Abstract
Passe-Crassane pears require a 3-month chilling treatment at 0 °C to be able to produce ethylene and ripen autonomously after subsequent rewarming. The chilling treatment strongly stimulated ACC oxidase activity, and to a lesser extent ACC synthase activity. At the same time, the levels of mRNAs hybridizing to ACC synthase and ACC oxidase probes increased dramatically. Fruit stored at 18 °C immediately after harvest did not exhibit any of these changes, while fruit that had been previously chilled exhibited a burst of ethylene production associated with high activity of ACC oxidase and ACC synthase upon rewarming. ACC oxidase mRNA strongly accumulated in rewarmed fruits, while ACC synthase mRNA level decreased. The chilling-induced accumulation of ACC synthase and ACC oxidase transcripts was strongly reduced when ethylene action was blocked during chilling with 1-methylcyclopropene (1-MCP). Upon rewarming ACC synthase and ACC oxidase transcripts rapidly disappeared in 1-MCP-treated fruits. A five-week treatment of non-chilled fruits with the ethylene analog propylene led to increased expression of ACC oxidase and to ripening. However, ethylene synthesis, ACC synthase activity and ACC synthase mRNAs remained at very low level. Our data indicate that ACC synthase gene expression is regulated by ethylene only during, or after chilling treatment, while ACC oxidase gene expression can be induced separately by either chilling or ethylene.
Similar content being viewed by others
References
Abeles FB, Morgan PW, Saltveit ME: Ethylene in Plant Biology, 2nd ed. Academic Press, New York (1992).
Autio WB, Bramlage WJ: Chilling sensitivity of tomato fruit in relation to ripening and senescence. J Am Soc Hort Sci 111: 201–204 (1986).
Blankenship SM, Richardson DG: Development of ethylene biosynthesis and ethylene-induced ripening in d'Anjou pears during the cold requirement for ripening. J Am Soc Hort Sci 110: 520–523 (1985).
Bouzayen M, Cooper W, Barry C, Zegzouti H, Hamilton AJ, Grierson D: EFE multigene family in tomato plant: expression and charaterization. In: Pech J-C, Latché A, Balagué C (eds) Cellular and Molecular Aspects of the Plant Hormone Ethylene, pp. 76–81. Kluwer Academic Publishers, Dordrecht (1993)
Bufler G: Ethylene-promoted conversion of 1-aminocyclopropane 1-carboxylic acid to ethylene in apple at various stages of fruit development. Plant Physiol 80: 539–543 (1986).
Chandler PM, Robertson M: Gene expression regulated by abscisic asid and its relationship to stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 45: 113–141 (1994).
Chen PM, Richardson DG, Mellenthin WM: Differences in biochemical composition between ‘Beurré d'Anjou’ and ‘Bosc’ pears during fruit development and storage. J Am Soc Hort Sci 107: 807–812 (1982).
Chomszynski P, Sacchi N: Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156–159 (1987).
Dong JG, Fernandez-Maculet JC, Yang SF: Purification and characterization of a 1-aminocyclopropane-1-carboxylate oxidase from apple fruit. Proc Natl Acad Sci USA 89: 9789–9793 (1992).
Dong JG, Kim WT, Yip WK, Thompson GA, Li L, Bennett AB, Yang SF: Cloning of a cDNA encoding 1-aminocyclopropane-1-carboxylate synthase and expression of its mRNA in ripening apple fruit. Planta 185: 38–45 (1991).
Dong JG, Olson D, Silverstone A, Yang SF: Sequence of a cDNA coding for a 1-aminocyclopropane-1-carboxylate oxidase homolog. Plant Physiol 98: 1530–1531 (1992).
Dopico B, Lowe AL, Wilson ID, Merodio C, Grierson D: Cloning and characterization of avocado fruit mRNAs and their expression during ripening and low-temperature storage. Plant Mol Biol 21: 437–449 (1993).
Drouet A, Hartmann C: Polyribosomes from pear fruit. II. Changes occuring in pulp tissues during ripening and senescence. Plant Physiol 69: 885–887 (1982).
Dupille E, Rombaldi C, Lelièvre J-M, Cleyet-Marel J-C, Pech J-C, Latché A: Purification, properties and partial amino acid sequence of 1-aminocyclopropane-1-carboxylic acid oxidase from apple fruits. Planta 190: 65–70 (1993).
Dupille E, Sisler EC: Effects of an ethylene receptor antagonist on plant material. In: Ait-Oubahou A, El-Otmani M (eds) Postharvest Physiology, Pathology and Technologies for Horticultural Commodities: Recent Advances, pp. 294–301. Published by J.A.V. Hassan II, Marocco (1995).
Feinberg AP, Vogelstein B: Atechnique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6-13 (1983).
Hamilton AJ, Bouzayen M, Grierson D: Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. Proc Natl Acad Sci USA 88: 7434–7437 (1991).
Hansen E, Hartman H: Effect of ethylene and certain metabolic gases upon respiration and ripening of pears before and after cold storage. Plant Physiol 12: 441–454 (1937).
Jobling J, McGlasson WB, Dilley DR: Induction of ethylene synthesizing competency in Granny Smith apples by exposure to low temperature in air. Postharv Biol Technol 1: 111–118 (1991).
Kende H: Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44: 283–307 (1993).
Kim WT, Silverstone A, Yip WK, Dong JG, Yang SF: Induction of 1-aminocyclopropane-1-carboxylate synthase mRNA by auxin in mung bean hypocotyls and cultured apple shoots. Plant Physiol 98: 465–471 (1992).
Kim WT, Yang SF: Structure and expression of cDNAs encoding 1-aminocyclopropane-1-carboxylate oxidase homologs isolated from excised mung bean hypocotyls. Planta 194: 223–229 (1994).
Knee M: Development of ethylene biosynthesis in pear fruits at –1 °C. J Exp Bot 38: 1724–1733 (1987).
Knee M, Looney NE, Hatfield SGS, Smith SM: Initiation of rapid ethylene synthesis by apple and pear fruits in relation to storage temperature. J Exp Bot 34: 1207–1212 (1983).
Larrigaudière C, Vendrell M: Short-term activation of the conversion of 1-aminocyclopropane-1-carboxylic acid to ethylene in rewarmed Granny Smith apples. Plant Physiol Biochem 31: 585–591 (1993).
Lasserre E, Bouquin T, Hernandez J, Bull J, Pech J-C, Balagu é C: Structure and expression of three genes encoding ACC homologs frommelon (Cucumis melo L.). Mol Gen Genet 251: 81–90 (1996).
Lay-Yee M, Knighton ML: A full length cDNA encoding 1-aminocyclopropane-1-carboxylate synthase from apple. Plant Physiol 107: 1017–1018 (1995).
Lelièvre J-M, Tichit L, Fillion L, Larrigaudière C, Vendrell M, Pech J-C: Cold-induced accumulation of 1-aminocyclopropane-1-carboxylate oxidase protein in Granny Smith apples. Postharvest Biol Technol 5: 11–17 (1995).
Liu Y, Hoffman NE, Yang SF. Promotion by ethylene of the capability to convert 1-aminocyclopropane-1-carboxylic acid to ethylene in preclimacteric tomato and cantaloupe fruits. Plant Physiol 77: 407–411 (1985).
Looney NE: Interactions of harvest maturity cold storage and two growth-regulators on ripening of ‘Bartlett’ pears. J Am Soc Hort Sci 97: 81–83 (1972).
Lyons JM: Chilling injury in plants. Annu Rev Plant Physiol 24: 445–466 (1973).
McMurchie EJ, McGlasson WB, Eaks IL: Treatment of fruit with polypropylene gives information about the biogenesis of ethylene. Nature 237: 235–236 (1972).
Manning K: Isolation of nucleic acids from plants by differential solvent precipitation. Anal Biochem 195: 45–50 (1991).
Morin F, Rigault C, Hartmann C: Conséquences d'un séjour au froid sur lemétabolisme de l'éthylène au cours de lamaturation de la poire Passe-Crassane après récolte. Physiol Vég 23: 353–359 (1985).
Palva ET: Gene expression under temperature stress. In: Basra AS (ed) Stress-induced Gene Expression in Plants, pp. 103-130. Harwood Academic Publishers, Switzerland (1994).
Picton S, Barton SL, Bouzayen M, Hamilton AJ, Grierson D: Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J 3: 469–481 (1993).
Ross GS, Knighton ML, Lay-Yee M: An ethylene-related cDNA from ripening apples. Plant Mol Biol 19: 231–238 (1992).
Rudnicky R, Machnik J, Pieniazek J: Accumulation of abscisic acid during ripening of pears (Clapp's Favourite) in various storage conditions. Bull Acad Pol Sci ClV 16: 509–512 (1968).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Serek M, Sisler EC, Reid MS: Novel gaseous ethylene-binding inhibitor prevents ethylene effects in potted flowering plants. J Am Hort Sci 119: 1230–1233 (1994).
Spanu P, Boller T, Kende H: Differential accumulation of transcripts of 1-aminocyclopropane-1-carboxylate synthase in tomato plants infected with Phytophtora infestans and elicitortreated tomato cell suspensions. J Plant Physiol 141: 557–562 (1993).
Theologis A: One rotten apple spoils the whole bushel: the role of ethylene in fruits ripening. Cell: 70: 181–184 (1992).
Theologis A, Oeller PW, Wong LM, Rottmann WH, Gantz DM: Use of a tomato mutant constructed with reverse genetics to study fruit ripening, a complex developmental process. Devel Genet 14: 282–295 (1993).
Ulrich R: Temperature and maturation: pears require preliminary cold treatment. Rec Adv Bot 1961: 1172–1176 (1961).
Ulrich R, Paulin A: Sur la complexité des conditions thermiques de la maturation des poires Passe-Crassane. C R Acad Agric Fr 40: 280–282 (1954).
Ulrich R, Paulin A: Sur la maturation des poires Passe-Crassane. C R Acad Agric Fr 40: 603–604 (1954).
Wang CY, Adams DO: Chilling-induced ethylene production in cucumbers (Cucumis sativus L.). Plant Physiol 69: 424–427 (1982).
Wang CY, Mellenthin WH, Hansen E: Effect of temperature on development of premature ripening in Bartlett pears. J Am Soc Hort Sci 96: 122–125 (1971).
Wang CY, Wang SY, Mellenthin WM: Identification of abscisic acid in Bartlett pears and its relationship to premature ripening. J Agric Food Chem 20: 451–453 (1972).
Watkins CB, Picton S, Grierson D: Stimulation and inhibition of expression of ripening-related mRNAs in tomatoes as influenced by chilling temperatures. J Plant Physiol 136: 318–323 (1990).
Wilson ID, Tucker GA, Knee M, Grierson D: Changes in mRNA during low temperature storage and ripening of pears. Phytochemistry 29: 2407–2409 (1990).
Woodson WR, Park KY, Drory A, Larsen PB, Wang H: Expression of ethylene biosynthetic pathway transcripts in senesning carnations flowers. Plant Physiol 99: 526–532 (1992).
Yang, SF, Hoffmann NE: Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35: 155–189 (1984).
Yip WK, Dong JG, Yang SF: Purification and characterization of 1-aminocyclopropane-1-carboxylatate synthase from apple fruits. Plant Physiol 95: 251–257 (1991).
Zarembinski TI, Theologis A: Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26: 1579–1597 (1994).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lelièvre*, JM., Tichit, L., Dao, P. et al. Effects of chilling on the expression of ethylene biosynthetic genes in Passe-Crassane pear (Pyrus communis L.) fruits. Plant Mol Biol 33, 847–855 (1997). https://doi.org/10.1023/A:1005750324531
Issue Date:
DOI: https://doi.org/10.1023/A:1005750324531