Induced resistance in tomato plants to the toxin-dependent necrotrophic pathogen Alternaria alternata

Physiological and Molecular Plant Pathology

Volumn 73, Issue 4-5, 2008, Pages 67-77

  Egusa, Mayumi ^a   Akamatsu, Hajime ^b   Tsuge, Takashi ^c   Otani, Hiroshi ^b   Kodama, Motoichiro ^b  

^a TOTTORI UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

AAL toxin; Alternaria alternata; Host specific toxin; Induced resistance; Jasmonic acid; Salicylic acid; Solanum lycopersicum

Indexed keywords

ALTERNARIA; ALTERNARIA ALTERNATA; LYCOPERSICON ESCULENTUM; SOLANUM;

EID: 67651089783     PISSN: 08855765     EISSN: 10961178     Source Type: Journal    
DOI: 10.1016/j.pmpp.2009.02.001     Document Type: Article

References (70)

1. Jones J.D.G., and Dangl J.L. The plant immune system. Nature 444 (2006) 323-329
2. Nurnberger T., and Lipka V. Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6 (2005) 335-345
3. Thordal-Christensen H. Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6 (2003) 351-357
4. Van Loon L.C., Rep M., and Pieterse C.M.J. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44 (2006) 135-162
5. Bent A.F., and Mackey D. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45 (2007) 399-436
6. Mysore K.S., and Ryu C- M. Nonhost resistance: how much do we know?. Trends Plant Sci 9 (2004) 97-104
7. Felix G., Duran J.D., Volko S., and Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18 (1999) 265-276
8. Kunze G., Zipfel C., Robatzek S., Niehaus K., Boller T., and Felix G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16 (2004) 3496-3507
9. Jurgen E. Oligoglucoside elicitor-mediated activation of plant defense. Bioessays 20 (1998) 569-576
10. Shibuya N., and Minami E. Oligosaccharide signalling for defence responses in plant. Physol Mol Plant Pathol 59 (2001) 223-233
11. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43 (2005) 205-227
12. Thomma B.P.H.J., Eggermont K., Penninckx I.A.M.A., Mauch-Mani B., Vogelsang R., Cammue B.P.A., et al. 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 (1998) 15107-15111
13. Ton J., Van Pelt J.A., Van Loon L.C., and Pieterse C.M.J. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol Plant Microbe Interact 15 (2002) 27-34
14. Cao H., Bowling S.A., Gordon A.S., and Dong X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6 (1994) 1583-1592
15. Delaney T.P., Friedrich L., and Ryals J.A. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92 (1995) 6602-6606
16. Friedrich L., Lawton K., Ruess W., Masner P., Specker N., Rella M.G., et al. A benzothiadiazole derivative induces systemic aquired resistance in tobacco. Plant J 10 (1996) 61-70
17. Cohen Y., Gisi U., and Niderman T. Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester. Phytopathology 83 (1993) 1054-1062
18. Thomma B.P.H.J., Eggermont K., Broekaert W.F., and Cammue B.P.A. Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol Biochem 38 (2000) 421-427
19. Thomma B.P.H.J., Tierens K.F.M., Penninckx I.A.M.A., Mauch-Mani B., Broekaert W.F., and Cammue B.P.A. Different micro-organisms differentially induce Arabidopsis disease response pathways. Plant Physiol Biochem 39 (2001) 673-680
20. Brading P.A., Hammond-Kosack K.E., Parr A., and Jones J.D.G. Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum. Plant J 23 (2000) 305-318
21. Dewdney J., Reuber T.L., Wildermuth M.C., Devoto A., Cui J., Stutius L.M., et al. Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J 24 (2000) 205-218
22. Mellersh D.G., and Heath M.C. An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. Mol Plant Microbe Interact 16 (2003) 398-404
23. Zimmerli L., Stein M., Lipla V., Schulze-Lefert P., and Somerville S. Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J 40 (2004) 633-646
24. Lightner J., Pearce G., Ryan C.A., and Browse J. Isolation of signaling mutants of tomato (Lycopersicon esculentum). Mol Gen Genet 241 (1993) 595-601
25. Howe G.A., Lightner J., Browse J., and Ryan C.A. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8 (1996) 2067-2077
26. Thaler J., Owen B., and Higgins V.J. The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135 (2004) 530-538
27. Feys B.J.F., Benedetti C.E., Penfold C.N., and Turner J.G. 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 (1994) 751-759
28. Nishimura S., and Kohmoto K. Host-specific toxins and chemical structures from Alternaria species. Annu Rev Phytopathol 21 (1983) 87-116
29. Otani H., Kohmoto K., Kodama M., and Nishimura S. Role of host-specific toxins in the pathogenesis of Alternaria alternata. In: Patil S.S., Ouchi S., Mills D., and Vance C. (Eds). Molecular strategies of pathogens and host plants (1991), Springer-Verlag, New York 139-149
30. Kohmoto K., and Otani H. Host-recognition by toxigenic plant pathogens. Experientia 47 (1991) 755-764
31. Otani H., Kohmoto K., and Kodama M. Alternaria toxins and their effects on host plants. Can J Bot 73 (1995) S453-S458
32. Friesen T.L., Faris J.D., Solomon P.S., and Oliver R.P. Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10 (2008) 1421-1428
33. Gilchrist D.G., and Grogan R.G. Production and nature of a host-specific toxin from Alternaria alternata f. sp. lycopersici. Phytopathology 66 (1976) 165-171
34. Yamagishi D., Akamatsu H., Otani H., and Kodama M. Pathological evaluation of host-specific AAL-toxins and fumonisin mycotoxins produced by Alternaria and Fusarium species. J Gen Plant Pathol 72 (2006) 323-327
35. Akamatsu H., Itoh Y., Kodama M., Otani H., and Kohmoto K. AAL-toxin-deficient mutants of Alternaria alternata tomato pathotype by restriction enzyme-mediated integration. Phytopathology 87 (1997) 967-972
36. Bottini A.T., Bowen J.R., and Gilchrist D.G. Phytotoxins. II. Characterization of a phytotoxic fraction from Alternaria alternata f. sp. lycopersici. Tetrahedron Lett 22 (1981) 2723-2726
37. Bottini A.T., and Gilchrist D.G. Phytotoxins. I. A 1-aminodimethylheptadecapentol from Alternaria alternata f. sp. lycopersici. Tetrahedron Lett 22 (1981) 2719-2722
38. Gilchrist D.G., Wang H., and Bostock R.M. Sphingosine-related mycotoxins in plant and animal disease. Can J Bot 73 (1995) S459-S467
39. Wang H., Jones C., Ciacci-Zanella J., Holt T., Gilchrist D.G., and Dickman M.B. Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc Natl Acad Sci USA 93 (1996) 3461-3465
40. Spassieva S.D., Markham J.E., and Hille J. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J 32 (2002) 561-572
41. Brandwagt B.F., Mesbah L.A., Takken F.L.W., Laurent P.L., Kneppers T.J.A., Hille J., et al. 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 (2000) 4961-4966
42. Gomi K., Itoh N., Yamamoto H., and Akimitsu K. Characterization and functional analysisof class I and II acidic chitinase cDNA from rough lemon. J Gen Plant Pathol 68 (2002) 191-199
43. Gomi K., Yamamoto H., and Akimitsu K. Characterization of a lipoxygenase gene in roughlemon induced by Alternaria alternata. J Gen Plant Pathol 68 (2002) 21-30
44. Gotoh Y., Nalumpang S., Isshiki A., Utsumi T., Gomi K., Yamamoto H., et al. A cDNA encoding polygalacturonase-inhibiting protein induced in citrus leaves by polygaracturonase of Alternaria citri. J Gen Plant Pathol 68 (2002) 57-61
45. Johnson R.D., Johnson L., Itoh Y., Kodama M., Otani H., and Kohmoto K. 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 (2000) 742-753
46. Blazquez C.H. Target spot. In: Jones J.B., Jones J.P., Stall R.E., and Zitter T.A. (Eds). Compendium of tomato diseases (1991), APS Press, St. Paul, Minnesota 23
47. Wei C.T. Notes on Corynespora. Mycol Papers 34 (1950) 1-10
48. Takahashi H., Shimizu A., Arie T., Rosmalawati S., Fukushima S., Kikuchi M., et al. Catalog of Micro-Tom tomato responses to common fungal, bacterial, and viral pathogens. J Gen Plant Pathol 71 (2005) 8-22
49. Akamatsu H, Otani H, Kodama M. 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, California; 2003. p. 121.
50. Enyedi A.J., Yalpani N., Silverman P., and Raskin I. Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci USA 89 (1992) 2480-2484
51. Audenaert K., De Meyer G.B., and Hofte M.M. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128 (2002) 491-501
52. Diaz J., Ten Have A., and Van Kan J.A.L. The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol 129 (2002) 1341-1351
53. Wasternack C. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress responses, growth and development. Ann Bot 100 (2007) 681-697
54. Lamb C.J., Lawton M.A., Dron M., and Dixon R.A. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56 (1989) 215-224
55. Kobayashi I., and Hakuno H. Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta 217 (2003) 340-345
56. McCurdy D.W., Kovar D.R., and Staiger C.J. Actin and actin-binding proteins in higher plants. Protoplasma 215 (2001) 89-104
57. Schutz I., Gus-Mayer S., and Schmelzer E. Profilin and Rop GTPases are localized at infection sites of plant cells. Protoplasma 227 (2006) 229-235
58. Shen G., Adam Z., and Zhang H. The E3 ligase AtCHIP ubiquitylates FtsH1, a component of the chloroplast FtsH protease, and affects protein degradation in chloroplasts. Plant J 52 (2007) 309-321
59. Innes R. New effects of type III effectors. Mol Microbiol 50 (2003) 363-365
60. Kim C.Y., Koo Y.D., Jin J.B., Moon B.C., Kang C.H., Kim S.T., et al. Rice C2-domain proteins are induced and translocated to the plasma membrane in response to a fungal elicitor. Biochemistry 42 (2003) 11625-11633
61. Sandrock R.W., and VanEtten H.D. Fungal sensitivity to and enzymatic degradation of the phytoanticipin a-tomatine. Phytopathology 88 (1998) 137-143
62. Oh S.-K., Lee S., Chung E., Park J.M., Yu S.H., Ryu C.-M., et al. Insight into Types I and II nonhost resistance using expression patterns of defense-related genes in tobacco. Planta 223 1 (2006) 101-107
63. Kodama M., Wada H., Otani H., Kohmoto K., and Kimura Y. 3,5-DI-O-caffeoylquinic acid, an infection-inhibiting factor from Pyrus pyrifolia induced by infection with Alternaria alternata. Phytochemistry 47 (1998) 371-373
64. Van Loon L.C., Geraats B.P.J., and Linthorst H.J.M. Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11 (2006) 184-191
65. Moore T., Martineau B., Bostock R.M., Lincoln J.E., and Gilchrist D.G. Molecular and genetic characterization of ethylene involvement in mycotoxin-induced plant cell death. Physiol Mol Plant Pathol 54 (1999) 73-85
66. Moussatos V.V., Yang S.F., Ward B., and Gilchrist D.G. AAL-toxin induced physiological changes in Lycopersicon esculentum Mill:role for ethylene and pyrimidine intermediates in necrosis. Physiol Mol Plant Pathol 44 (1994) 455-468
67. Zipfel C., Robatzek S., Navarro L., Oakeley E.J., Jones J.D.G., Felix G., et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428 (2004) 764-767
68. Thuerig B., Felix G., Binder A., Boller T., and Tamm L. An extract of Penicillium chrysogenum elicits early defense-related responses and induces resistance in Arabidopsis thaliana independently of known signalling pathways. Physiol Mol Plant Pathol 67 (2006) 180-193
69. Spoel S.H., Johnson J.S., and Dong X. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104 (2007) 18842-18847
70. Gomez-Gomez L., Felix G., and Boller T. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18 (1999) 277-284