 25(2):149-157. 10.1046/j.1365-313x.2001.00952.x, 11169191.
5. Iwai T, Seo S, Mitsuhara I, Ohashi Y. Probenazole-induced accumulation of salicylic acid confers resistance to Magnaporthe grisea in adult rice plants. Plant Cell Physiol 2007, 48(7):915-924. 10.1093/pcp/pcm062, 17517758.
6. Friedrich L, Lawton K, Ruess W, Masner P, Specker N, Rella MG, Meier B, Dincher S, Staub T, Uknes S, et al. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 1996, 10(1):61-70.
7. Lawton KA, Friedrich L, Hunt M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 1996, 10(1):71-82. 10.1046/j.1365-313X.1996.10010071.x, 8758979.
8. Yasuda M, Kusajima M, Nakajima M, Akutsu K, Kudo T, Yoshida S, Nakashita H. Thiadiazole carboxylic acid moiety of tiadinil, SV-03, induces systemic acquired resistance in tobacco without salicylic acid accumulation. J Pestic Sci 2006, 31(3):329-334.
9. Conrath U, Pieterse CM, Mauch-Mani B. Priming in plant-pathogen interactions. Trends Plant Sci 2002, 7(5):210-216. 10.1016/S1360-1385(02)02244-6, 11992826.
10. Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE. Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 1996, 15(20):5690-5700. 452313, 8896462.
11. Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J 1999, 18(17):4689-4699. 10.1093/emboj/18.17.4689, 1171542, 10469648.
12. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 2000, 26(4):403-410. 10.1038/82521, 11101835.
13. Pandey SP, Somssich IE. The role of WRKY transcription factors in plant immunity. Plant Physiol 2009, 150(4):1648-1655. 10.1104/pp.109.138990, 2719123, 19420325.
14. Ross CA, Liu Y, Shen QJ. The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 2007, 49(6):827-842.
15. Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S. OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant-Microbe Interact 2007, 20(5):492-499. 10.1094/MPMI-20-5-0492, 17506327.
16. Qiu D, Xiao J, Xie W, Liu H, Li X, Xiong L, Wang S. Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant 2008, 1(3):538-551. 10.1093/mp/ssn012, 19825559.
17. Liu XQ, Bai XQ, Qian Q, Wang XJ, Chen MS, Chu CC. OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1. Cell Res 2005, 15(8):593-603. 10.1038/sj.cr.7290329, 16117849.
18. Liu X, Bai X, Wang X, Chu C. OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 2007, 164(8):969-979. 10.1016/j.jplph.2006.07.006, 16919842.
19. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H. Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 2007, 19(6):2064-2076. 10.1105/tpc.106.046250, 1955718, 17601827.
20. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. The WRKY superfamily of plant transcription factors. Trends Plant Sci 2000, 5(5):199-206. 10.1016/S1360-1385(00)01600-9, 10785665.
21. Kalde M, Barth M, Somssich IE, Lippok B. Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant-Microbe Interact 2003, 16(4):295-305. 10.1094/MPMI.2003.16.4.295, 12744458.
22. Li J, Brader G, Palva ET. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 2004, 16(2):319-331. 10.1105/tpc.016980, 341906, 14742872.
23. Shimono M, Koga H, Akagi AYA, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang C-J, et al. Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol 2012, 13(1):83-94. 10.1111/j.1364-3703.2011.00732.x, 21726399.
24. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 2009, 137(5):860-872. 10.1016/j.cell.2009.03.038, 2704463, 19490895.
25. Matsushita A, Inoue H, Goto S, Nakayama A, Sugano S, Hayashi N, Takatsuji H. The nuclear ubiquitin proteasome degradation affects WRKY45 function in the rice defense program. Plant J 2013, 73(2):302-313.
26. Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A, Sugano S, Jiang CJ, Takatsuji H. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc Natl Acad Sci U S A 2013, 110(23):9577-9582. 10.1073/pnas.1222155110, 3677490, 23696671.
27. Wang D, Amornsiripanitch N, Dong X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathol 2006, 2(11):e123.
28. Blanco F, Salinas P, Cecchini N, Jordana X, Van Hummelen P, Alvarez M, Holuigue L. Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 2009, 70(1):79-102.
29. Knoth C, Ringler J, Dangl JL, Eulgem T. Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant-Microbe Interact 2007, 20(2):120-128. 10.1094/MPMI-20-2-0120, 17313163.
30. Sugano S, Jiang C-J, Miyazawa S-I, Masumoto C, Yazawa K, Hayashi N, Shimono M, Nakayama A, Miyao M, Takatsuji H. Role of OsNPR1 in rice defense program as revealed by genome-wide expression analysis. Plant Mol Biol 2010, 74(6):549-562. 10.1007/s11103-010-9695-3, 20924648.
31. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Soc 1995, B57:289-300.
32. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, et al. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 2005, 310(5751):1180-1183. 10.1126/science.1119409, 16293760.
33. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, et al. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 2003, 425(6961):973-977. 10.1038/nature02076, 14586469.
34. Stein M, Dittgen J, Sanchez-Rodriguez C, Hou B-H, Molina A, Schulze-Lefert P, Lipka V, Somerville S. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 2006, 18(3):731-746. 10.1105/tpc.105.038372, 1383646, 16473969.
35. Moons A. Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett 2003, 553(3):370-376. 10.1016/S0014-5793(03)01060-3, 14572653.
36. de Montellano PR O, Nielsen K, Møller B. Cytochrome P450s in plants. Cytochrome P450 2005, 553-583. US: Springer.
37. Cao P-J, Bartley LE, Jung K-H, Ronald PC. Construction of a rice glycosyltransferase phylogenomic database and identification of rice-diverged glycosyltransferases. Mol Plant 2008, 1(5):858-877. 10.1093/mp/ssn052, 19825588.
38. Bowles D, Isayenkova J, Lim EK, Poppenberger B. Glycosyltransferases: managers of small molecules. Curr Opin Plant Biol 2005, 8(3):254-263. 10.1016/j.pbi.2005.03.007, 15860422.
39. Vogt T, Jones P. Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci 2000, 5(9):380-386. 10.1016/S1360-1385(00)01720-9, 10973093.
40. Umemura K, Satou J, Iwata M, Uozumi N, Koga J, Kawano T, Koshiba T, Anzai H, Mitomi M. Contribution of salicylic acid glucosyltransferase, OsSGT1, to chemically induced disease resistance in rice plants. Plant J 2009, 57(3):463-472. 10.1111/j.1365-313X.2008.03697.x, 18826428.
41. Langlois-Meurinne M, Gachon CMM, Saindrenan P. Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis. Plant Physiol 2005, 139(4):1890-1901. 10.1104/pp.105.067223, 1310567, 16306146.
42. Blée E. Impact of phyto-oxylipins in plant defense. Trends Plant Sci 2002, 7(7):315-322. 10.1016/S1360-1385(02)02290-2, 12119169.
43. Tani T, Sobajima H, Okada K, Chujo T, Arimura S-I, Tsutsumi N, Nishimura M, Seto H, Nojiri H, Yamane H. Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 2008, 227(3):517-526. 10.1007/s00425-007-0635-7, 17938955.
44. Peng Y, Bartley LE, Chen X, Dardick C, Chern M, Ruan R, Canlas PE, Ronald PC. OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 2008, 1(3):446-458. 10.1093/mp/ssn024, 19825552.
45. Park CJ, Ronald PC. Cleavage and nuclear localization of the rice XA21 immune receptor. Nat Commun 2012, 3:920. 3621455, 22735448.
46. Kaneda T, Taga Y, Takai R, Iwano M, Matsui H, Takayama S, Isogai A, Che F-S. The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J 2009, 28(7):926-936. 10.1038/emboj.2009.39, 2670867, 19229294.
47. Taga Y, Takai R, Kaneda T, Matsui H, Isogai A, Che FS. Role of OsHSP90 and IREN, Ca2+ dependent nuclease, in plant hypersensitive cell death induced by transcription factor OsNAC4. Plant Signal Behav 2009, 4(8):740-742. 10.4161/psb.4.8.9087, 2801386, 19820348.
48. Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K. A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci U S A 2002, 99(11):7530-7535. 10.1073/pnas.112209199, 124274, 12032317.
49. Kojo K, Yaeno T, Kusumi K, Matsumura H, Fujisawa S, Terauchi R, Iba K. Regulatory mechanisms of ROI generation are affected by rice spl mutations. Plant Cell Physiol 2006, 47(8):1035-1044. 10.1093/pcp/pcj074, 16816407.
50. Aoyama T, Chua NH. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 1997, 11(3):605-612. 10.1046/j.1365-313X.1997.11030605.x, 9107046.
51. Zhang JZ. Overexpression analysis of plant transcription factors. Curr Opin Plant Biol 2003, 6(5):430-440. 10.1016/S1369-5266(03)00081-5, 12972043.
52. Ryu H-S, Han M, Lee S-K, Cho J-I, Ryoo N, Heu S, Lee Y-H, Bhoo S, Wang G-L, Hahn T-R, et al. A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 2006, 25(8):836-847. 10.1007/s00299-006-0138-1, 16528562.
53. Wang D, Weaver ND, Kesarwani M, Dong X. Induction of protein secretory pathway is required for systemic acquired resistance. Science 2005, 308(5724):1036-1040. 10.1126/science.1108791, 15890886.
54. Kalde M, Nühse TS, Findlay K, Peck SC. The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc Natl Acad Sci U S A 2007, 104(28):11850-11855. 10.1073/pnas.0701083104, 1913864, 17592123.
55. Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, et al. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 2009, 323(5910):101-106. 10.1126/science.1163732, 19095900.
56. Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H. Early infection of scutellum tissue with Agrobacterium allows high speed transformation of rice. Plant J 2006, 47:969-976. 10.1111/j.1365-313X.2006.02836.x, 16961734.