High humidity suppresses ssi4-mediated cell death and disease resistance upstream of MAP kinase activation, H2O2 production and defense gene expression

Plant Journal

Volumn 39, Issue 6, 2004, Pages 920-932

  Zhou, Fasong ^a   Menke, Frank L H ^a,b   Yoshioka, Keiko ^a,c   Moder, Wolfgang ^a,c   Shirano, Yumiko ^a   Klessig, Daniel F ^a  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Arabidopsis; Cell death; Defense responses; Humidity; ssi4; TIR NBS LRR

Indexed keywords

ATMOSPHERIC HUMIDITY; CELLS; DISEASES; GENETIC ENGINEERING; PROTEINS;

GAIN-OF-FUNCTION MUTATION; OOMYCETE PATHOGENS; PATHOGENESIS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; PLANT RNA; SSI4 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CELL DEATH; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMIDITY; INNATE IMMUNITY; ISOLATION AND PURIFICATION; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; CELL DEATH; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, PLANT; HUMIDITY; HYDROGEN PEROXIDE; IMMUNITY, NATURAL; MITOGEN-ACTIVATED PROTEIN KINASES; RNA, PLANT;

CELLS; DISEASES; GENETIC ENGINEERING; HUMIDITY; PLANTS;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); ERYSIPHALES; EUKARYOTA;

EID: 4944233157     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02180.x     Document Type: Article

References (47)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker, J.E. (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. Agrios, G.N. (1997) Plant Pathology. San Diego, CA: Academic Press.
3. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M. and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415, 977-983.
4. Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F. and Dong, X. (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell, 6, 1845-1857.
5. Chen, W., Provart, N.J., Glazebrook, J. et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell, 14, 559-574.
6. Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell, 10, 557-569.
7. Creutz, C.E., Tomsig, J.L., Snyder, S.L., Gautier, M.C., Skouri, F., Beisson, J. and Cohen, J. (1998) The copines, a novel class of C2 domain-containing, calcium-dependent, phospholipid-binding proteins conserved from Paramecium to humans. J. Biol. Chem. 273, 1393-1402.
8. Dangl, J.L. and Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
9. Dempsey, D.A., Shah, J. and Klessig, D.F. (1999) Salicylic acid and disease resistance in pants. Crit. Rev. Plant Sci. 18, 547-575.
10. Droillard, M., Boudsocq, M., Barbier-Brygoo, H. and Lauriere, C. (2002) Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett. 527, 43-50.
11. Eulgem, T., Rushton, P.J., Robatzek, S. and Somssich, I.E. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206.
12. Falk, A., Feys, B.J., Frost, L.N., Jones, J.D., Daniels, M.J. and Parker, J.E. (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic upases. Proc. Natl Acad. Sci. USA, 96, 3292-3297.
13. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993) Requirement of salicylic-acid for the induction of systemic acquired-resistance. Science, 261, 754-756.
14. Glazebrook, J. (2001) Genes controlling expression of defence responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4, 301-308.
15. Hammond-Kosack, K.E., Silverman, P., Raskin, I. and 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.
16. Jambunathan, N., Siani, J.M. and McNellis, T.W. (2001) A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. Plant Cell, 13, 2225-2240.
17. Jin, H., Liu, Y., Yang, K.Y., Kim, C.Y., Baker, B. and Zhang, S. (2003) Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J. 33, 719-731.
18. Kachroo, P., Yoshioka, K., Shah, J., Dooner, H.K. and Klessig, D.F. (2000) Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. Plant Cell, 12, 677-690.
19. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K.A., Dangl, J.L. and Dietrich, R.A. (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26, 403-410.
20. Mauch, F., Mauch-Mani, B., Gaille, C., Kull, B., Haas, D. and Reimmann, C. (2001) Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. Plant J. 25, 67-77.
21. May, M.J., Hammond-Kosack, K.E. and Jones, J. (1996) Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defence response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110, 1367-1379.
22. Menke, F.L.H., van Pelt, J.A., Pieterse, C.J.M., Klessig, D.F. (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16, 897-907.
23. Nawrath, C. and Metraux, J.P. (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell, 11, 1393-1404.
24. Nuhse, T.S., Peck, S.C., Hirt, H. and Boller, T. (2000) Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. J. Biol. Chem. 275, 7521-7526.
25. Rate, D.N., Cuenca, J.V., Bowman, G.R., Guttman, D.S. and Greenberg, J.T. (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defences, and cell growth. Plant Cell, 11, 1695-1708.
26. Ren, D., Yang, H. and Zhang, S. (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J. Biol. Chem. 277, 559-565.
27. Reuber, T.L., Plotnikova, J.M., Dewdney, J., Rogers, E.E., Wood, W. and Ausubel, F.M. (1998) Correlation of defence gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473-485.
28. Robatzek, S. and Somssich, I.E. (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. Plant J. 28, 123-133.
29. Robatzek, S. and Somssich, I.E. (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defence. Genes Dev. 16, 1139-1149.
30. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D. (1999) Rapid Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell, 11, 273-287.
31. Shah, J., Kachroo, P. and Klessig, D.F. (1999) The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell, 11, 191-206.
32. Shirano, Y., Kachroo, P., Shah, J. and 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 defence responses and results in enhanced disease resistance. Plant Cell, 14, 3149-3162.
33. Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A. and Lamb, C. (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defence mechanisms. Plant Cell, 9, 261-270.
34. Shirasu, K., Lahaye, T., Tan, M.W., Zhou, F., Azevedo, C. and Schulze-Lefert, P. (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell, 99, 355-366.
35. Tao, Y., Xie, Z.Y., Chen, W.Q., Glazebrook, J., Chang, H.S., Han, B., Zhu, T., Zou, G.Z. and Katagiri, F. (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell, 15, 317-330.
36. Verberne, M.C., Verpoorte, R., Bol, J.F., Mercado-Blanco, J. and Linthorst, H.J. (2000) Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat. Biotechnol. 18, 779-783.
37. Weymann, K., Hunt, M., Uknes, S., Neuenschwander, U., Lawton, K., Steiner, H.Y. and Ryals, J. (1995) Suppression and restoration of lesion formation in Arabidopsis Isd mutants. Plant Cell, 7, 2013-2022.
38. Whitham, S.A., Quan, S., Chang, H.S., Cooper, B., Estes, B., Zhu, T., Wang, X. and Hou, Y.M. (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J. 33, 271-283.
39. Xiao, S., Ellwood, S., Calis, O., Patrick, E., Li, T., Coleman, M. and Turner, J.G. (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science, 291, 118-120.
40. Xiao, S., Brown, S., Patrick, E., Brearley, C. and 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.
41. Yang, S. and Hua, J., (2004) A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell, 16, 1060-1071.
42. Yoshioka, K., Kachroo, P., Tsui, F., Sharma, S.B., Shah, J. and Klessig, D.F. (2001) Environmentally sensitive, SA-dependent defence responses in the cpr22 mutant of Arabidopsis. Plant J. 26, 447-459.
43. Zhang, S. and Klessig, D.F. (1998a) Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc. Natl Acad. Sci. USA, 95, 7433-7438.
44. Zhang, S. and Klessig, D.F. (1998b) The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl Acad. Sci. USA, 95, 7225-7230.
45. Zhang, S. and Klessig, D.F. (2001) MAPK cascades in plant defence signaling. Trends Plant Sci. 6, 520-527.
46. Zhang, S., Du, H. and Klessig, D.F. (1998) Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell, 10, 435-450.
47. Zhou, F., Andersen, C.H., Burhenne, K., Fischer, P.H., Collinge, D.B. and Thordal-Christensen, H. (2000) Proton extrusion is an essential signalling component in the HR of epidermal single cells in the barley-powdery mildew interaction. Plant J. 23, 245-254.