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A peanut seed lipoxygenase responsive to Aspergillus colonization

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Abstract

Several lines of evidence have indicated that lipoxygenase enzymes (LOX) and their products, especially 9S- and 13S-hydroperoxy fatty acids, could play a role in the Aspergillus/seed interaction. Both hydroperoxides exhibit sporogenic effects on Aspergillus spp. (Calvo, A., Hinze, L., Gardner, H.W. and Keller, N.P. 1999. Appl. Environ. Microbiol. 65: 3668–3673) and differentially modulate aflatoxin pathway gene transcription (Burow, G.B., Nesbitt, T.C., Dunlap, J. and Keller, N.P. 1997. Mol. Plant-Microbe Interact. 10: 380–387). To examine the role of seed LOXs at the molecular level, a peanut (Arachis hypogaea L.) seed gene, PnLOX1, was cloned and characterized. Analysis of nucleotide sequence suggests that PnLOX1 encodes a predicted 98 kDa protein highly similar in sequence and biochemical properties to soybean LOX2. The full-length PnLOX1 cDNA was subcloned into an expression vector to determine the type(s) of hydroperoxide products the enzyme produces. Analysis of the oxidation products of PnLOX1 revealed that it produced a mixture of 30% 9S-HPODE (9S-hydroperoxy-10E, 12Z-octadecadienoic acid) and 70% 13S-HPODE (13S-hydroperoxy-9Z, 11E-octadecadienoic acid) at pH 7. PnLOX1 is an organ-specific gene which is constitutively expressed in immature cotyledons but is highly induced by methyl jasmonate, wounding and Aspergillus infections in mature cotyledons. Examination of HPODE production in infected cotyledons suggests PnLOX1 expression may lead to an increase in 9S-HPODE in the seed.

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References

  • Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.

    Google Scholar 

  • Axelrod, B., Cheesebrough, T.M. and Laakso, S. 1981. Lipoxygenase from soybeans. Meth. Enzymol. 71: 441–451.

    Google Scholar 

  • Bell, E. and Mullet, J.E. 1994. Lipoxygenase gene expression is modulated in plants by water deficit, wounding, and methyl jasmonate. Mol. Gen. Genet. 230: 456–462.

    Google Scholar 

  • Bell, E. and Mullet, J.E. 1993. Characterization of an Arabidopsis thaliana lipoxygenase responsive to methyl jasmonate and wounding. Plant Physiol. 103: 1133–1137.

    Google Scholar 

  • Burow, G.B., Nesbitt, T.C., Dunlap, J. and Keller, N.P. 1997. Seed lipoxygenase products modulate Aspergillus mycotoxin biosynthesis. Mol. Plant-Microbe Interact. 10: 380–387.

    Google Scholar 

  • Calvo, A., Hinze, L., Gardner, H.W. and Keller, N.P. 1999. Sporogenic effect of polyunsaturated fatty acids on Aspergillus spp. development. Appl. Environ. Microbiol. 65: 3668–3673.

    Google Scholar 

  • Champe, S.P. and El-Zayat, E. 1989. Isolation of a sexual sporulation hormone from Aspergillus nidulans. J. Bact. 171: 3982–3988.

    Google Scholar 

  • Doehlert, D.C., Wicklow, D.T. and Gardner, H.W. 1993. Evidence implicating the lipoxygenase pathway in providing resistance to soybean against Aspergillus flavus. Phytopathology 183: 1473–1477.

    Google Scholar 

  • Ealing, P.M. and Casey, R. 1989. The cDNA cloning of a pea (Pisum sativum) seed lipoxygenase: sequence comparisons of the two major pea lipoxygenase isoforms. Biochem. J. 264: 929-932.

  • Farmer, E.E. and Ryan, C.A. 1992. Octadecanoid precursor of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4: 129–134.

    Google Scholar 

  • Frohman, M.A. 1990. RACE: rapid amplification of cDNA ends. In: M.A. Innis, D.H. Gelfand, T.J. Sninsky and T.J. White (Eds.), PCR Protocols: A Guide to Methods and Applications, Academic Press, San Diego, CA, pp. 28–38.

    Google Scholar 

  • Gardner, H.W. 1995. Biological roles and biochemistry of the lipoxygenase pathway. Hort. Sci. 30: 197–205.

    Google Scholar 

  • Gardner, H.W. 1998. 9-Hydroxy-traumatin, a new metabolite of the lipoxygenase pathway. Lipids 33: 745–749.

    Google Scholar 

  • Gardner, H.W., Takamura, H., Hildebrand, D.F., Croft, K.P.C., Simpson, T.D. and Salch, Y.P. 1996. Oxylipin pathway in soybeans and its physiological significance. In: G. Piazza (Ed.), Lipoxygenase and Lipoxygenase Pathway Enzymes, American Oil Chemical Society Press, Champaign, IL, pp. 162–175.

    Google Scholar 

  • Gardner, H.W., Grove, M.J. and Keller, N.P. 1998. Soybean lipoxygenase is active on nonaqueous media at low moisture: a constraint to xerophilic fungi and aflatoxins? J. Am. Oil Chem. Soc. 75: 1801–1808.

    Google Scholar 

  • Geerts, A., Feltkamp, D. and Rosahl, S. 1994. Expression of lipoxygenase in wounded tubers of Solanum tuberosum L. Plant Physiol. 105: 269–277.

    Google Scholar 

  • Gilman, D.F. and Smith, O.D. 1977. Internal pericarp color as a subjective maturity index for peanut breeding. Peanut Sci 4: 67–70.

    Google Scholar 

  • Gish, W. and States, D.J. 1993. Identification of protein coding regions by database similarity search. Nature Genet. 3: 266–272.

    Google Scholar 

  • Goodrich-Tanrikulu, M., Mahoney, N. and Rodriguez, S.B. 1995. The plant growth regulator methyl jasmonate inhibits aflatoxin production by Aspergillus flavus. Microbiology 141: 2831–2837.

    Google Scholar 

  • Heitz, T., Bergey, D.R. and Ryan, C.A. 1997. A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol. 114: 1085–1093.

    Google Scholar 

  • Hildebrand, D. 1989: Lipoxygenases. Physiol. Plant. 76: 249–253.

    Google Scholar 

  • Kozak, M. 1984. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucl. Acids Res. 12: 857–872.

    Google Scholar 

  • Lee, L.S., Lillehoj, E.B. and Kwolek, W.F. 1980. Aflatoxin distribution in individual corn kernels from intact ears. Cereal Chem. 57: 340–343.

    Google Scholar 

  • Ludwig, P., Holtzhutter, H.-G., Colosimo, A., Silvestrini, M.C., Schewe, T. and Rapoport, S.M. 1987. A kinetic model for lipoxygenases based on experimental data with the lipoxygenase of reticulocytes. Eur. J. Biochem. 168: 325–337.

    Google Scholar 

  • Lutcke, H.A., Chow, K.C., Mickel, F.S., Moss, K.A., Kern, H.F. and Scheele, G.A. 1987. Selection of AUG initiation codons differ in plants and animals. EMBO J. 6: 43–48.

    Google Scholar 

  • Melan, M.A., Dong, X., Endara, M.E., Davis, K.R., Ausubel, F.M. and Peterman, T.K. 1993. An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol. 101: 441–450.

    Google Scholar 

  • Ohta, H., Shida, K., Peng, Y.-L., Furusawa, I., Shishiyama, J., Abaira, S. and Morita, Y. 1991. A lipoxygenase pathway is activated in rice after infection with the rice blast fungus Magnaporthe grisea. Plant Physiol. 97: 94–98.

    Google Scholar 

  • Pattee, H.E. and Singleton, J.A. 1977. Isolation of isomeric hydroperoxides from the peanut lipoxygenase-linoleic acid reaction. J. Am. Oil. Chem. 54: 183–185.

    Google Scholar 

  • Peng, Y.L., Shirano, Y., Ohta, H., Hibino, T., Tanaka, K. and Shibata, D. 1994. A novel lipoxygenase from rice: primary structure and specific expression upon incompatible infection with rice blast fungus. J. Biol. Chem. 269: 3755–3761.

    Google Scholar 

  • Porter, N.A. and Wujek, D.G. 1984. Autoxidation of polyunsaturated fatty acids, an expanded mechanistic study. J. Am. Chem. Soc. 106: 2626–2629.

    Google Scholar 

  • Rance, I., Fournier, J. and Esquerre-Tugaye, M.-T. 1998. The incompatible interaction between Phytophthora parasitica var. nicotinae race 0 and tobacco is suppressed in transgenic plants expressing antisense lipoxygenase sequences. Proc. Natl. Acad. Sci. USA 95: 6554–6559.

    Google Scholar 

  • Ricker, K.E. and Bostock, R.M. 1993. Eicosanoids in the Phytophthora infestans-potato interaction: lypoxygenase metabolism of arachidonic acid and biological activities of selected lipoxygenase products. Physiol. Mol. Plant. Path. 44: 65–80.

    Google Scholar 

  • Royo, J., Vancanneyt, G., Perez, A.G., Sanz, C., Stormann, K. and Sanchez-Serrano, J. 1996. Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J. Biol. Chem. 271: 21012–21019.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Sanders, T.H., Pattee, H.E. and Singleton, J.A. 1975. Lipoxygenase isozymes of peanut. Lipids 10: 681–685.

    Google Scholar 

  • Sanders, T.H., Schubert, A.M. and Pattee, H.E. 1982. Maturity methodology and postharvest physiology. In: H.E. Pattee and C.T. Young (Eds.), Peanut Science and Technology, American Peanut Research and Education Society, Texas, pp. 624–628.

    Google Scholar 

  • Shibata, D., Steczko, J., Dixon, J.E., Hermodson, M., Yazdanparast, R. and Axelrod, B. 1987. Primary structure of soybean lipoxygenase-1. J. Biol. Chem. 262: 10080–10084.

    Google Scholar 

  • Shibata, D., Steczko, J., Dixon, J.E., Andrews, P.C., Hermodson, M. and Axelrod, B. 1988. Primary structure of soybean lipoxygenase L-2. J. Biol. Chem. 263: 6816–6821.

    Google Scholar 

  • Siedow, J.N. 1998. Plant lipoxygenases: structure and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 145–188.

    Google Scholar 

  • Smart, M.G., Shotwell, O.L. and Caldwall, R.W. 1990. Pathogenesis in Aspergillus ear rot of maize: aflatoxin B1 levels in grains around wound-inoculated sites. Phytopathology 80: 1283–1286.

    Google Scholar 

  • Steczko, J., Donoho, G.P., Dixon, J.E., Sugimoto, T. and Axelrod, B. 1991. Effect of ethanol and low-temperature culture on expression of soybean lipoxygenase L-1 in Escherichia coli. Prot. Exp. Purif. 2: 221–227.

    Google Scholar 

  • Steczko, J., Donoho, G.P., Clemens, J.C., Dixon, J.E. and Axelrod, B. 1992. Conserved histidine residues in soybean lipoxygenase: functional consequences of their replacement. Biochemistry 31: 4053–4057.

    Google Scholar 

  • Veronesi, C., Rickauer, M., Fournier, J., Pouenat, M.-L. and Esquerre-Tugaye, M.-T. 1996. Lypoxygenase gene expression in the tobacco-Phytophthora parasitica nicotianae interaction. Plant Physiol. 112: 997–1004.

    Google Scholar 

  • Wu, S., Kriz, A. and Widholm, J.M. 1994. Molecular analysis of two cDNA clones encoding acidic class 1 chitinase in maize. Plant Physiol 105: 1097–1105.

    Google Scholar 

  • Zeringue, H., Brown, R., Neucere, J. and Cleveland, T. 1996. Relationship between C6-C12 alkanal and alkenal volatile contents and resistance of maize genotypes to Aspergillus flavus and aflatoxin production. J. Agric. Food Chem. 44: 403–407.

    Google Scholar 

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Burow, G.B., Gardner, H.W. & Keller, N.P. A peanut seed lipoxygenase responsive to Aspergillus colonization. Plant Mol Biol 42, 689–701 (2000). https://doi.org/10.1023/A:1006361305703

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