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Repression of the pea lipoxygenase gene loxg is associated with carpel development

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Abstract

A cDNA clone (loxg) corresponding to a gene repressed during carpel development has been isolated from a cDNA library of unpollinated carpels induced to grow by treatment with gibberellic acid (GA3). The sequences of loxg cDNA and the deduced polypeptide have a high similarity with legume type 2 lipoxygenases, especially with Phaseolus lox1 (78.5% similarity at the protein level) and pea and soybean lox3 (83.6% and 85.4%, respectively). loxg expression is constant in unstimulated carpels but it decreases in carpels induced to keep growing by fertilization or hormone treatment. A similar pattern of repression was observed in lipoxygenase activity of pea and tomato carpels. In situ hybridization studies showed that loxg mRNAs are present in the endocarp and the mesocarp of pea pods; no loxg expression was detectable either in the pod exocarp or in the ovules. Loxg is also expressed in other young growing tissues, especially in flower organs. Nevertheless, the natural pattern of flower and fruit development is associated with loxg repression.

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References

  1. Anstis PJP, Friend J: The isoenzyme distribution of etiolated pea seedling lipoxygenase. Planta 115: 329–335 (1974).

    Google Scholar 

  2. Axelrod B, Cheesbrough TM, Laakso S: Lipoxygenase from soybean. Meth Enzymol 71: 441–451 (1981).

    Google Scholar 

  3. Bell E, Mullet JE: Lipoxygenase gene expression is modulated in plants by water deficit, wounding and methyl jasmonate. Mol Gen Genet 230: 456–462 (1991).

    Google Scholar 

  4. Bell E, Mullet JE: Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol 103: 1133–1137 (1993).

    Google Scholar 

  5. Beltrán JP, Estruch JJ, Cañas L, Parets-Soler A: Assimilate unloading in the pea pod controlled by gibberellins. In: Bonnemain JL, Delrot S, Lucas WJ, Dainty J, (eds) Recent Advances in Phloem Transport and Assimilate Compartmentation, pp. 275–282. Quest, Nantes, France (1991).

    Google Scholar 

  6. Ben-Aziz A, Grossman S, Ascarelli I, Budowski P: Linoleate oxidation induced by lipoxygenase and heme proteins: a direct spectrophotometric assay. Anal Biochem 34: 88–100 (1970).

    Google Scholar 

  7. Boyington JC, Gaffney BJ, Amzel LM: The three-dimensional structure of an arachidonic acid 15-lipoxygenase. Science 260: 1482–1486 (1993).

    Google Scholar 

  8. Bradford MM: 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 (1976).

    Google Scholar 

  9. Creelman RA, Bell E, Mullet JE: Involvement of a lipoxygenase-like enzyme in abscisic acid biosynthesis. Plant Physiol 99: 1258–1260 (1992).

    Google Scholar 

  10. Domoney C, Firmin JL, Sidebottom C, Ealing PM, Slabas A, Casey R: Lipoxygenase heterogeneity in Pisum sativum. Planta 181: 35–43 (1990).

    Google Scholar 

  11. Domoney C, Casey R, Turner L, Ellis N: Pisum lipoxygenase genes. Theor Appl Genet 81: 800–805 (1991).

    Google Scholar 

  12. Droillard MJ, Rouet-Mayer MA, Bureau JM, Laurière C: Membrane-associated and soluble lipoxygenase isoforms in tomato pericarp. Characterization and involvement in membrane alterations. Plant Physiol 103: 1211–1219 (1993).

    Google Scholar 

  13. Ealing PM, Casey R: The complete amino acid sequence of a pea (Pisum sativum) seed lipoxygenase predicted from a near full-length cDNA. Biochem J 253: 915–918 (1988).

    Google Scholar 

  14. Ealing PM, Casey R: The cDNA cloning of a pea (Pisum sativum) seed lipoxygenase. Biochem J 253: 929–932 (1989).

    Google Scholar 

  15. Eiben HG, Slusarenko AJ: Complex spatial and temporal expression of lipoxygenase genes during Phaseolus vulgaris (L.) development. Plant J 5: 123–135 (1994).

    Google Scholar 

  16. Estruch JJ, Beltrán JP: Changes in invertase activities precede ovary growth induced by gibberellic acid in Pisum sativum. Physiol Plant 81: 319–326 (1991).

    Google Scholar 

  17. Estruch JJ, Beltrán JP: Gibberellic acid stimulates acid invertase secretion in pea ovary protoplasts. FEBS Lett 279: 303–306 (1991).

    Google Scholar 

  18. García-Martínez JL, Beltrán JP: Interaction between vegetative and reproductive organs during early fruit development in pea. In: Karssen CM, van Loon LC, Vrengdenhil D (eds) Progress in Plant Growth Regulation, pp. 401–410, Kluwer Academic Publishers, Dordrecht, The Netherlands (1992).

    Google Scholar 

  19. García-Martínez JL, Carbonell J: Fruit set of unpollinated ovaries in Pisum sativum L. Influence of plant growth regulators. Planta 147: 451–456 (1980).

    Google Scholar 

  20. García-Martínez JL, Santes C, Croker SJ, Hedden P: Identification, quantitation and distribution of gibberellins in fruits of Pisum sativum L. cv. Alaska during pod development. Planta 184: 53–60 (1991).

    Google Scholar 

  21. Gillaspy G, Ben-David H, Gruissem W: Fruits: a developmental perspective. Plant Cell 5: 1439–1451 (1993).

    Google Scholar 

  22. Granell A, Harris N, Pisabarro AG, Carbonell J: Temporal and spatial expression of a thiolprotease gene during pea ovary senescence, and its regulation by gibberellin. Plant J 2: 907–915 (1992).

    Google Scholar 

  23. Grimes HD, Koetje DS, Franceschi VR: Expression, activity and cellular accumulation of methyl jasmonate-responsive lipoxygenase in soybean seedlings. Plant Physiol 100: 433–443 (1992).

    Google Scholar 

  24. Hamberg Mm, Gardner HW: Oxylipin pathway to jasmonates: biochemistry and biological significance. Biochem Biophys Acta 1165: 1–18 (1992).

    Google Scholar 

  25. Hardy DJ, Gallegos MAV, Gaunt JK: Extracts of Pisum sativum metabolise phospholipid via a lipoxygenase-like mechanism. Phytochemistry 30: 2889–2894 (1991).

    Google Scholar 

  26. Hedley CL, Ambrose MJ: An analysis of seed development in Pisum sativum L. Ann Bot 46: 89–105 (1980).

    Google Scholar 

  27. Hildebrand DF: Lipoxygenases. Physiol Plant 76: 249–253 (1989).

    Google Scholar 

  28. jahnke S, Bier D, Estruch JJ, Beltrán JP: Distribution of photoassimilates in the pea plant: chronology of events in non-fertilized ovaries and effects of gibberelllic acid. Planta 180: 53–60 (1989).

    Google Scholar 

  29. Kato T, Shirano Y, Kawazu T, Tada Y, Itoh E, Shibata D: A modified β-glucuronidase gene: sensitive detection of plant promoter activities in suspension-cultured cells of tobacco and rice. Plant Mol Biol Rep 9: 333–339 (1991).

    Google Scholar 

  30. Leshem YY: Interactions of cytokinins with lipid-associated oxy free radicals during senescence: a prospective mode of cytokinin action. Can J Bot 62: 2943–2949 (1984).

    Google Scholar 

  31. Longemann J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissue. Anal Biochem 163: 16–20 (1987).

    Google Scholar 

  32. Melan MA, Dong X, Endara ME, Davis KR, Ausubel FM, Peterman TK: An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid and methyl jasmonate. Plant Physiol 101: 441–450 (1993).

    Google Scholar 

  33. Ohta H, Shirano Y, Tanaka K, Morita Y, Shibata D: cDNA cloning of rice lipoxygenase L-2 and characterization using an active enzyme expressed from the cDNA in Escherichia coli. Eur J Biochem 206: 331–336 (1992).

    Google Scholar 

  34. Peretó JG, Beltrán JP, García-Martínez JL: The source of gibberellins in the parthenocarpic development of ovaries on topped pea plants. Planta 175: 493–499 (1988).

    Google Scholar 

  35. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  36. Sánchez-Beltrán MJ, Carbonell J, García-Martínez JL, López-Díaz I: Gene expression during two alternative pathways of ovary development in Pisum sativum: fruit development and ovary senscence. Physiol Plant 85: 69–76 (1992).

    Google Scholar 

  37. Schewe T, Rapoport SM, Kuhn H: Enzymology and physiology of reticulocyte lipoxygenase: comparison with other lipoxygenases. Adv Enzymol Mol Biol 58: 191–272 (1986).

    Google Scholar 

  38. Shibata D, Steczko J, Dixon JE, Andrews PC, Hermodson M, Axelrod B: Primary structure of soybean lipoxygenase L-2, J Biol Chem 263: 6816–6821 (1988).

    Google Scholar 

  39. Siedow JN: Plant lipoxygenase: structure and function. Annu Rev Plant Physiol Plant Mol Biol 42: 145–188 (1991).

    Google Scholar 

  40. Sommer H, Beltrán JP, Huijser P, Pape H, Lönnig WE, Saedler H, Schwarz-Sommer Zs: Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9: 605–613 (1990).

    Google Scholar 

  41. Vercher Y, Molowny A, Carbonell J: Gibberellic acid effects on the ultrastructure of endocarp cells of unpollinated ovaries of Pisum sativum. Physiol Plant 71: 302–308 (1987).

    Google Scholar 

  42. Vercher Y, Carbonell J: Changes in the structure of ovary tissues and in the ultrastructure of mesocarp cells during ovary senscence or fruit development induced by plant growth substances in Pisum sativum. Physiol Plant 81: 518–526 (1991).

    Google Scholar 

  43. Vick BA, Zimmerman DC: Oxidative systems for modification of fatty acids: the lipoxygenase pathway. In: Stumpf PK, Conn EE (eds). The Biochemistry of Plants vol. 9, pp. 53–90. Academic Press, Orlando, FL (1987).

    Google Scholar 

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  1. Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-CSIC, Camino Vera s/n, 46022, Valencia, Spain

    Manuel Rodríguez-Concepción & José Pío Beltrán

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  1. Manuel Rodríguez-Concepción
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  2. José Pío Beltrán
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Rodríguez-Concepción, M., Beltrán, J.P. Repression of the pea lipoxygenase gene loxg is associated with carpel development. Plant Mol Biol 27, 887–899 (1995). https://doi.org/10.1007/BF00037017

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  • DOI: https://doi.org/10.1007/BF00037017

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