A gain-of-function mutation in the arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature

Plant Physiology

Volumn 154, Issue 2, 2010, Pages 796-809

  Huang, Xiaozhen ^a   Li, Jianyong ^a   Bao, Fei ^a   Zhang, Xiaoyan ^a   Yang, Shuhua ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; PERONOSPORA;

EID: 77957745042     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.157610     Document Type: Article

References (88)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 95: 10306-10311
2. Ade J, De Young BJ, Golstein C, Innes RW (2007) Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci USA 104: 2531-2536
3. Alcazar R, Garcia AV, Parker JE, Reymond M (2009) Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc Natl Acad Sci USA 106: 334-339
4. Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JD, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295: 2077-2080
5. Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18: 1038-1051
6. Bates LS, Waldren RP, Teare ID (1972) Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207
7. Bendahmane A, Farnham G, Moffett P, Baulcombe DC (2002) Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J 32: 195-204
8. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9: 1573-1584
9. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592
10. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-63
11. Century KS, Holub EB, Staskawicz BJ (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad Sci USA 92: 6597-6601
12. Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38: 432-447
13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
14. Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139: 847-856
15. Diener AC, Li H, Zhou W, Whoriskey WJ, Nes WD, Fink GR (2000) Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell 12: 853-870
16. Dinesh-Kumar SP, Tham WH, Baker BJ (2000) Structure-function analysis of the tobacco mosaic virus resistance gene N. Proc Natl Acad Sci USA 97: 14789-14794
17. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21: 972-984
18. Dong CH, Hu X, Tang W, Zheng X, Kim YS, Lee BH, Zhu JK (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol 26: 9533-9543
19. Dong H, Deng Y, Mu J, Lu Q, Wang Y, Xu Y, Chu C, Chong K, Lu C, Zuo J (2007) The Arabidopsis Spontaneous Cell Death1 gene, encoding a zetacarotene desaturase essential for carotenoid biosynthesis, is involved in chloroplast development, photoprotection and retrograde signalling. Cell Res 17: 458-470
20. 2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457: 1154-1158
21. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209
22. Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53: 1249-1254
23. Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18: 13-21
24. Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54: 767-781
25. Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143: 973-982
26. Gray WM, Muskett PR, Chuang HW, Parker JE (2003) Arabidopsis SGT1b is required for SCF(TIR1)-mediated auxin response. Plant Cell 15: 1310-1319
27. Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41: 187-223
28. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacteriummediated plant transformation. Plant Mol Biol 42: 819-832
29. Hideg E, Barta C, Kalai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43: 1154-1164
30. Hirashima M, Tanaka R, Tanaka A (2009) Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. Plant Cell Physiol 50: 719-729
31. Howles P, Lawrence G, Finnegan J, McFadden H, Ayliffe M, Dodds P, Ellis J (2005) Autoactive alleles of the flax L6 rust resistance gene induce non-race-specific rust resistance associated with the hypersensitive response. Mol Plant Microbe Interact 18: 570-582
32. Huang X, Zhang X, Yang S (2009) A novel chloroplast-localized protein EMB1303 is required for chloroplast development in Arabidopsis. Cell Res 19: 1205-1216
33. Hwang CF, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM (2000) Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12: 1319-1329
34. Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53: 225-245
35. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA 96: 13583-13588
36. Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant Microbe Interact 20: 120-128
37. Lee BH, Kapoor A, Zhu J, Zhu JK (2006) STABILIZED1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell 18: 1736-1749
38. Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21: 2692-2702
39. Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, et al (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49: 79-90
40. Li X, Clarke JD, Zhang Y, Dong X (2001) Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact 14: 1131-1139
41. Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98: 329-339
42. Li Y, Yang S, Yang H, Hua J (2007) The TIR-NB-LRR gene SNC1 is regulated at the transcript level by multiple factors. Mol Plant Microbe Interact 20: 1449-1456
43. Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666: 142-157
44. Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24: 445-466
45. Mauch-Mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8: 203-212
46. Mayda E, Mauch-Mani B, Vera P (2000) Arabidopsis dth9 mutation identifies a gene involved in regulating disease susceptibility without affecting salicylic acid-dependent responses. Plant Cell 12: 2119-2128
47. McDowell JM, Cuzick A, Can C, Beynon J, Dangl JL, Holub EB (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J 22: 523-529
48. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809-834
49. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
50. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19: 1403-1414
51. Muskett PR, Kahn K, Austin MJ, Moisan LJ, Sadanandom A, Shirasu K, Jones JD, Parker JE (2002) Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14: 979-992
52. Nanjo T, Kobayashi M, Yoshiba Y, Sanada Y, Wada K, Tsukaya H, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999) Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J 18: 185-193
53. Noel L, Moores TL, van Der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11: 2099-2112
54. O'Kane D, Gill V, Boyd P, Burdon R (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198: 371-377
55. Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, Daniels MJ (1996) Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8: 2033-2046
56. Pfannschmidt T, Schutze K, Fey V, Sherameti I, Oelmuller R (2003) Chloroplast redox control of nuclear gene expression: a new class of plastid signals in interorganellar communication. Antioxid Redox Signal 5: 95-101
57. Rafiqi M, Bernoux M, Ellis JG, Dodds PN (2009) In the trenches of plant pathogen recognition: role of NB-LRR proteins. Semin Cell Dev Biol 20: 1017-1024
58. Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57: 400-412
59. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279: 11736-11743
60. Scheel D (1998) Resistance response physiology and signal transduction. Curr Opin Plant Biol 1: 305-310
61. Schneider JC, Hugly S, Somerville CR (1995) Chilling-sensitivemutants of Arabidopsis. Plant Mol Biol Rep 13: 11-17
62. Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61: 661-671
63. Seo PJ, Lee AK, Xiang F, Park CM (2008) Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol 49: 334-344
64. Snider CS, Hsiang T, Zhao G, Griffith M (2000) Role of ice nucleation and antifreeze activities in pathogenesis and growth of snow molds. Phytopathology 90: 354-361
65. Someya N, Niinuma K, Kimura M, Yamaguchi I, Hamamoto H (2004) Pattern of N gene-mediated systemic hypersensitive response and turnover of viral replicase protein in tobacco. Arch Virol 149: 2105-2113
66. Stokes TL, Richards EJ (2002) Induced instability of two Arabidopsis constitutive pathogen-response alleles. Proc Natl Acad Sci USA 99: 7792-7796
67. Takken FL, Albrecht M, Tameling WI (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9: 383-390
68. Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL, Haring MA, Cornelissen BJ (2002) The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14: 2929-2939
69. Tanaka R, Hirashima M, Satoh S, Tanaka A (2003) The Arabidopsisaccelerated cell death gene ACD1 is involved in oxygenation of pheophorbide a: inhibition of the pheophorbide a oxygenase activity does not lead to the "stay-green" phenotype in Arabidopsis. Plant Cell Physiol 44: 1266-1274
70. Tao Y, Yuan F, Leister RT, Ausubel FM, Katagiri F (2000) Mutational analysis of the Arabidopsis nucleotide binding site-leucine-rich repeat resistance gene RPS2. Plant Cell 12: 2541-2554
71. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187-1194
72. Tsutsui T, Kato W, Asada Y, Sako K, Sato T, Sonoda Y, Kidokoro S, Yamaguchi-Shinozaki K, Tamaoki M, Arakawa K, et al (2009) DEAR1, a transcriptional repressor of DREB protein that mediates plant defense and freezing stress responses in Arabidopsis. J Plant Res 122: 633-643
73. Ueda H, Yamaguchi Y, Sano H (2006) Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol Biol 61: 31-45
74. van der Biezen EA, Freddie CT, Kahn K, Parker JE, Jones JD (2002) Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NBLRR genes and confers downy mildew resistance through multiple signalling components. Plant J 29: 439-451
75. van Ooijen G, Mayr G, Kasiem MM, Albrecht M, Cornelissen BJ, Takken FL (2008) Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59: 1383-1397
76. Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998) A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10: 1439-1452
77. Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152: 401-412
78. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565
79. Xiao S, Charoenwattana P, Holcombe L, Turner JG (2003) The Arabidopsis genes RPW8.1 and RPW8.2 confer induced resistance to powdery mildew diseases in tobacco. Mol Plant Microbe Interact 16: 289-294
80. Xin Z, Browse J (1998) Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc Natl Acad Sci USA 95: 7799-7804
81. Xin Z, Mandaokar A, Chen J, Last RL, Browse J (2007) Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. Plant J 49: 786-799
82. Yang S, Hua J (2004) A haplotype-specific resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 16: 1060-1071
83. Yang S, Yang H, Grisafi P, Sanchatjate S, Fink GR, Sun Q, Hua J (2006) The BON/CPN gene family represses cell death and promotes cell growth in Arabidopsis. Plant J 45: 166-179
84. Yi H, Richards EJ (2007) A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19: 2929-2939
85. Zhang Y, Goritschnig S, Dong X, Li X (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15: 2636-2646
86. Zhou F, Mosher S, Tian M, Sassi G, Parker J, Klessig DF (2008) The Arabidopsis gain-of-function mutant ssi4 requires RAR1 and SGT1b differentially for defense activation and morphological alterations. Mol Plant Microbe Interact 21: 40-49
87. Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu JK, Hasegawa PM, Bohnert HJ, Shi H, Yun DJ, et al (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 105: 4945-4950
88. Zhu Y, Qian W, Hua J (2010) Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog 6: e1000844