The jasmonate signaling pathway in tomato regulates susceptibility to a toxin-dependent necrotrophic pathogen

详细信息    查看全文

• 作者：Mayumi Egusa (1)
  Rika Ozawa (2)
  Junji Takabayashi (2)
  Hiroshi Otani (1)
  Motoichiro Kodama (1)
  
• 关键词：Alternaria ; Disease susceptibility ; Host ; specific toxin ; AAL ; toxin ; Jasmonic acid ; Tomato
• 刊名：Planta
• 出版年：2009
• 出版时间：March 2009
• 年：2009
• 卷：229
• 期：4
• 页码：965-976
• 全文大小：729KB
• 参考文献：1. Akamatsu H, Itoh Y, Kodama M, Otani H, Kohmoto K (1997) AAL-toxin-deficient mutants of / Alternaria alternata tomato pathotype by restriction enzyme-mediated integration. Phytopathology 87:967鈥?72 CrossRef
  2. Akamatsu H, Otani H, Kodama M (2003) Characterization of a gene cluster for host-specific AAL-toxin biosynthesis in the tomato pathotype of / Alternaria alternata. Abstracts of the 22nd fungal genetics conference, Asilomar, pp 121
  3. Arie T, Kaneko I, Yoshida T, Noguchi M, Nomura Y, Yamaguchi I (2000) Mating-type genes from asexual phytopathogenic Ascomycetes / Fusarium oxysporum and / Alternaria alternata. Mol Plant Microbe Interact 13:1330鈥?339 CrossRef
  4. Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in / Arabidopsis protoplasts requires jasmonate-, ethylene-, salicylate-dependent signaling pathways. Plant Cell 12:1823鈥?835 CrossRef
  5. Berger S, Bell E, Mullet JE (1996) Two methyl jasmonate-insensitive mutants show altered expression of / AtVsp in response to methyl jasmonate and wounding. Plant Physiol 111:525鈥?31
  6. Bottini AT, Gilchrist DG (1981) Phytotoxins. I. A 1-aminodimethylheptadecapentol from / Alternaria alternata f. sp. / lycopersici. Tetrahedron Lett 22:2719鈥?722 CrossRef
  7. Bottini AT, Bowen JR, Gilchrist DG (1981) Phytotoxins. II. Characterization of a phytotoxic fraction from / Alternaria alternata f. sp. / lycopersici. Tetrahedron Lett 22:2723鈥?726 CrossRef
  8. Brandwagt BF, Mesbah LA, Takken FLW, Laurent PL, Kneppers TJA, Hille J, Nijkamp HJJ (2000) A longevity assurance gene homolog of tomato mediates resistance to / Alternaria alternata f. sp. / lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 97:4961鈥?966 CrossRef
  9. Cohen Y, Gisi U, Niderman T (1993) Local and systemic protection against / Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester. Phytopathology 83:1054鈥?062 CrossRef
  10. Farmer EE, Johnson RR, Ryan CA (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol 98:995鈥?002 CrossRef
  11. Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) / Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751鈥?59 CrossRef
  12. Friesen TL, Faris JD, Solomon PS, Oliver RP (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10:1421鈥?428 CrossRef
  13. Gilchrist DG, Grogan RG (1976) Production and nature of a host-specific toxin from / Alternaria alternata f. sp. / lycopersici. Phytopathology 66:165鈥?71 CrossRef
  14. Gilchrist DG, Wang H, Bostock RM (1995) Sphingosine-related mycotoxins in plant and animal disease. Can J Bot 73:S459鈥揝467 CrossRef
  15. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205鈥?27 CrossRef
  16. Gundlach H, Muller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89:2389鈥?393 CrossRef
  17. Howe GA, Ryan CA (1999) Suppressors of systemin signaling identify genes in the tomato wound responses pathway. Genetics 153:1411鈥?421
  18. Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067鈥?077 CrossRef
  19. Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, Kohmoto K (2000) Cloning and characterization of a cyclic peptide synthetase gene from / Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant Microbe Interact 13:742鈥?53 CrossRef
  20. Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to / Pseudomonas syringae conferred by an / Arabidopsis thaliana coronatine-insensitive ( / coi1) mutation occurs through two distinct mechanisms. Plant J 26:509鈥?22 CrossRef
  21. Kodama M, Otani H, Kohmoto K (1995) A rapid and sensitive procedure for the quantitative detection of AL-toxin by fluorescence derivatization and separation by high performance liquid chromatography. Ann Phytopathol Soc Jpn 61:477鈥?80
  22. Kohmoto K, Otani H (1991) Host recognition by toxigenic plant pathogens. Experientia 47:755鈥?64 CrossRef
  23. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325鈥?31 CrossRef
  24. Lanahan MB, Yen H-C, Giovannoni JJ, Klee HJ (1994) The / Never Ripe mutation blocks ethylene perception in tomato. Plant Cell 6:521鈥?30 CrossRef
  25. Laurie-Berry N, Joardar V, Street IH, Kunkel BN (2006) The / Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by / Pseudomonas syringae. Mol Plant Microbe Interact 19:789鈥?00 CrossRef
  26. Li C, Liu G, Xu C, Lee GI, Bauer P, Ling H-Q, Ganal MW, Howe GA (2003) The tomato / suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646鈥?661 CrossRef
  27. Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126鈥?43 CrossRef
  28. Lightner J, Pearce G, Ryan CA, Browse J (1993) Isolation of signaling mutants of tomato ( / Lycopersicon esculentum). Mol Gen Genet 241:595鈥?01 CrossRef
  29. Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) / JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in / Arabidopsis. Plant Cell 16:1938鈥?950 CrossRef
  30. McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an / Arabidopsis mutant. Plant Cell 8:403鈥?16 CrossRef
  31. Moore T, Martineau B, Bostock RM, Lincoln JE, Gilchrist DG (1999) Molecular and genetic characterization of ethylene involvement in mycotoxin-induced plant cell death. Physiol Mol Plant Pathol 54:73鈥?5 CrossRef
  32. Moussatos VV, Yang SF, Ward B, Gilchrist DG (1994) AAL-toxin induced physiological changes in / Lycopersicon esculentum Mill: role for ethylene and pyrimidine intermediates in necrosis. Physiol Mol Plant Pathol 44:455鈥?68 CrossRef
  33. Nishimura S, Kohmoto K (1983) Host-specific toxins and chemical structures from / Alternaria species. Annu Rev Phytopathol 21:87鈥?16 CrossRef
  34. Nojiri H, Sugimori M, Yamane H, Nishimura Y, Yamada A, Shibuya N, Kodama O, Murofushi N, Omori T (1996) Involvement of jasmonic acid in elicitor-induced phytoalexin production in suspension-cultured rice cells. Plant Physiol 110:387鈥?92
  35. O鈥橠onnell PJ, Jones JB, Antoine FR, Ciardi J, Klee HJ (2001) Ethylene-dependent salicylic acid regulates an expanded cell death response to a plant pathogen. Plant J 25:315鈥?23 CrossRef
  36. O鈥橠onnell PJ, Schmelz E, Block A, Miersch O, Wasternack C, Jones JB, Klee HJ (2003) Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiol 133:1181鈥?189 CrossRef
  37. Otani H, Kohmoto K, Kodama M, Nishimura S (1991) Role of host-specific toxins in the pathogensis of / Alternaria alternata. In: Patil SS, Ouchi S, Mills D, Vance C (eds) Molecular strategies of pathogens and host palnts. Springer, New York, pp 139鈥?49
  38. Otani H, Kohmoto K, Kodama M (1995) / Alternaria toxins and their effects on host plants. Can J Bot 73:S453鈥揝458 CrossRef
  39. Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372鈥?79 CrossRef
  40. Spassieva SD, Markham JE, Hille J (2002) The plant disease resistance gene / Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J 32:561鈥?72 CrossRef
  41. Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an / Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837鈥?840 CrossRef
  42. Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of / Arabidopsis are susceptible to the soil fungas / Pythium irregulare. Plant J 15:747鈥?54 CrossRef
  43. Thaler J, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135:530鈥?38 CrossRef
  44. Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in / Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107鈥?5111 CrossRef
  45. Thomma BPHJ, Eggermont K, Broekaert WF, Cammue BPA (2000) Disease development of several fungi on / Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol Biochem 38:421鈥?27 CrossRef
  46. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with / Pseudomonas sytingae pv. / tomato DC3000. Mol Plant Microbe Interact 20:955鈥?65 CrossRef
  47. Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of / Arabidopsis. Proc Natl Acad Sci USA 95:7209鈥?214 CrossRef
  48. Wang H, Jones C, Ciacci-Zanella J, Holt T, Gilchrist DG, Dickman MB (1996) Fumonisins and / Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc Natl Acad Sci USA 93:3461鈥?465 CrossRef
  49. Wasternack C (2007) Jasmonates: An update on biosynthesis, signal transduction and action in plant stress responses, growth and development. Ann Bot 100:681鈥?97 CrossRef
  50. Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato鈥攔ole of jasmonic acid. J Plant Physiol 163:297鈥?06 CrossRef
  51. Yamagishi D, Akamatsu H, Otani H, Kodama M (2006) Pathological evaluation of host-specific AAL-toxins and fumonisin mycotoxins produced by / Alternaria and / Fusarium species. J Gen Plant Pathol 72:323鈥?27 CrossRef
  52. Yoder OC, Scheffer RP (1969) Role of toxin in early interactions of / Helminthosporium victoriae with susceptible and resistant oat tissue. Phytopathology 59:1954鈥?959
  53. Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) Virulence systems of / Pseudomonas syringae pv. / tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485鈥?99 CrossRef
  
• 作者单位：Mayumi Egusa (1)
  Rika Ozawa (2)
  Junji Takabayashi (2)
  Hiroshi Otani (1)
  Motoichiro Kodama (1)
  
  1. Laboratory of Plant Pathology, Faculty of Agriculture, Tottori University, 4-101 Koyama-Minami, Tottori, 680-8553, Japan
  2. Center for Ecological Research, Kyoto University, Hirano 2-509-3, Otsu, 520-2113, Japan
  

文摘

The plant hormone, jasmonic acid (JA), is known to have a critical role in both resistance and susceptibility against bacterial and fungal pathogen attack. However, little is known about the involvement of JA in the interactions between plants and toxigenic necrotrophic fungal pathogens. Using the tomato pathotype of Alternaria alternata (Aa) and its AAL-toxin/tomato interaction as a model system, we demonstrate a possible role for JA in susceptibility of plants against pathogens, which utilize host-specific toxins as virulence effectors. Disease development and in planta growth of the tomato pathotype of Aa were decreased in the def1 mutant, defective in biosynthesis of JA, compared with the wild-type (WT) cultivar. Exogenous methyl jasmonate (MeJA) application restored pathogen disease symptoms to the def1 mutant and led to increased disease in the WT. On the other hand, necrotic cell death was similarly induced by AAL-toxin both on def1 and WT, and MeJA application to the tomatoes did not affect the degree of cell death by the toxin. These results indicate that the JA-dependent signaling pathway is not involved in host basal defense responses against the tomato pathotype of Aa, but rather might affect pathogen acceptability via a toxin-independent manner. Data further suggest that JA has a promotional effect on susceptibility of tomato to toxigenic and necrotrophic pathogens, such that pathogens might utilize the JA signaling pathway for successful infection.