A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death

Plant Journal

Volumn 43, Issue 6, 2005, Pages 873-888

  Noutoshi, Yoshiteru ^a,b   Ito, Takuya ^a   Seki, Motoaki ^a,c   Nakashita, Hideo ^d   Yoshida, Shigeo ^d   Marco, Yves ^e   Shirasu, Ken ^b   Shinozaki, Kazuo ^a,c,f  

^a RIKEN TSUKUBA INSTITUTE   (Japan)

^b SAINSBURY LABORATORY   (United Kingdom)

^c RIKEN YOKOHAMA INSTITUTE   (Japan)

^d RIKEN   (Japan)

^e LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^f RIKEN Plant Science Center   (Japan)

Author keywords

Cell death; Lesion mimic mutant; R genes; Salicylic acid; Transcription factor and global transcription

Indexed keywords

CELLS; DNA; GELS; PROTEINS; SOILS;

CELL DEATH; LESION MIMIC MUTANTS; R GENES; TRANSCRIPTION FACTOR AND GLOBAL TRANSCRIPTION;

AMINO ACIDS;

AMINO ACIDS; CELLS; NUCLEIC ACIDS; SALICYLIC ACID; SOIL;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); RALSTONIA SOLANACEARUM;

ARABIDOPSIS PROTEIN; DNA BINDING PROTEIN; SLH1 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CELL DEATH; CHROMOSOME MAP; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMIDITY; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; MOLECULAR GENETICS; PHENOTYPE; PHYSIOLOGY; PLANT CHROMOSOME; PLANT DISEASE; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; RALSTONIA SOLANACEARUM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; UPREGULATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DEATH; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; HUMIDITY; IMMUNITY, NATURAL; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT DISEASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RALSTONIA SOLANACEARUM; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 32944465711     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02500.x     Document Type: Article

References (65)

1. Axtell M.J. Staskawicz B.J. ( 2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell, 112, 369 377.
2. Belkhadir Y. Subramaniam R. Dangl J.L. ( 2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr. Opin. Plant Biol. 7, 391 399.
3. Bendahmane A. Farnham G. Moffett P. Baulcombe D.C. ( 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.
4. Bowling S.A. Clarke J.D. Liu Y. Klessig D.F. Dong X. ( 1997) The cpr 5 mutant of Arabidopsis expresses both NPR-dependent and NPRT-independent resistance. Plant Cell, 9, 1573 1584.
5. Brodersen P. Petersen M. Pike H.M. Olszak B. Skov S. Odum N. Jorgensen L.B. Brown R.E. Mundy J. ( 2002) Knockout of Arabidopsis accelerated-cell- death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 16, 490 502.
6. Cao H. Bowling S.A. Gordon A.S. Dong X. ( 1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 6, 1583 1592.
7. Cao H. Glazebrook J. Clarke J.D. 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.
8. Clough S.J. Bent A.F. ( 1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
9. Dangl J.L. Jones J.D. ( 2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826 833.
10. Dangl J.L. Dietrich R.A. Richberg M.H. ( 1996) Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell, 8, 1793 1807.
11. Deslandes L. Pileur F. Liaubet L. Camut S. Can C. Williams K. Holub E. Beynon J. Arlat M. Marco Y. ( 1998) Genetic characterization of RRS1, a recessive locus in Arabidopsis thaliana that confers resistance to the bacterial soilborne pathogen Ralstonia solanacearum. Mol. Plant Microbe Interact. 11, 659 667.
12. Deslandes L. Olivier J. Theulieres F. Hirsch J. Feng D.X. Bittner-Eddy P. Beynon J. Marco Y. ( 2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl Acad. Sci. USA, 99, 2404 2409.
13. Deslandes L. Olivier J. Peeters N. Feng D.X. Khounlotham M. Boucher C. Somssich I. Genin S. Marco Y. ( 2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl Acad. Sci. USA, 100, 8024 8029.
14. Dietrich R.A. Delaney T.P. Uknes S.J. Ward E.R. Ryals J.A. Dangl J.L. ( 1994) Arabidopsis mutants simulating disease resistance response. Cell, 77, 565 577.
15. Dong J. Chen C. Chen Z. ( 2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol. 51, 21 37.
16. Eulgem T. Rushton P.J. Robatzek S. Somssich I.E. ( 2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199 206.
17. Feys B.J. Parker J.E. ( 2000) Interplay of signaling pathways in plant disease resistance. Trends Genet. 16, 449 455.
18. Gaffney T. Friedrich L. Vernooij B. Negrotto D. Nye G. Uknes S. Ward E. Kessmann H. Ryals J. ( 1993) Requirement of salicylic acid for induction of systemic acquired resistance. Science, 261, 754 756.
19. Greenberg J.T. Ausubel F.M. ( 1993) Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 4, 327 341.
20. Hammond-Kosack K.E. Silverman P. Raskin I. Jones J. ( 1996) Race-specific elicitors of Cladosporium fulvum induce changes in cell morphology and the synthesis of ethylene and salicylic acid in tomato plants carrying the corresponding Cf disease resistance gene. Plant Physiol. 110, 1381 1394.
21. Heath M.C. ( 2000) Hypersensitive response-related death. Plant Mol. Biol. 44, 321 334.
22. Heck S. Grau T. Buchala A. Metraux J.P. Nawrath C. ( 2003) Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis-Pseudomonas, syringae pv. tomato interaction. Plant. J. 36, 342 352.
23. Hosford R.M., Jr. ( 1978) Effects of wetting period on resistance to leaf spotting of wheat, barley, and rye by Leptosphaeria herpotrichoides. Phytopathology, 68, 591 594.
24. Hulbert S.H. ( 1997) Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu. Rev. Phytopathol. 35, 293 310.
25. Hwang C.F. Bhakta A.V. Truesdell G.M. Pudlo W.M. Williamson V.M. ( 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.
26. Ito T. Motohashi R. Kuromori T. Mizukado S. Sakurai T. Kanahara H. Seki M. Shinozaki K. ( 2002) A new resource of locally transposed dissociation elements for screening gene-knockout lines in silico on the Arabidopsis genome. Plant Physiol. 129, 1695 1699.
27. Jabs T. Dietrich R.A. Dangl J.L. ( 1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science, 273, 1853 1856.
28. Jambunathan N. Siani J.M. McNellis T.W. ( 2001) A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. Plant Cell, 13, 2225 2240.
29. Jia Y. McAdams S.A. Bryan G.T. Hershey H.P. Valent B. ( 2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 4004 4014.
30. Kalde M. Barth M. Somssich I.E. Lippok B. ( 2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol. Plant Microbe Interact. 16, 295 305.
31. Kuromori T. Hirayama T. Kiyosue Y. Takabe H. Mizukado S. Sakurai T. Akiyama K. Kamiya A. Ito T. Shinozaki K. ( 2004) A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J. 37, 897 905.
32. Kwak J.M. Mori I.C. Pei Z.M. Leonhardt N. Torres M.A. Dangl J.L. Bloom R.E. Bodde S. Jones J.D. Schroeder J.I. ( 2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623 2633.
33. Lebel E. Heifetz P. Thorne L. Uknes S. Ryals J. Ward E. ( 1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J. 16, 223 233.
34. Li J. Brader G. Palva E.T. ( 2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell, 16, 319 331.
35. Lohman K.N. Gan S. John M.C. Amasino R.M. ( 1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol. Plant. 92, 322 328.
36. Mackey D. Holt B.F. Wiig A. Dangl J.L. ( 2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell, 108, 743 754.
37. Mackey D. Belkhadir Y. Alonso J.M. Ecker J.R. Dangl J.L. ( 2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112, 379 389.
38. MAPK Group ( 2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301 308.
39. Marcotte E.M. Pellegrini M. Ng H.L. Rice D.W. Yeates T.O. Eisenberg D. ( 1999) Detecting protein function and protein-protein interactions from genome sequences. Science, 285, 751 753.
40. Moffett P. Farnham G. Peart J. Baulcombe D.C. ( 2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 21, 4511 4519.
41. Nakashita H. Yoshioka K. Yasuda M. Nitta T. Arai Y. Yoshida S. Yamaguchi I. ( 2002) Probenazole induces systemic acquired resistance in tobacco through salicylic acid accumulation. Physiol. Mol. Plant Pathol. 61, 197 203.
42. Nawrath C. Heck S. Parinthawong N. Metraux J.P. ( 2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell, 14, 275 286.
43. Oldroyd G.E.D. Staskawicz B.J. ( 1998) Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl Acad. Sci. USA, 95, 10300 10305.
44. Rinehart T.A. Dean C. Weil C.F. ( 1997) Comparative analysis of non-random DNA repair following Ac transposon excision in maize and Arabidopsis. Plant J. 12, 1419 1427.
45. Robatzek S. Somssich I.E. ( 2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev. 16, 1139 1149.
46. Rushton P.J. Reinstadler A. Lipka V. Lippok B. Somssich I.E. ( 2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell, 14, 749 762.
47. Seki M. Narusaka M. Ishida J. et al. ( 2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279 292.
48. Shah J. Kachroo P. Klessig D.F. ( 1999) The Arabidopsis ssiI mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell, 11, 191 206.
49. Shao F. Golstein C. Ade J. Stoutemyer M. Dixon J.E. Innes R.W. ( 2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science, 301, 1230 1233.
50. Shirano Y. Kachroo P. Shah J. Klessig D.F. ( 2002) A gain-of-function mutation in an Arabidopsis Toll Interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell, 14, 3149 3162.
51. Shirasu K. Schulze-Lefert P. ( 2003) Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci. 8, 252 258.
52. Sticher L. Mauch-Mani B. Metraux J.P. ( 1997) Systemic acquired resistance. Annu. Rev. Phytopathol. 35, 235 270.
53. Tang X. Frederick R.D. Zhou J. Halterman D.A. Jia Y. Martin G.B. ( 1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science, 274, 2060 2063.
54. Tang X. Xie M. Kim Y.J. Zhou J. Klessig D.F. Martin G.B. ( 1999) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell, 11, 15 29.
55. Tao Y. Xie Z. Chen W. Glazebrook J. Chang H.S. Han B. Zhu T. Zou G. Katagiri F. ( 2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell, 15, 317 330.
56. Torres M.A. Dangl J.L. Jones J.D. ( 2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA, 99, 517 522.
57. Tsuge T. Tsukaya H. Uchimiya H. ( 1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development, 122, 1589 1600.
58. Valvekens D. Montagu M.V. Lijsebettens M.V. ( 1998) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl Acad. Sci. USA, 85, 5536 5540.
59. Whitham S. Dinesh-Kumar S.P. Choi D. Hehl R. Corr C. Baker B. ( 1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell, 78, 1101 1115.
60. Wildermuth M.C. Dewdney J. Wu G. Ausubel F.M. ( 2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562 565.
61. Xiao S. Brown S. Patrick E. Brearley C. Turner J.G. ( 2003) Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell, 15, 33 45.
62. Yamasaki K. Kigawa T. Inoue M. et al. ( 2005) Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell, 17, 944 956.
63. Yoshioka K. Kachroo P. Tsui F. Sharma S.B. Shah J. Klessig D.F. ( 2001) Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. Plant J. 26, 447 459.
64. 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.
65. Zhou N. Tootle T.L. Tsui F. Klessig D.F. Glazebrook J. ( 1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell, 10, 1021 1030.