Expression of the 12-oxophytodienoic acid 10,11-reductase gene in the compatible interaction between pea and fungal pathogen

Plant and Cell Physiology

Volumn 43, Issue 10, 2002, Pages 1210-1220

  Ishiga, Yasuhiro ^a   Funato, Akiko ^a   Tachiki, Tomoyuki ^a   Toyoda, Kazuhiro ^a   Shiraishi, Tomonori ^a   Yamada, Tetsuji ^a   Ichinose, Yuki ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Jasmonic acid; Oxophytodienoic acid reductase; Suppressor

Indexed keywords

ARABIDOPSIS THALIANA; ASCOCHYTA; DIDYMELLA PINODES; EMBRYOPHYTA; FUNGI; MYCOSPHAERELLA; MYCOSPHAERELLA PINODES; PISUM SATIVUM;

EID: 0036809969     PISSN: 00320781     EISSN: None     Source Type: Journal    
DOI: 10.1093/pcp/pcf144     Document Type: Article

References (59)

1. Andi, S., Taguchi, F., Toyoda, K., Shiraishi, T. and Ichinose, Y. (2001) Effect of methyl jasmonate on harpin-induced hypersensitive cell death, generation of hydrogen peroxide and expression of PAL mRNA in tobacco suspension cultured by-2 cells. Plant Cell Physiol. 42: 446-449.
2. Andresen, I., Becker, W., Schlueter, K., Burges, J., Parthier, B. and Apel, K. (1992) The identification of leaf thionin as one of the main jasmonate-induced proteins of barley (Hordeum vulgare). Plant Mol. Biol. 19: 193-204.
3. Basse, C.W., Bock, K. and Boller, T. (1992) Elicitors and suppressors of the defense response in tomato cells. Purification and characterization of glycopeptide elicitors and glycan suppressors generated by enzymatic cleavage of yeast invertase. J. Biol. Chem. 267: 10258-10265.
4. Biesgen, C. and Weiler, E.W. (1999) Structure and regulation of OPR1 and OPR2, two closely related genes encoding 12-oxophytodienoic acid-10,11-reductases from Arabidopsis thaliana. Planta 208: 155-165.
5. Budde, I.P. and Ullrich, M.S. (2000) Interactions of Pseudomonas syringae pv. glycinea with host and non-host plants in relation to temperature and phytotoxin synthesis. Mol. Plant-Microbe Interact. 113: 951-961.
6. Chomczynski, P. (1992) One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal. Biochem. 201: 134-139.
7. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
8. Cohen, Y., Gisi, U. and 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: 1054-1062.
9. Costa, C.L., Arruda, P. and Benedetti, C.E. (2000) An Arabidopsis gene induced by wounding functionally homologous to flavoprotein oxidoreductases. Plant Mol. Biol. 44: 61-71.
10. Creelman, R.A. and Mullet, J.E. (1995) Jasmonic acid distribution and action in plants: Regulation during development and response to biotic and abiotic stress. Proc. Natl. Acad. Sci. USA 92: 4114-4119.
11. Creelman, R.A. and Mullet, J.E. (1997) Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 355-381.
12. Doares, S.T., Narvaez-Vasquez, J., Conconi, A. and Ryan, C.A. (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108: 1741-1746.
13. Doke, N. (1975) Prevention of the hypersensitive reaction of potato cells to infection with an incompatible race of Phytophthora infestans by constituents of the zoospores. Physiol. Plant Pathol. 7: 1-7.
14. Doke, N. (1983) Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity. Physiol. Plant Pathol. 23: 359-367.
15. Doke, N., Garas, N.A. and Kuc, J. (1979) Partial characterization and aspects of the mode of action of a hypersensitivity-inhibiting factor (HIF) isolated from Phytophthora infestans. Physiol. Plant Pathol. 15: 127-140.
16. Felton, G.W., Korth, K.L., Bi, J.L., Wesley, S.V., Huhman, D.V., Mathews, M.C., Murphy, J.B., Lamb, C. and Dixon, R.A. (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr. Biol. 9: 317-320.
17. Feys, B.J.F., Benedetti, C.E., Penfold, C.N. and Turner, J.G. (1994) Arabidopsis mutant selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751-759.
18. Gundlach, H., Müller, M.J., Kutchan, T.M. and Zenk, M.H. (1992) Jasmonic acid is a signal tranducer in elicitor-induced plant cell cultures. Proc. Natl. Acad. Sci. USA 89: 2389-2393.
19. Gupta, V., Willits, M.G. and Glazebrook, J. (2000) Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: Evidence for inhibition of jasmonic acid signaling by SA. Mol. Plant-Microbe. Interact. 13: 503-511.
20. Ichinose, Y., Hisayasu, Y., Sanematsu, S., Ishiga, Y., Seki, H., Toyoda, K., Shiraishi, T. and Yamada, T. (2001) Molecular cloning and functional analysis of cDNA E86 encoding homologous protein to hypersensitivity related hsr203J. Plant Sci. 160: 997-1006.
21. Ichinose, Y., Tiemann, K., Schwenger-Erger, C., Toyoda, K., Hein, F., Hanselle, T., Cornels, H. and Barz, W. (2000) Genes expressed in Ascochyta rabiei-inoculated chickpea plants and elicited cell cultures as detected by differential cDNA-hybridization. Z. Naturforsch. [C] 55: 44-54.
22. Iuchi, S., Yamaguchi-Shinozaki, K., Urao, T., Terao, T. and Shinozaki, K. (1996) Novel drought-inducible genes in the highly drought-tolerant cowpea: Cloning of cDNAs and analysis of the expression of the corresponding genes. Plant Cell Physiol. 37: 1073-1082.
23. Kato, H., Wada, M., Muraya, K., Malik, K., Shiraishi, T., Ichinose, Y. and Yamada, T. (1995) Characterization of nuclear factors for elicitor-mediated activation of the promoter of the pea phenylalanine ammonia-lyase gene I. Plant Physiol. 108: 129-139.
24. Kawamata, S., Yamada, T., Tanaka, Y., Sriprasertsak, P., Kato, H., Ichinose, Y., Kato, H., Shiraishi, T. and Oku, H. (1992) Molecular cloning of phenylalanine ammonia-lyase cDNA from Pisum sativum. Plant Mol. Biol. 20: 167-170.
25. Kessmann, H. and Barz, W. (1986) Elicitation and suppression of phytoalexin and isoflavone accumulation in cotyledons of Cicer arietinum L. as caused by wounding and by polymeric components from fungus Ascochyta rabiei. J. Phytopathol. 117: 321-335.
26. Kiba, A., Miyake, C., Toyoda, K., Ichinose, Y., Yamada, T. and Shiraishi, T. (1997) Superoxide generation in extracts from isolated plant cell walls is regulated by fungal signal molecules. Phytopathology 87: 846-852.
27. Kiba, A., Toyoda, K., Ichinose, Y., Yamada, T. and Shiraishi, T. (1996) Species-specific suppression of superoxide-anion generation of surfaces of pea leaves by the suppressor from Mycosphaerella pinodes. Ann. Phytopathol. Soc. Jpn. 62: 508-512.
28. Koda, Y., Takahashi, K., Kikuta, Y., Greulich, F., Toshima, H. and Ichihara, A. (1996) Similarities of the biological activities of coronatine and coronafacic acid to those of jasmonic acid. Phytochemistry 41: 93-96.
29. Lamb, C.J., Lawton, M.A., Dron, M. and Dixon, R.A. (1989) Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56: 215-224.
30. Matsubara, M. and Kuroda, H. (1987) The structure and physiological activity of a glycoprotein secreted from conidia of Mycosphaerella pinodes. II. Chem. Pharm. Bull. 35: 249-255.
31. McConn, M., Creelman, R.A., Bell, E., Mullet, J.E. and Browse, J. (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 94: 5473-5477.
32. McDowell, J.M. and Dangl, J.L. (2000) Signal transduction in the plant immune response. Trends Biochem. Sci. 25: 79-82.
33. Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N. and Ohashi, Y. (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39: 500-507.
34. Peña-Cortés, H., Albrecht, T., Prat, S., Water, E.W. and Willmitzer, L. (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191: 123-128.
35. Penninckx, I.A., Eggermont, K., Terras, F.R., Thomma, B.P., De Samblanx, G.W., Buchala, A., Metraux, J.P., Manners, J.M. and Broekaert, W.F. (1996) Pathogen-induced systemic activation of plant defense gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8: 2309-2323.
36. Rao, M.V., Lee, H.-I., Creelman, R.A., Mullet, J.E. and Davis, K.R. (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12: 1633-1648.
37. Reinbothe, S., Reinbothe, C., Lehmann, J., Becker, W., Apel, K. and Parthier, B. (1994) JIP60, a methyl jasmonate-induced ribosome-inactivating protein involved in plant stress reactions. Proc. Natl. Acad. Sci. USA 91: 7012-7016.
38. Rohde, B.H., Schmid, R. and Ullrich, M.S. (1999) Thermoregulated expression and characterization of an NAD(P)H-dependent 2-cyclohexen-1-one reductase in the plant pathogenic bacterium Pseudomonas syringae pv. glycinea. J. Bacteriol. 181: 814-822.
39. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning, a Laboratory Manual, 2nd Edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
40. Sano, H., Seo, S., Koizumi, N., Niki, T., Iwamura, H. and Ohashi, Y. (1996) Regulation by cytokinins of endogenous levels of jasmonic and salicylic acids in mechanically wounded tobacco plants. Plant Cell Physiol. 37: 762-769.
41. Sasaki, Y., Asamizu, E., Shibata, D., Nakamura, Y., Kaneko, T., Awai, K., Amagai, M., Kuwata, C., Tsugane, T., Masuda, T., Shimada, H., Takamiya, K., Ohta, H. and Tabata, S. (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: Self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res. 8: 153-161.
42. Schaller, F. (2001) Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. J. Exp. Bot. 52: 11-23.
43. Schaller, F., Biesgen, C., Mussig, C., Altmann, T. and Weiler, E.W. (2000) 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210: 979-984.
44. Schaller, F. and Weiler, W. (1997a) Molecular cloning and characterization of 12-oxophytodienoate reductase, an enzyme of the octadecanoid signaling pathway from Arabidopsis thaliana. J. Biol. Chem. 272: 28066-28072.
45. Schaller, F. and Weiler, W. (1997b) Enzymes of octadecanoid biosynthesis in plants: 12-Oxo-phytodienoate 10, 11-reductase. Eur. J. Biochem. 245: 294-299.
46. Shiraishi, T., Oku, H., Yamashita, M. and Ouchi, S. (1978) Elicitor and suppressor of pisatin induction in spore germination fluid of pea pathogen, Mycosphaerella pinodes. Ann. Phytopathol. Soc. Jpn. 44: 659-665.
47. Shiraishi, T., Saitoh, K., Kim, H.M., Kato, T., Tahara, M., Oku, H., Yamada, T. and Ichinose, Y. (1992) Two suppressors, Supprescins A and B, secreted by a pea pathogen, Mycosphaerella pinodes. Plant Cell Physiol. 33: 663-667.
48. Shiraishi, T., Yamada, T., Ichinose, Y., Kiba, A., Toyoda, K., Kato, T., Murakami, Y. and Seki, H. (1999) Suppressor as a factor determining plant-pathogen specificity. In Plant-Microbe Interactions, Vol. 4. Edited by Stacey, G. and Keen, N.T pp. 121-161. APS Press, St. Paul, MN.
49. Shiraishi, T., Yamada, T., Saitoh, K., Kato, T., Toyoda, K., Yoshioka, H., Kim, H.-M., Ichinose, Y., Tahara, M. and Oku, H. (1994) Suppressors: Determinants of specificity produced by plant pathogens. Plant Cell Physiol. 35: 1107-1119.
50. Stintzi, A. and Browse, J. (2000) The Arabidopsis male-sterile mutant, OPR3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc. Natl. Acad. Sci. USA 97: 10625-10630.
51. Stintzi, A., Weber, H., Reymond, P., Browse, J. and Farmer, E.E. (2001) Plant defense in the absence of jasmonic acid: The role of cyclopentenones. Proc. Natl. Acad Sci. USA 98: 12317-12319.
52. Storti, E., Pelucchini, D., Tegri, S. and Scala, A. (1988) A potential defense mechanism tomato against the late blight disease is suppressed by germinating sporangia-derived substances from Phvtophthora infestans. J. Phytopathol. 121: 275-282.
53. Straßner, J., Fürholz, A., Macheroux, P., Amrhein, N. and Schaller, A. (1999) A homolog of old yellow enzyme in tomato. Spectral properties and substrate specificity of the recombinant protein. J. Biol. Chem. 274: 35067-35073.
54. Toyoda, K, Shiraishi, T., Yamada, T., Ichinose, Y. and Oku, H. (1993) Rapid changes in polyphosphoinositide metabolism in pea in response to fungal signals. Plant Cell Physiol. 34: 729-735.
55. Vick, B.A. and Zimmerman, D.C. (1986) Characterization of 12-oxo-phytodienoic acid reductase in corn. Plant Physiol. 80: 202-205.
56. Vijayan, P., Shockey, J., Levesque, C.A., Cook, R.J. and Beowse, J. (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 7209-7214.
57. Weiler, E.W., Kutchan, T.M., Gorba, T., Brodschelm, W., Nieesel, U. and Bublitz, F. (1994) The Pseudomonas phytotoxin coronatine mimics octadecanoid signalling molecules of higher plants. FEBS Lett. 345: 9-13.
58. Yamada, T., Hashimoto, H., Shiraishi, T. and Oku, H. (1989) Suppression of pisatin, phenylalanine ammonia-lyase mRNA, and chalcone synthase mRNA by a putative pathogenicity factor from the fungus Mycosphaerella pinodes. Mol. Plant-Microbe Interact. 2: 256-261.
59. Yoshioka, H., Shiraishi, T., Kawamata, S., Nasu, K., Yamada, T., Ichinose, Y. and Oku, H. (1992) Orthovanadate suppresses an accumulation of phenylalanine ammonia-lyase mRNAs and chalcone synthase mRNA in pea epicotyls that is induced by an elicitor from Mycosphaerella pinodes. Plant Cell Physiol. 32: 201-204.