OsNPR1 negatively regulates herbivore-induced JA and ethylene signaling and plant resistance to a chewing herbivore in rice

Physiologia Plantarum

Volumn 147, Issue 3, 2013, Pages 340-351

  Li, Ran ^a   Afsheen, Sumera ^a   Xin, Zhaojun ^a   Han, Xiu ^a   Lou, Yonggen ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPENTANE DERIVATIVE; ESSENTIAL OIL; ETHYLENE; ETHYLENE DERIVATIVE; JASMONIC ACID; LIPOXYGENASE; OXYLIPIN; PHYTOHORMONE; SALICYLIC ACID; TRYPSIN INHIBITOR; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; HERBIVORY; IMMUNOLOGY; INJURY; ISOLATION AND PURIFICATION; LEPIDOPTERA; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT STEM; RICE; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; UPREGULATION;

ANIMALS; CYCLOPENTANES; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; HERBIVORY; LEPIDOPTERA; LIPOXYGENASE; OILS, VOLATILE; ORYZA SATIVA; OXYLIPINS; PLANT DISEASES; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANT PROTEINS; PLANT STEMS; PLANTS, GENETICALLY MODIFIED; SALICYLIC ACID; SEEDLING; SIGNAL TRANSDUCTION; TRYPSIN INHIBITORS; UP-REGULATION; WOUNDS AND INJURIES;

CHILO SUPPRESSALIS; CNAPHAROCROSIS MEDINALIS;

EID: 84873750159     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2012.01666.x     Document Type: Article

References (52)

1. Cao H, Bowling SA, Gordon AS, Dong XN (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired-resistance. Plant Cell 6: 1583-1592
2. Cao H, Glazebrook J, Clarke JD, Volko S, Dong XN (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-63
3. Cao H, Li X, Dong XN (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95: 6531-6536
4. Cheng JA, He JH (1996) Rice Insect Pests. China Agriculture Press, Beijing
5. Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong XN, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 27: 101-113
6. Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005) Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant Microbe Interact 18: 511-520
7. Cui J, Jander G, Racki LR, Kim PD, Pierce NE, Ausubel FM (2002) Signals involved in Arabidopsis resistance to trichoplusia ni caterpillars induced by virulent and avirulent strains of the phytopathogen Pseudomonas syringae. Plant Physiol 129: 551-564
8. Despres C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12: 279-290
9. Fan WH, Dong XN (2002) In vivo interaction between npr1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14: 1377-1389
10. Feng JX, Cao L, Li J, Duan CJ, Luo XM, Le N, Wei HH, Liang SJ, Chu CC, Pan QH, Tang JL (2011) Involvement of OsNPR1/NH1 in rice basal resistance to blast fungus Magnaporthe oryzae. Eur J Plant Pathol 131: 221-235
11. Fitzgerald HA, Chern MS, Navarre R, Ronald PC (2004) Overexpression of (At)NPR1 in rice leads to a BTH- and environment-induced lesion-mimic/cell death phenotype. Mol Plant Microbe Interact 17: 140-151
12. Girling RD, Madison R, Hassall M, Poppy GM, Turner JG (2008) Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles. J Exp Bot 59: 3077-3085
13. Halitschke R, Baldwin IT (2005) Jasmonates and related compounds in plant-insect interactions. J Plant Growth Regul 23: 238-245
14. Isikawa K, Yoshimura K, Harada K, Fukusaki E, Ogawa T, Tamoi M, Shigeoka S (2010) AtNUDX6, an ADP-Ribose/NADH pyrophosphohydrolase in Arabidopsis, positively regulates NPR1-dependent salicylic acid signaling. Plant Physiol 152: 2000-2012
15. Kanno H, Hasegawa M, Kodama O (2011) Accumulation of salicylic acid, jasmonic acid and phytoalexins in rice, Oryza sativa, infested by the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Appl Entomol Zool 47: 27-34
16. Kinkema M, Fan WH, Dong XN (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12: 2339-2350
17. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146: 839-844
18. Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RA, Ritsema T, Pieterse CM (2009) Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 149: 1797-1809
19. 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
20. Lindermayr C, Sell S, Müller B, Leister D, Durner J (2010) Redox regulation of NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22: 2894-2907
21. Liu YD, Zhang SQ (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16: 3386-3399
22. Lou YG, Baldwin IT (2003) Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proc Natl Acad Sci USA 100: 14581-14586
23. Lou YG, Du MH, Turlings TCJ, Cheng JA, Shan WF (2005a) Exogenous application of jasmonic acid induces volatile emissions in rice and enhances parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae. J Chem Ecol 31: 1985-2002
24. Lou YG, Ma B, Cheng JA (2005b) Attraction of the parasitoid Anagrus nilaparvatae to rice volatiles induced by the rice brown planthopper Nilaparvata lugens. J Chem Ecol 31: 2357-2372
25. Lou YG, Hua XY, Turlings TCJ, Cheng JA, Chen XX, Ye GY (2006) Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field. J Chem Ecol 32: 2375-2387
26. Lu YJ, Wang X, Lou YG, Cheng JA (2006) Role of ethylene signaling in the production of rice volatiles induced by the rice brown planthopper Nilaparvata lugens. Chin Sci Bull 51: 2457-2465
27. Lu J, Ju HP, Zhou GX, Zhu CS, Erb M, Wang XP, Wang P, Lou YG (2011) An EAR-motif-containing ERF transcription factor affects herbivore-induced signaling, defense and resistance in rice. Plant J 68: 583-596
28. Maier F, Zwicker S, Hückelhoven A, Meißner M, Funk J, Fitzner AJP, Pfitzner UM (2011) NONEXPRESSOR OF PATHOGENESIS-RELATED PROTEINS1 (NPR1) and some NPR1-related proteins are sensitive to salicylic acid. Mol Plant Pathol 12: 73-91
29. Meur G, Budatha M, Srinivasan T, Rajesh Kumar KR, Dutta Gupta A, Kirti PB (2008) Constitutive expression of Arabidopsis NPR1 confers enhanced resistance to the early instars of Spodoptera litura in transgenic tobacco. J Plant Physiol 133: 765-775
30. Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67: 2450-2462
31. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944
32. Parkhi V, Kumar V, Campbell LAM, Bell AA, Shah J, Rathore KS (2010) Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NPR1. Transgenic Res 19: 959-975
33. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103: 1111-1120
34. Pieterse CMJ, van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7: 456-464
35. Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway control induced systemic resistance in Arabidopsis. Plant Cell 10: 1571-1580
36. Qi JF, Zhou GX, Yang LJ, Erb M, Lu YH, Sun XL, Cheng JA, Lou YG (2011) The chloroplast-localized phospholipases D α4 and α5 regulate herbivore-induced direct and indirect defenses in rice. Plant Physiol 157: 1987-1999
37. Rayapuram C, Baldwin IT (2007) Increased SA in NPR1-silenced plants antagonizes JA and JA-dependent direct and indirect defenses in herbivore-attacked Nicotiana attenuata in nature. Plant J 52: 700-715
38. Shah J (2003) The salicylic acid loop in plant defense. Curr Opin Plant Biol 6: 365-371
39. 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
40. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, van Loon LC, Dong XN, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760-770
41. Spoel SH, Mou ZL, Tada Y, Spivey NW, Genschik P, Dong XN (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137: 860-872
42. Stotz HU, Koch T, Biedermann A, Weniger K, Boland W, Mitchell-Olds T (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214: 648-652
43. Sugano S, Jiang CJ, Miyazawa SI, Masumoto C, Yazawa K, Hayashi N, Shimono M, Nakayama A, Miyao M, Takatsuji H (2010) Role of OsNPR1 in rice defense program as revealed by genomewide expression analysis. Plant Mol Biol 74: 549-562
44. van Dam NM, Horn M, Mares M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27: 547-568
45. Wally O, Jayaraj J, Punja ZK (2009) Broad-spectrum disease resistance to necrotrophic and biotrophic pathogens in transgenic carrots (Daucus carota L.) expressing an Arabidopsis NPR1 gene. Planta 231: 131-141
46. Wang X, Hu LC, Zhou GX, Cheng JA, Lou YG (2011) Salicylic acid and ethylene signaling pathways are involved in production of rice trypsin proteinase inhibitors induced by the leaf folder Cnaphalocrocis medinalis (Guenée). Chin Sci Bull 56: 2351-2358
47. Wu JQ, Baldwin IT (2009) Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 32: 1161-1174
48. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory Manual for Physiological Studies of Rice, 3rd Edn. The International Rice Research Institute, Manila
49. Yuan YX, Zhong SH, Li Q, Zhu ZR, Lou YG, Wang LY, Wang JJ, Wang MY, Li QL, Yang DL, He ZH (2007) 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 5: 313-324
50. Zhou GX, Qi JF, Ren N, Cheng JA, Erb M, Mao BZ, Lou YG (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60: 638-648
51. Zhou GX, Wang X, Yan F, Wang X, Li R, Cheng JA, Lou YG (2011) Genome-wide transcriptional changes and defense-related chemical profiling of rice in response to infestation by the rice striped stem borer Chilo suppressalis. Physiol Plant 143: 21-40
52. Ziegler J, Keinänen M, Baldwin IT (2001) Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuate. Phytochemistry 58: 729-738