Interaction specificity and coexpression of rice NPR1 homologs 1 and 3 (NH1 and NH3), TGA transcription factors and Negative Regulator of Resistance (NRR) proteins

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Chern, Mawsheng ^a   Bai, Wei ^a,b   Ruan, Deling ^a   Oh, Taeyun ^a   Chen, Xuewei ^a,c   Ronald, Pamela C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INNER MONGOLIA AGRICULTURAL UNIVERSITY   (China)

^c SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Bridged split YFP; Co expression; Innate immunity; NH1; NPR1; Protein interaction; RH; Salicylic acid; SAR; Split YFP; TGA; Yeast two hybrid

Indexed keywords

HYBRID PROTEIN; NEGATIVE REGULATOR OF RESISTANCE PROTEIN; NPR1 HOMOLOGS 1 PROTEIN; NPR1 HOMOLOGS 3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TGA; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CONTROLLED STUDY; GENOME ANALYSIS; MICROARRAY ANALYSIS; NONHUMAN; PLANT GENOME; PLANT IMMUNITY; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; RICE; DISEASE RESISTANCE; EPISTASIS; GENE EXPRESSION; GENETICS; METABOLISM; SEQUENCE HOMOLOGY; TWO HYBRID SYSTEM;

ARABIDOPSIS;

DISEASE RESISTANCE; EPISTASIS, GENETIC; GENE EXPRESSION; ORYZA SATIVA; PLANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84904046803     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-461     Document Type: Article

References (54)

1. Durrant WE, Dong X. Systemic acquired resistance. Annu Rev Phytopathol 2004, 42:185-209.
2. Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexader DC, Ahl-Goy P, Metraux JP, Ryals JA. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 1991, 3:1085-1094.
3. Friedrich L, Lawton K, Ruess W, Masner P, Speckner N, Gt Rella M, Meier B, Dinher S, Staub T, Uknes S, Metraux J-P, Kessman H, Ryals J. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 1996, 9:61-70.
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, 25:149-157.
5. Gorlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel K-H, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 1996, 8:629-643.
6. Smith JA, Metraux J-P. Pseudomonas syringae pathovar syringae induces systemic resistance to pyricularia oryzae in rice. Physiol and Mol Plant Pathol 1991, 39:451-461.
7. Schweizer P, Schlagenhauf E, Schaffrath U, Dudler R. Different patterns of host genes are induced in rice by Pseudomonas syringae, a biological inducer of resistance, and the chemical inducer benzothiadiazole (BTH). Eur J Plant Pathol 1999, 105:659-665.
8. Rohilla R, Singh US, Singh RL. Mode of action of acibenzolar-S-methyl against sheath blight of rice, caused by Rhizoctonia solani kuhn. Pest Manag Sci 2002, 58:63-69.
9. 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, 19:2064-2076.
10. Morris SW, Vernoolij B, Titatarn S, Starrett M, Thomas S, Wiltse CC, Frederiksen RA, Bhandhufalck A, Hulbert S, Uknes S. Induced resistance responses in maize. Mol Plant-Microbe Interact 1998, 11:643-658.
11. 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, 6:1583-1592.
12. Delaney TP, Friedrich L, Ryals JA. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci 1995, 92:6602-6606.
13. Glazebrook J, Rogers EE, Ausubel FM. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 1996, 143:973-982.
14. Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D, Steiner H-Y, Johnson J, Delaney TP, Jesse T, Vos P, Uknes S. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. Plant Cell 1997, 9:425-439.
15. Shah J, Tsui F, Klessig DF. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact 1997, 10:69-78.
16. Cao H, Glazebrook J, Clarke J, Volko S, Dong X. The Arabidopsis npr1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 1997, 88:57-63.
17. Mou Z, Fan W, Dong X. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 2003, 113:1-10.
18. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, Luca VD, Despres C. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 2012, 1:639-647.
19. Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, Dong X. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 2012, doi:10.1038/nature11162.
20. Cao H, Li X, Dong X. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci 1998, 95:6531-6536.
21. Chern M, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC. Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 2001, 27:101-113.
22. Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC. Over-expression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant Microbe Interact 2005, 18:511-520.
23. Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Li Q, Yang D, He Z. 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, 5:313-324.
24. Bai W, Chern M, Ruan D, Canlas PE, Sze-To WH, Ronald PC. Enhanced disease resistance and hypersensitivity to BTH by introduction of an NH1/OsNPR1 paralog. Plant Biotechnol J 2011, 9:205-215.
25. Jun JH, Ha CM, Fletcher JC. BLADE-ON-PETIOLE1 coordinates organ determinacy and axial polarity in Arabidopsis by directly activating asymmetric leaves2. Plant Cell 2010, 22:62-76.
26. Zhang Y, Fan W, Kinkema M, Li X, Dong X. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci U S A 1999, 96:6523-6528.
27. Despres C, DeLong C, Glaze S, Liu E, Fobert PR. The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 2000, 12:279-290.
28. Johnson C, Boden E, Arias J. Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 2003, 15:1846-1858.
29. Fan W, Dong X. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 2002, 14:1377-1389.
30. Zhang Y, Tessaro MJ, Lassner M, Li X. Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 2003, 15:2647-2653.
31. Rochon A, Boyle P, Wignes T, Fobert PR, Després C. The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 2006, 18:3670-3685.
32. Boyle P, Su EL, Rochon A, Shearer HL, Murmu J, Chu JY, Fobert PR, Despres C. The BTB/POZ domain of the Arabidopsis disease resistance protein NPR1 interacts with the repression domain of TGA2 to negate its function. Plant Cell 2009, 21:3700-3713.
33. Weigel RR, Bauscher C, Pfitzner AJ, Pfitzner UM. NIMIN-1, NIMIN-2 and NIMIN-3, members of a novel family of proteins from Arabidopsis that interact with NPR1/NIM1, a key regulator of systemic acquired resistance in plants. Plant Mol Biol 2001, 46:143-160.
34. Weigel RR, Pfitzner UM, Gatz C. Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 2005, 17:1279-1291.
35. Zwicker S, Mast S, Stos V, Pfitzner AJP, Pfitzner UM. Tobacco NIMIN2 proteins control PR gene induction through transient repression early in systemic acquired resistance. Mol Plant Pathol 2007, 8:385-400.
36. Chern M, Canlas PE, Fitzgerald HA, Ronald PC. Rice NRR, a Negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1. Plant J 2005, 43:623-635.
37. Chern M, Bai W, Sze-To WH, Canlas PE, Bartley LE, Ronald PC. A rice transient assay system identifies a novel domain in NRR required for interaction with NH1/OsNPR1 and inhibition of NH1-mediated transcriptional activation. Plant Methods 2012, 8:6.
38. Chern M, Canlas PE, Ronald PC. Strong suppression of systemic acquired resistance in Arabidopsis by NRR is dependent on its ability to interact with NPR1 and its putative repression domain. Mol Plant 2008, 1:552-559.
39. Fitzgerald H, Canlas PE, Chern M, Ronald PC. Alteration of TGA factor activity in rice results in enhanced tolerance to Xanthomonas oryzae pv. oryzae. Plant J 2005, 43:335-347.
40. Mukhtar MS, Carvunis A-R, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT, Pevzner SJ, Donovan SE, Ghamsari L, Santhanam B, Romero V, Poulin MM, Gebreab F, Gutierrez BJ, Tam S, Monachello D, Boxem M, Harbort CJ, McDonald N, Gai L, Chen H, He Y, Vandenhaute J, Roth FP, Hill DE, et al. European Union Effectoromics Consortium Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 2011, 333:596-601. European Union Effectoromics Consortium.
41. Arabidopsis Interactome Mapping Consortium Evidence for network evolution in an Arabidopsis interactome map. Science 2011, 333:601-607. Arabidopsis Interactome Mapping Consortium.
42. Ding X, Richter T, Chen M, Fujii H, Seo YS, Xie M, Zheng X, Kanrar S, Stevenson RA, Dardick C, Li Y, Jiang H, Zhang Y, Yu F, Bartley LE, Chern M, Bart R, Chen X, Zhu L, Farmerie WG, Gribskov M, Zhu JK, Fromm ME, Ronald PC, Song WY. A rice kinase-protein interaction map. Plant Physiol 2009, 149:1478-1492.
43. Bracha-Drori K, Shichrur K, Katz A, Oliva M, Angelovici R, Yalovsky S, Ohad N. Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 2004, 40:419-427.
44. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 2004, 40:428-438.
45. Seo YS, Chern M, Barley LE, Han M, Jung KH, Lee I, Walia H, Richter T, Xu X, Cao P, Bai W, Ramanan R, Amonpant F, Arul L, Canlas PE, Ruan R, Park CJ, Chen X, Hwang S, Jeon JS, Ronald PC. Towards establishment of a rice stress response interactome. PLoS Genet 2011, 7:e1002020.
46. Kodama Y, Hu CD. Bimolecular fluorescence complementation (BiFC): a 5-year update and future perspectives. BioTechniques 2012, 53:285-298.
47. Li S, Pandey S, Gookin TE, Zhao Z, Wilson L, Assmann SM. Gene-sharing networks reveal organizing principles of transcriptomes in Arabidopsis and other multicellular organisms. Plant Cell 2012, 24:1362-1378.
48. Yeung KY, Dombek KM, Lo K, Mittler JE, Zhu J, Schadt EE, Bumgamer RE, Raftery AE. Construction of regulatory networks using expression time-series data of a genotyped population. Proc Natl Acad Sci U S A 2011, 108:19436-19441.
49. Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Höfert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, et al. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415:141-147.
50. Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 2003, 130:161-172.
51. Hepworth SR, Zhang Y, McKim S, Li X, Haughn GW. BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. Plant Cell 2005, 17:1434-1448.
52. Canet JV, Dobon A, Fajmonova J, Tornero P. The BLADE-ON-PETIOLE genes of Arabidopsis are essential for resistance induced by methyl jasmonate. BMC Plant Biol 2012, 12:199.
53. Robert-Seilaniantz A, Grant M, Jones JD. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 2011, 49:317-343.
54. Bart R, Chern M, Park CJ, Bartley L, Ronald PC. A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2006, 2:13. doi:10.1186/1746-4811-2-13.