Differences in cell death induction by Phytophthora elicitins are determined by signal components downstream of MAP kinase kinase in different species of Nicotiana and cultivars of Brassica rapa and Raphanus sativus

Plant Physiology

Volumn 138, Issue 3, 2005, Pages 1491-1504

  Takemoto, Daigo ^a   Hardham, Adrienne R ^a   Jones, David A ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; GENES; PLANT CELL CULTURE;

CELL DEATH; PLANT-PATHOGEN INTERACTIONS; TOXIN SENSITIVITY;

CELLS;

CELLS; CULTURE MEDIA; ENZYMES; PLANTS;

ALTERNARIA; ALTERNARIA BRASSICICOLA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA RAPA; BRASSICA RAPA SUBSP. RAPA; NICOTIANA; PHYTOPHTHORA; PHYTOPHTHORA ELICITINS; PHYTOPHTHORA NICOTIANAE; RAPHANUS SATIVUS;

ALGAL PROTEIN; ELICITIN, PHYTOPHTHORA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MYCOTOXIN;

ARTICLE; CELL DEATH; CYTOLOGY; DRUG EFFECT; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; RADISH; SIGNAL TRANSDUCTION; TOBACCO; TURNIP;

ALGAL PROTEINS; BRASSICA RAPA; CELL DEATH; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MYCOTOXINS; PHYTOPHTHORA; PLANT DISEASES; RAPHANUS; SIGNAL TRANSDUCTION; TOBACCO;

EID: 27244458984     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.058388     Document Type: Article

References (68)

1. Alfano JR, Collmer A (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8: 1683-1698
2. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983
3. Baillieul F, de Ruffray P, Kauffmann S (2003) Molecular cloning and biological activity of α-, β-, and γ-megaspermin, three elicitins secreted by Phytophthora megasperma H20. Plant Physiol 131: 155-166
4. Blein J-P, Coutos-Thevenot P, Marion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7: 293-296
5. Boissy G, de La Fortelle E, Kahn R, Huet J-C, Bricogne G, Pernollet J-C, Brunie S (1996) Crystal structure of a fungal elicitor secreted by Phytophthora cryptogea, a member of a novel class of plant necrotic proteins. Structure 4: 1429-1439
6. Bonnet P, Bourdon E, Ponchet M, Blein J-P, Ricci P (1996) Acquired resistance triggered by elicitins in tobacco and other plants. Eur J Plant Pathol 102: 181-192
7. Bourque S, Binet M-N, Ponchet M, Pugin A, Lebrun-Garcia A (1999) Characterization of the cryptogein binding sites on plant plasma membranes. J Biol Chem 274: 34699-34705
8. Colas V, Conrod S, Venard P, Keller H, Ricci P, Panabières F (2001) Elicitin genes expressed in vitro by certain tobacco isolates of Phytophthora parasitica are down regulated during compatible interactions. Mol Plant Microbe Interact 14: 326-335
9. Cordelier S, de Ruffray P, Fritig B, Kauffmann S (2003) Biological and molecular comparison between localized and systemic acquired resistance induced in tobacco by a Phytophthora megasperma glycoprotein elicitin. Plant Mol Biol 51: 109-118
10. Cornelissen BJ, Horowitz J, van Kan JAL, Goldberg RB, Bol JF (1987) Structure of tobacco genes encoding pathogenesis-related proteins from the PR-1 group. Nucleic Acids Res 15: 6799-6811
11. Curtis MJ, Wolpert TJ (2004) The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J 38: 244-259
12. Devadas SK, Raina R (2002) Preexisting systemic acquired resistance suppresses hypersensitive response-associated cell death in Arabidopsis hrl1 mutant. Plant Physiol 128: 1234-1244
13. Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88: 685-694
14. Dodds PN, Lawrence GJ, Catanzariti A-M, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16: 755-768
15. Epple P, Mack AA, Morris VRF, Dangl JL (2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc Natl Acad Sci USA 100: 6831-6836
16. Gabor BK, O'Gara ET, Philip BA, Horan DP, Hardham AR (1993) Monoclonal antibodies specific for Phytophthora cinnamomi and their application in two rapid diagnostic assays. Plant Dis 77: 1189-1197
17. Hendrix JW (1970) Sterols in growth and reproduction of fungi. Annu Rev Phytopathol 8: 111-130
18. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907
19. Kamoun S, Young M, Glascock CB, Tyler BM (1993) Extracellular protein elicitors from Phytophthora: host specificity and induction of resistance to bacterial and fungal phytopathogens. Mol Plant Microbe Interact 6: 15-25
20. Kamoun S, van West P, Vleeshouwers VGAA, de Groot KE, Govers F (1998) Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10: 1413-1425
21. Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S, Katou S, Yoshioka H, Terauchi R (2003) Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol Plant Pathol 4: 383-391
22. Kapila J, de Rycke R, van Montagu M, Angenon G (1997) An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci 122: 101-108
23. Kawai-Yamada M, Ohori Y, Uchimiya H (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16: 21-32
24. Keizer DW, Schuster B, Grant BR, Gayler KR (1998) Interactions between elicitins and radish Raphanus sativus. Planta 204: 480-489
25. Keller H, Blein J-P, Bonnet P, Ricci P (1996) Physiological and molecular characteristics of elicitin-induced systemic acquired resistance in tobacco. Plant Physiol 110: 365-376
26. Keogh RC, Deverall BJ, McLeod S (1980) Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans Br Mycol Soc 74: 329-333
27. Kliebenstein DJ, Dietrich RA, Martin AC, Last RL, Dangl JL (1999) LSD1 regulates salicylic acid induction of copper zinc Superoxide dismutase in Arabidopsis thaliana. Mol Plant Microbe Interact 12: 1022-1026
28. Lahaye T (2004) Illuminating the molecular basis of gene-for-gene resistance; Arabidopsis thaliana RRS1-R and its interaction with Ralstonia solanacearum popP2. Trends Plant Sci 9: 1-4
29. Lazo GR, Stein PA, Ludwig RA (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology 9: 963-967
30. Lorrain S, Vailleau F, Balaqué C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8: 263-271
31. MacDonald MV, Ingram DS (1986) Towards the selection in vitro for resistance to Alternaria brassicicola (Schw.) Wilts., in Brassica napus ssp. oleifera (Metzg.) Sinsk., winter oilseed rape. New Phytol 104: 621-629
32. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54: 23-61
33. Mayama S, Tani T, Midland SL, Sims JJ, Keen NT (1986) The purification of victorin and its phytoalexin elicitor activity in oat leaves. Physiol Mol Plant Pathol 29: 1-18
34. Mikes V, Milat M-L, Ponchet M, Panabières F, Ricci P, Blein J-P (1998) Elicitins, proteinaceous elicitors of plant defense, are a new class of sterol carrier proteins. Biochem Biophys Res Commun 245: 133-139
35. Milat M-L, Ricci P, Bonnet P, Blein J-P (1991) Capsidiol and ethylene production by tobacco cells in response to cryptogein, an elicitor from Phytophthora cryptogea. Phytochemistry 30: 2171-2173
36. Monteiro A, Gabelman WH, Williams PH (1988) Use of sodium chloride solution to overcome self-incompatibility in Brassica campestris. HortScience 23: 876-877
37. Montesano M, Brader G, Palva ET (2003) Pathogen derived elicitors: searching for receptors in plants. Mol Plant Pathol 4: 73-79
38. Navarre DA, Wolpert TJ (1999) Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell 11: 237-249
39. Osman H, Vauthrin S, Mikes V, Milat M-L, Panabières F, Marais A, Brunie S, Maume B, Ponchet M, Blein J-P (2001) Mediation of elicitin activity on tobacco is assumed by elicitin-sterol complexes. Mol Biol Cell 12: 2825-2834
40. Otani H, Kohnobe A, Kodama M, Kohmoto K (1998) Production of a host-specific toxin by germinating spores of Alternaria brassicicola. Physiol Mol Plant Pathol 52: 285-295
41. Peart JR, Lu R, Sadanandom A, Malcuit I, Moffett P, Brice DC, Schauser L, Jaggard DAW, Xiao S, Coleman MJ, et al (2002) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc Natl Acad Sci USA 99: 10865-10869
42. Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux J-P, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103-2113
43. Ponchet M, Panabières F, Milat M-L, Mikes V, Montillet J-L, Suty L, Triantaphylides C, Tirilly Y, Blein J-P (1999) Are elicitins cryptograms in plant-Oomycete communications? Cell Mol Life Sci 56: 1020-1047
44. Qutob D, Huitema E, Gijzen M, Kamoun S (2003) Variation in structure and activity among elicitins from Phytophthora sojae. Mol Plant Pathol 4: 119-124
45. Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277: 559-565
46. Ricci P, Bonnet P, Huet JC, Sallantin M, Beauvais-Cante F, Bruneteau M, Billard V, Michel G, Pernollet JC (1989) Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur J Biochem 183: 555-563
47. Ricci P, Trentin F, Bonnet P, Venard P, Mouton-Perronnet F, Bruneteau M (1992) Differential production of parasiticein, an elicitor of necrosis and resistance in tobacco, by isolates of Phytophthora parasitica. Plant Pathol 41: 298-307
48. Rustérucci C, Stallaert V, Milat M-L, Pugin A, Ricci P, Blein J-P (1996) Relationship between active oxygen species, lipid peroxidation, necrosis, and phytoalexin production induced by elicitins in Nicotiana. Plant Physiol 111: 885-891
49. Shapiro AD, Zhang C (2001) The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis. Plant Physiol 127: 1089-1101
50. Sharma PC, Ho A, Shimizu T, Terauchi R, Kamoun S, Saitoh H (2003) Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana. Mol Genet Genomics 269: 583-591
51. Stone JM, Heard JE, Asai T, Ausubel FM (2000) Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12: 1811-1822
52. Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33: 775-792
53. 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
54. Tavernier E, Wendehenne D, Blein J-P, Pugin A (1995) Involvement of free calcium in action of cryptogein, a proteinaceous elicitor of hypersensitive reaction in tobacco cells. Plant Physiol 109: 1025-1031
55. Tyler BM (2002) Molecular basis of recognition between Phytophthora pathogens and their hosts. Annu Rev Phytopathol 40: 137-167
56. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4: 645-656
57. Vauthrin S, Mikes V, Milat M-L, Ponchet M, Maume B, Osman H, Blein J-P (1999) Elicitins trap and transfer sterols from micelles, liposomes and plant plasma membranes. Biochim Biophys Acta 1419: 335-342
58. Waldron J, Peace CP, Searle IR, Furtado A, Wade N, Findlay I, Graham MW, Carroll BJ (2002) Randomly amplified DNA fingerprinting: a culmination of DNA marker technologies based on arbitrarily-primed PCR amplification. J Biomed Biotechnol 2: 141-150
59. Wang H, Li J, Bostock RM, Gilchrist DG (1996) Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8: 375-391
60. Williams PH, Hill CB (1986) Rapid-cycling populations of Brassica. Science 232: 1385-1389
61. Yang K-Y, Liu YD, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98: 741-746
62. Yao N, Tada Y, Park P, Nakayashiki H, Tosa Y, Mayama S (2001) Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. Plant J 28: 13-26
63. 2 accumulation and resistance to Phytophthora infestans. Plant Cell 15: 706-718
64. Yu LM (1995) Elicitins from Phytophthora and basic resistance in tobacco. Proc Natl Acad Sci USA 92: 4088-4094
65. Zhang C, Gutsche AT, Shapiro AD (2004) Feedback control of the Arabidopsis hypersensitive response. Mol Plant Microbe Interact 17: 357-365
66. Zhang S, Du H, Klessig DF (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: 435-449
67. Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6: 520-527
68. Zhang S, Liu Y, Klessig DF (2000) Multiple levels of tobacco WIPK activation during the induction of cell death by fungal elicitins. Plant J 23: 339-347