Skip to main content
SpringerLink
Log in

Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush)

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

An expression profile of genes induced by non-pathogenic Alternaria alternata on rough lemon leaves was obtained by sequencing 500 subtractive PCR clones generated from mRNA of leaves inoculated with the fungus after subtraction with that of non-inoculated leaves. About 6% of the cDNA sequences had homology to known putative defense-related genes including epoxide hydrolase. A full-length cDNA (951 bp) from rough lemon that encoded epoxy hydrolase was isolated by random amplification of cDNA ends (RACEs), based on sequence information from subtractive PCR, and designated as RlemEH. The product of this gene expressed with an in vitro translation system with Escherichia coli also had activity of a soluble type of epoxide hydrolase. The transcript of rough lemon RlemEH was not detected in flowers, fruits, stems or leaves, but was induced after inoculation of leaves with conidia of Alternaria alternata, wounding, or treatment with C6 volatiles, including trans-2-hexenol and cis-3-hexenol, and methyl jasmonate. The response of the epoxide hydrolase gene correlated well with the activation of defense mechanisms induced in plant-fungus interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akimitsu, K., Kohmoto, K., Otani, H. and Nishimura, S. 1989. Host-specific effect of toxin from the rough lemon pathotype of Alternaria alternata on mitochondria. Plant Physiol. 89: 925–931.

    Google Scholar 

  • Arahira, M., Nong, V.H., Udaka, K. and Fukazawa, C. 2000. Purification, molecular cloning and ethylene-inducible expression of a soluble-type epoxide hydrolase from soybean (Glycine max [L.] Merr.). Eur. J. Biochem. 267: 2649–2657.

    Google Scholar 

  • Arand, M., Wagner, H. and Oesch, F. 1996. Asp333, Asp495, and His523 form the catalytic triad of rat soluble epoxide hydrolase. J. Biol. Chem. 271: 4223–4229.

    Google Scholar 

  • Baker, E.A., Procopiou, J. and Hunt, G.M. 1975. The cuticles of Citrus species. Composition of leaf and fruit waxes. J. Sci. Food Agric. 26: 1093–1101.

    Google Scholar 

  • Baker, B., Zambryski, P., Staskawicz, B. and Dinesh-Kumar, S.P. 1997. Signaling in plant-microbe interactions. Science 276: 726–733.

    Google Scholar 

  • Bate, N.J. and Rothstein, S.J. 1998. C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J. 16: 561–569.

    Google Scholar 

  • Bate, N.J., Sivasankar, S., Moxon, C., Riley, J.M.C., Thompson, J.E. and Rothstein, S.J. 1998. Molecular characterization of an Arabidopsis thaliana gene encoding hydroperoxide lyase, a cytochrome P-450 that is wound inducible. Plant Physiol. 117: 1393–1400.

    Google Scholar 

  • Blee, E. and Schuber, F. 1992a. Occurrence of fatty acid epoxide hydrolases in soybean (Glycine max). Biochem. J. 282: 711–714.

    Google Scholar 

  • Blee, E. and Schuber, F. 1992b. Regio-and enantioselectivity of soybean fatty acid epoxide hydrolase. J. Biol. Chem. 267: 11881–11887.

    Google Scholar 

  • Blee, E. and Schuber, F. 1993. Biosynthesis of cutin monomers: involvement of lipoxygenase/peroxygenase pathway. Plant J. 4: 113–123.

    Google Scholar 

  • Blee, E. and Schuber, F. 1995. Stereocontrolled hydrolysis of the linolenic acid monoepoxide regioisomers catalyzed by soybean epoxide hydrolase. Eur. J. Biochem. 230: 229–234.

    Google Scholar 

  • Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.

    Google Scholar 

  • Croft, K.P.C., Juttner, F. and Slusarenko, A.J. 1993. Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv. phaseolicola. Plant Physiol. 101: 13–24.

    Google Scholar 

  • Croteau, R. and Kolattukudy, P.E. 1975a. Biosynthesis of hydroxyfatty acids polymers. Enzymatic epoxidation of 18-hydroxyoleic acid to 18-hydroxy-cis-9,10-epoxystearic acid by a particulate preparation from spinach (Spinacia oleracea). Arch. Biochem. Biophys. 170: 61–72.

    Google Scholar 

  • Croteau, R. and Kolattukudy, P.E. 1975b. Biosynthesis of hydroxyfatty acids polymers. Enzymatic epoxidation of 18-hydroxyoleic acid to 18-hydroxy-cis-9,10-epoxystearic acid by a particulate preparation from apple (Malus pumila). Arch. Biochem. Biophys. 170: 73–81.

    Google Scholar 

  • Diatchenko, L., Lau, Y.F., Campbell, A.P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E.D. and Siebert, P.D. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA 93: 6025–6030.

    Google Scholar 

  • Dong, X. 1998. SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1: 316–323.

    Google Scholar 

  • Espelie, K.E., Davis, R.W. and Kolattukudy, P.E. 1980. Composition, ultrastructure and function of the cutin-and suberincontaining layers in the leaf, fruit peel, juice-sac and inner seed coat of grapefruit (Citrus paradisi Macfed.). Planta 149: 498–511.

    Google Scholar 

  • Gomi, K., Itoh, N., Yamamoto, H. and Akimitsu, K. 2002a. Characterization and functional analysis of class I and II acidic chitinase cDNA from rough lemon. J. Gen. Plant Path. 68: 191–199.

    Google Scholar 

  • Gomi, K., Yamamoto, H. and Akimitsu, K. 2002b. Characterization of lipoxygenase gene in rough lemon induced by Alternaria alternata. J. Gen. Plant Path. 68: 21–30.

    Google Scholar 

  • Gomi, K., Yamasaki, Y., Yamamoto, H. and Akimitsu, K. 2003. Characterization of citrus hydroperoxide lyase gene and effect of C6-volatiles on expression of oxylipin-metabolizing enzyme genes. J. Plant Physiol. 160: 1219–1231.

    Google Scholar 

  • Guo, A., Durner, J. and Klessig, D.F. 1998. Characterization of a tobacco epoxide hydrolase gene induced during the resistance response to TMV. Plant J. 15: 647–656.

    Google Scholar 

  • Hamberg, M. and Fahlstadius, P. 1992. On the specificity of a fatty acid epoxygenase in broad bean (Vicia faba L.). Plant Physiol. 99: 987–995.

    Google Scholar 

  • Hamilton-Kemp, T.R., McCracken, C.T. Jr., Loughrin, J.H., Andersen, R.A. and Hildebrand, D.F. 1992. Effects of some natural volatile compounds on the pathogenic fungi Alternaria alternate and Botrytis cinerea. J. Chem. Ecol. 18: 1083–1091.

    Google Scholar 

  • Hasegawa, L.S. and Hammock, B.D. 1982. Spectrophotometric assay for mammalian cytosolic epoxide hydrolase using trans stilbene oxide as the substrate. Biochem. Pharmacol. 31: 1979–1984.

    Google Scholar 

  • Hatanaka, A., Kajiwara, T. and Sekiya, J. 1987. Biosynthetic pathway for C6-aldehydes formation from linolenic acid in green leaves. Chem. Phys. Lipids 44: 341–361.

    Google Scholar 

  • Kato, T., Yamaguchi, Y., Uehara, T., Yokoyama, T., Namai, T. and Yamanaka, S. 1983. Defense mechanism of the rice plant against rice blast disease. Naturwissenschaften 70: 200–201.

    Google Scholar 

  • Kato, T., Yamaguchi, Y., Abe, N., Uehara, T., Namai, T., Kodama, M. and Shiobara, Y. 1985. Structure and synthesis of unsaturated trihydroxy C18 fatty acids in rice plants suffering from rice blast disease. Tetrahedron Lett. 26: 2357–2360.

    Google Scholar 

  • Kiyosue, T., Beetham, J.K., Pinot, F., Hammock, B.D., Yamaguchi-Shinozaki, K. and Shinozaki, K. 1994. Characterization of an Arabidopsis cDNA for a soluble epoxide hydrolase gene that is inducible by auxin and water stress. Plant J. 6: 259–269.

    Google Scholar 

  • Kohmoto, K., Akimitsu, K. and Otani, H. 1991. Correlation of resistance and susceptibility of citrus to Alternaria alternata with sensitivity to host-specific toxins. Phytopathology 81: 719–722.

    Google Scholar 

  • Kohmoto, K., Itoh, Y., Shimomura, N., Kondoh, Y., Otani, H., Kodama, M., Nishimura, S. and Nakatsuka, S. 1993. Isolation and biological activities of two host-specific toxins from the tangerine pathotype of Alternaria alternata. Phytopathology 83: 495–502.

    Google Scholar 

  • Kolattukudy, P.E. 1980. Biopolyester membranes of plants: cutin and suberin. Science 208: 990–1000.

    Google Scholar 

  • Kolattukudy, P.E. 1985. Enzymatic penetration of the plant cuticle by fungal pathogens. Annu. Rev. Phytopath. 23: 223–250.

    Google Scholar 

  • Liang, P. and Pardee, A.B. 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257: 967–971.

    Google Scholar 

  • Lisitsyn, N. and Wigler, M. 1993. Cloning the differences between two complex genomes. Science 259: 946–951.

    Google Scholar 

  • Masui, H., Kondo, T. and Kojima, M. 1989. An antifungal compound 9,12,13-trihydroxy-(E)-10-octadecenoic acid from Colocasia antiquorum inoculated with Ceratocystis fimbriata. Phytochemistry 28: 2613–2615.

    Google Scholar 

  • Masunaka, A., Tanaka, A., Tsuge, T., Peever, T.L., Timmer, L.W., Yamamoto, M., Yamamoto, H. and Akimitsu, K. 2000. Distribution and Characterization of AKT homologs in the tangerine pathotype of Alternaria alternata. Phytopathology 90: 762–768.

    Google Scholar 

  • Ohta, H., Shida, K., Peng, Y.-L., Furusawa, I., Shishiyama, J., Aibara, S. and Morita, Y. 1990. The occurrence of lipid hydroxyperoxide-decomposing activities in rice and the relationship of such activities to the formation of antifungal substances. Plant Cell Physiol. 31: 1117–1122.

    Google Scholar 

  • Pinot, F., Grant, D.F., Beetham, J.K., Parker, A.G., Borhan, B., Landt, S., Jones, A.D. and Hammock, B.D. 1995. Molecular and biochemical evidence for the involvement of the Asp333-His523 pair in catalytic mechanism of soluble epoxide hydrolase. J. Biol. Chem. 270: 7968–7974.

    Google Scholar 

  • Proudfoot, N.J. and Brownlee, G.G. 1976. 3′ Non-coding region sequences in eukaryotic messenger RNA. Nature 263: 211–214.

    Google Scholar 

  • Rink, R., Fennema, M., Smids, M., Dehmel, U. and Janssen, D.B. 1997. Primary structure and catalytic mechanism of the epoxide hydrolase from Agrobacterium radiobacter AD1. J. Biol. Chem. 272: 14650–14657.

    Google Scholar 

  • Sanger, F., Nicklen, S. and Coulson, A.R. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.

    Google Scholar 

  • Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. and Manners, J.M. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97: 11655–11660.

    Google Scholar 

  • Schweizer, P., Jeanguenat, A., Whitagre, D., Metraux, J.-P. and Mosinger, E. 1996. Induction of resistance in barley against Erysiphe graminis f. sp. hordei by free cutin monomers. Physiol. Mol. Plant Path. 49: 103–120.

    Google Scholar 

  • Stapleton, A., Beetham, J.K., Pinot, F., Garbarino, J.E., Rockhold, D.R., Friedman, M., Hammock, B.D. and Belknap, W.R. 1994. Cloning and expression of soluble epoxide hydrolase from potato. Plant J. 6: 251–258.

    Google Scholar 

  • Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.

    Google Scholar 

  • Velculescu, V.E., Zhang, L., Vogelstein, B. and Kinzler, K.W. 1995. Serial analysis of gene expression. Science 270: 484–487.

    Google Scholar 

  • Watson, J.B. and Margulies, J.E. 1993. Differential cDNA screening strategies to identify novel stage-specific proteins in the developing mammalian brain. Dev. Neurosci. 15: 77–86.

    Google Scholar 

  • White, O. and Kerlavage, A.R. 1996. TDB: New databases for biological discovery. Meth. Enzymol. 266: 27–40.

    Google Scholar 

  • Wixtrom, R.N. and Hammock, B.D. 1985. Membrane-bound and soluble-fraction epoxide hydrolases. In: D. Zakim and D.A. Vessey (Eds.) Biochemical Pharmacology and Toxicology, Volume 1, Wiley, New York, pp. 1–93.

    Google Scholar 

  • Ziegler, J., Hamberg, M., Miersch, O. and Parthier, B. 1997. Purification and characterization of allene oxide cyclase from dry corn seeds. Plant Physiol. 114: 565–573.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Plant Pathology, Faculty of Agriculture, Department of Life Sciences, Kagawa University, Miki, Kagawa, 761-0795, Japan

    Kenji Gomi, Hiroyuki Yamamato & Kazuya Akimitsu

Authors
  1. Kenji Gomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroyuki Yamamato
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuya Akimitsu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kazuya Akimitsu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gomi, K., Yamamato, H. & Akimitsu, K. Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush). Plant Mol Biol 53, 189–199 (2003). https://doi.org/10.1023/B:PLAN.0000009287.95682.24

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PLAN.0000009287.95682.24

Search

Navigation