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1-aminocyclopropane-1-carboxylate oxidase from embryonic axes of germinating chick-pea (Cicer arietinum L.) seeds: cellular immunolocalization and alterations in its expression by indole-3-acetic acid, abscisic acid and spermine

Published online by Cambridge University Press:  22 February 2007

María Del Carmen Gómez-Jiménez ,
Enrique García-Olivares  and
Angel J. Matilla
María Del Carmen Gómez-Jiménez
Affiliation:
Departamento de Biología Vegetal, Laboratorio de Fisiología Vegetal, Facultad de Ciencias, Universidad de Granada, 18001-Granada, Spain
Enrique García-Olivares
Affiliation:
Departamento de Bioquímica y Biología Molecular, Facultad de Medicina, Universidad de Granada, 18001-Granada, Spain
Angel J. Matilla*
Affiliation:
Departmento de Fisiología Vegetal, Facultad de Farmacia, Universidad de Santiago de Compostela, 15706-Santiago de compostela, A Coruña, Spain
*
*Correspondence Fax: +34-981-593-054 Email: [email protected]
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Abstract

A recombinant protein (approximately 38 kDa by SDS/PAGE), induced by expression in Escherichia coli of a cDNA encoding a 1-aminocyclopropane-1-carboxylate oxidase (ACO) isolated from embryonic axes of Cicer arietinum, was recognized by an antibody raised against an apple ACO. A monoclonal antibody, obtained from recombinant ACO of chick-peas, was used for immunolocalization experiments in the embryonic axes of chick-pea seeds. The results indicate that most of the ACO was present in the apoplast of the cell wall. No evidence of this protein in the vacuole was detected. During germination of C. arietinum seeds, the production of ethylene was induced in the embryonic axis; its highest value was reached when radicle emergence occurred. At this moment there was an accumulation of 1-aminocyclopropane-1-carboxylate (ACC), transcription of ACO mRNA, as well as maximal ACO activity. In the post-germinative period the activity of the last step of ethylene biosynthesis decreased. This decrease was eliminated by indole-3-acetic acid (IAA), which caused significant transcription of ACO mRNA. It is suggested that gene expression of ACO may be induced by auxins and spermine (Spm) and inhibited by abscisic acid (ABA).

Keywords

abscisic acidACC oxidasechick-pea seedCicer arietinumembryonic axisethylenegerminationindole-3-acetic acidLeguminosaespermine
Type
Research Article
Information
Seed Science Research , Volume 11 , Issue 3 , September 2001 , pp. 243 - 253
Copyright
Copyright © Cambridge University Press 2001

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References

Abeles, F.B., Morgan, P.W. and Salveit, M.E. (1992) Ethylene in plant biology (2nd edition). San Diego, Academic Press.Google Scholar
Ayub, R., Guis, M., Ben Amor, M., Gillot, L., Roustan, J.P., Latché, A., Bouzayen, M. and Pech, J.C. (1996) Expression of ACC oxidase antisense gene inhibits ripening of cantaloupe melon fruits. Nature Biotechnology 14, 862–866.CrossRefGoogle ScholarPubMed
Balagué, C., Watson, C.F., Turner, A.J., Rouge, P., Picton, S., Pech, J.C. and Grierson, D. (1993) Isolation of a ripening and wound-induced cDNA from Cucumis melo L. encoding a protein with homology to the ethyleneforming enzyme. European Journal of Biochemistry 212, 27–34.CrossRefGoogle Scholar
Barry, C.S., Blume, B., Bouzayen, M., Cooper, W., Hamilton, A.J. and Grierson, D. (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant Journal 9, 525–535.Google Scholar
Beaudoin, N., Serizet, C., Gosti, F. and Giraudat, J. (2000) Interactions between abscisic acid and ethylene signaling cascades. The Plant Cell 12, 1103–1115.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Bueno, M., Garrido, D. and Matilla, A. (1993) Gene expression induced by spermine in isolated embryonic axes of chick-pea seeds. Physiologia Plantarum 87, 381–388.Google Scholar
Casey, P.J. (1995) Protein lipidation in cell signaling. Science 268, 221–225.Google Scholar
Colorado, P., Nicolás, C., Nicolás, G. and Rodríguez, D. (1995) Expression of three ABA-regulated clones and their relationship to maturation processes during the embryogenesis of chick-pea seeds. Physiologia Plantarum 94, 1–6.CrossRefGoogle Scholar
Corpas, F.J., Bunkelmann, J. and Trelease, R.N. (1994) Identification and immunochemical characterization of a family of peroxisome membrane proteins (PMPs) in oilseed glyoxysomes. European Journal of Cell Biology 65, 280–290.Google ScholarPubMed
Fluhr, R. (1998) Ethylene perception: from two-component signal transducers to gene induction. Trends in Plant Science 3, 141–146.Google Scholar
Fluhr, R. and Mattoo, A.K. (1996) Ethylene – Biosynthesis and perception. Critical Reviews in Plant Sciences 15, 479–523.Google Scholar
Gallardo, M., Delgado, M.D., Sánchez-Calle, I.M. and Matilla, A.J. (1991) Ethylene production and 1- aminocyclopropane-1-carboxylic acid conjugation in thermoinhibited Cicer arietinum L. seeds. Plant Physiology 97, 122–127.CrossRefGoogle Scholar
Gallardo, M., Matilla, A. and Sánchez-Calle, I.M. (1992) Effects of spermine, abscisic acid and temperature upon ethylene production in Cicer arietinum L. seeds. Plant Physiology and Biochemistry 30, 19–27.Google Scholar
Gallardo, M., De Rueda, P.M., Matilla, A. and Sánchez- Calle, I.M. (1994) The relationships between ethylene production and germination of Cicer arietinum seeds. Biologia Plantarum 36, 201–207.Google Scholar
Ghassemian, M., Nambara, E., Cutler, S., Kawaide, H., Kamiya, Y. and McCourt, P. (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. The Plant Cell 12, 1117–1126.Google Scholar
Gómez-Jiménez, M.C., Matilla, A.J. and Garrido, D. (1998) Isolation and characterization of a cDNA encoding an ACC oxidase from Cicer arietinum and its expression during embryogenesis and seed germination. Australian Journal of Plant Physiology 25, 765–773.Google Scholar
Guilfoyle, T.J. (1999) Auxin-regulated genes and promotors. pp. 423–460in Hooykaas, P.J.J.; Hall, M.A; Libbenga, K.R. (Eds) Biochemistry and molecular biology of plant hormones. Amsterdam, Elsevier.CrossRefGoogle Scholar
Hamilton, A.J., Bouzayen, M. and Grierson, D. (1991) Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. Proceedings of the National Academy of Sciences USA 88, 7434–7437.Google Scholar
Harlow, E. and Lane, D. (1988) Antibodies – A laboratory manual. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press.Google Scholar
Hilhorst, H.W.M. (1995) A critical update on seed dormancy I. Primary dormancy. Seed Science Research 5, 61–73.CrossRefGoogle Scholar
Huang, X.L. and Khan, A.A. (1992) Alleviation of thermoinhibition in preconditioned lettuce seeds involves ethylene, not polyamine biosynthesis. Journal of the American Society for Horticultural Science 117, 841–845.Google Scholar
Imaseki, H. (1999) Control of ethylene synthesis and metabolism. pp. 209–245in Hooykaas, P.J.J.; Hall, M.A.; Libbenga, K.R. (Eds) Biochemistry and molecular biology of plant hormones. Amsterdam, Elsevier.CrossRefGoogle Scholar
Johnson, P.R. and Ecker, J.R. (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annual Review of Genetics 32, 227–254.CrossRefGoogle ScholarPubMed
Kelly, J.L., Greenleaf, A.L. and Lehman, I.R. (1986) Isolation of the nuclear gene encoding a subunit of the yeast mitochondrial RNA polymerase. Journal of Biological Chemistry 261, 10348–10351.Google Scholar
Kende, H. (1993) Ethylene biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 44, 283–307.Google Scholar
Kepczynski, J. and Kepczynska, E. (1997) Ethylene in seed dormancy and germination. Physiologia Plantarum 101, 720–726.Google Scholar
Kim, W.T. and Yang, S.F. (1994) Structure and expression of cDNAs encoding 1-aminocyclopropane-1-carboxylate oxidase homologs isolated from excised mung bean hypocotyls. Planta 194, 223–229.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680–685.Google Scholar
Lasserre, E., Bouquin, T., Hernández, J.A., Bull, J., Pech, J.C. and Balagué, C. (1996) Structure and expression of three genes encoding ACC oxidase homologs from melon (Cucumis melo L.). Molecular and General Genetics 251, 81–90.Google Scholar
Liang, X.W., Abel, S., Keller, J., Shen, N.F. and Theologis, A. (1992) The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 89, 11046–11050.CrossRefGoogle ScholarPubMed
Malerba, M. and Bianchetti, R. (1996) A mutant of Arabidopsis thaliana with decreased activity of the plasma-membrane proton pump lacks the fusicoccindependent stimulation of ethylene synthesis. Journal of Plant Physiology 147, 614–616.CrossRefGoogle Scholar
Malerba, M., Crosti, P. and Bianchetti, R. (1995) Ferricyanide induced ethylene production is a plasma membrane proton pump dependent 1-aminocyclopropane-1- carboxylic (ACC) oxidase activation. Journal of Plant Physiology 147, 182–190.CrossRefGoogle Scholar
Marion-Poll, A. (1997) ABA and seed development. Trends in Plant Science 2, 447–448.CrossRefGoogle Scholar
Matilla, A.J. (1996) Polyamines and seed germination. Seed Science Research 6, 81–93.Google Scholar
Matilla, A.J. (2000) Ethylene in seed formation and germination. Seed Science Research 10, 111–126.CrossRefGoogle Scholar
Miyazaki, J.H. and Yang, S.F. (1987) The methionine salvage pathway in relation to ethylene and polyamine biosynthesis. Physiologia Plantarum 69, 366–370.CrossRefGoogle Scholar
Munoz De Rueda, P.M., Gallardo, M., Sánchez-Calle, I.M. and Matilla, A.J. (1994) Germination of chick-pea seeds in relation to manipulation of the ethylene pathway and polyamine biosynthesis by inhibitors. Plant Science 97, 31–37.Google Scholar
Munoz De Rueda, P.M., Gallardo, M., Matilla, A.J. and Sánchez-Calle, I.M. (1995) Preliminary characterization of 1-aminocyclopropane-1-carboxylate oxidase properties from embryonic axes of chick-pea (Cicer arietinum L.) seeds. Journal of Experimental Botany 46, 695–700.CrossRefGoogle Scholar
Nakagawa, N., Mori, H., Yamazaki, K. and Imaseki, H. (1991) Cloning of a complementary DNA for auxin- induced 1-aminocyclopropane-1-carboxylate synthase and differential expression of the gene by auxin and wounding. Plant and Cell Physiology 32, 1153–1163.Google Scholar
Olson, D.C., White, J.A., Edelman, L., Harkins, R.N. and Kende, H. (1991) Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. Proceedings of the National Academy of Sciences USA 88, 5340–5344.CrossRefGoogle ScholarPubMed
Peck, S.C. and Kende, H. (1995) Sequential induction of the ethylene biosynthesis enzymes by indole-3-acetic acid in etiolated peas. Plant Molecular Biology 28, 293–301.Google Scholar
Peck, S.C. and Kende, H. (1998) Differential regulation of genes encoding 1-aminocyclopropane-carboxylate (ACC) synthase in etiolated pea seedlings: effects of indole-3-acetic acid, wounding, and ethylene. Plant Molecular Biology 38, 977–982.CrossRefGoogle Scholar
Peck, S.C., Reinhardt, D., Olson, D.C., Boller, T. and Kende, H. (1992) Localization of the ethylene-forming enzyme from tomatoes, 1-aminocyclopropane-1- carboxylate oxidase, in transgenic yeast. Journal of Plant Physiology 140, 681–686.Google Scholar
Peck, S.C., Olson, D.C. and Kende, H. (1993) A cDNA sequence encoding 1-aminocyclopropane-1-carboxylate oxidase from pea. Plant Physiology 101, 689–690.Google Scholar
Petruzzelli, L., Coraggio, I. and Leubner-Metzger, G. (2000) Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1- aminocyclopropane-1-carboxylic acid oxidase. Planta 211, 144–149.CrossRefGoogle Scholar
Ramassamy, S., Olmos, E., Bouzayen, M., Pech, J.C. and Latché, A. (1998) 1-aminocyclopropane-1-carboxylate oxidase of apple fruit is periplasmic. Journal of Experimental Botany 49, 1909–1915.Google Scholar
Reinhardt, D., Kende, H. and Boller, T. (1994) Subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in tomato cells. Planta 195, 142–146.CrossRefGoogle Scholar
Rodríguez, D., Nicolás, G., Aldasoro, J.J., Hernández- Nistal, J., Babiano, M.J. and Matilla, A. (1985) Altered development of polysomal RNA activity in chick-pea (Cicer arietinum) embryonic axes. Effects of abscisic acid and temperature. Planta 164, 517–523.Google Scholar
Rombaldi, C., Lelièvre, J.M., Latché, A., Petitprez, M., Bouzayen, M. and Pech, J.C. (1994) Immunocytolocalization of 1-aminocyclopropane-1- carboxylic acid oxidase in tomato and apple fruit. Planta 192, 453–460.CrossRefGoogle ScholarPubMed
Sakakibara, H., Watanabe, M., Hase, T. and Sugiyama, T. (1991) Molecular cloning and characterization of complementary DNA encoding for ferredoxindependent glutamate synthase in maize leaf. Journal of Biological Chemistry 266, 2028–2035.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning: A laboratory manual (2nd edition). Cold Spring Harbor, Cold Spring Harbor Laboratory Press.Google Scholar
Smith, J.J. and John, P. (1993) Activation of 1- aminocyclopropane-1-carboxylate oxidase by bicarbonate/carbon dioxide. Phytochemistry 32, 1381–1386.Google Scholar
Tang, X.Y., Gomes, A.M.T.R., Bhatia, A. and Woodson, W.R. (1994). Pistil-specific and ethylene-regulated expression of 1-aminocyclopropane-1-carboxylate oxidase genes in petunia flowers. The Plant Cell 6, 1227–1239.Google Scholar
Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences USA 76, 4350–4354.Google Scholar
Ververidis, P. and John, P. (1991) Complete recovery in vitro of ethylene-forming enzyme activity. Phytochemistry 30, 725–727.CrossRefGoogle Scholar
Wang, T.W. and Arteca, R.N. (1995) Identification and characterization of cDNAs encoding ethylene biosynthesis enzymes from Pelargonium – hortorum cv. Snow mass leaves. Plant Physiology 109, 627–636.CrossRefGoogle ScholarPubMed
Xu, Z.C., Ikoma, Y., Yano, M., Ogawa, K. and Hyodo, H. (1998) Varietal differences in the potential to produce ethylene and gene expression of ACC synthase and ACC oxidase between ‘Kui mi’ and ‘Hong xin’ of Chinese kiwifruit. Journal of the Japanese Society for Horticultural Science 67, 204–209.Google Scholar
Yoshii, H. and Imaseki, H. (1982) Regulation of auxininduced ethylene biosynthesis. Repression of inductive formation of 1-aminocyclopropane-1-carboxylate synthase by ethylene. Plant and Cell Physiology 23, 639–649.Google Scholar