Ethylene and fruit ripening

The latest advances in our understanding of the relationship between ethylene and fruit ripening are reviewed. Considerable progress has been made in the characterisation of genes encoding the key ethylene biosynthetic enzymes, ACC synthase (ACS) and ACC oxidase (ACO) and in the isolation of genes involved in the ethylene signal transduction pathway, particularly those encoding ethylene receptors (ETR). These have allowed the generation of transgenic fruit with reduced ethylene production and the identification of the Nr tomato ripening mutant as an ethylene receptor mutant. Through these tools, a clearer picture of the role of ethylene in fruit ripening is now emerging. In climacteric fruit, the transition to autocatalytic ethylene production appears to result from a series of events where developmentally regulated ACO and ACS gene expression initiates a rise in ethylene production, setting in motion the activation of autocatalytic ethylene production. Differential expression of ACS and ACO gene family members is probably involved in such a transition. Finally, we discuss evidence suggesting that the NR ethylene perception and transduction pathway is specific to a defined set of genes expressed in ripening climacteric fruit and that a distinct ETR pathway regulates other ethylene-regulated genes in both immature and ripening climacteric fruit as well as in non-climacteric fruit. The emerging picture is one where both ethylene-dependent and -independent pathways coexist in both climacteric and non-climacteric fruits. Further work is needed in order to dissect the molecular events involved in individual ripening processes and to understand the regulation of the expression of both ethylene-dependent and -independent genes.

[1]  J. Ecker,et al.  Activation of the Ethylene Gas Response Pathway in Arabidopsis by the Nuclear Protein ETHYLENE-INSENSITIVE3 and Related Proteins , 1997, Cell.

[2]  J. Ecker,et al.  Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. , 1995, Genetics.

[3]  D. Grierson,et al.  Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[4]  G. Bufler Ethylene-promoted conversion of 1-aminocyclopropane-1-carboxylic Acid to ethylene in peel of apple at various stages of fruit development. , 1986, Plant physiology.

[5]  P. John Ethylene biosynthesis: The role of 1‐aminocyclopropane‐1‐carboxylate (ACC) oxidase, and its possible evolutionary origin , 1997 .

[6]  J. B. Biale Growth, Maturation, and Senescence in Fruits: Recent knowledge on growth regulation and on biological oxidations has been applied to studies with fruits. , 1964, Science.

[7]  P. T. Atkey,et al.  The inhibition of tomato fruit ripening by silver. , 1984, Journal of plant physiology.

[8]  J. Ecker,et al.  Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. , 1990, The Plant cell.

[9]  R. Arteca,et al.  Purification and characterization of 1-aminocyclopropane-1-carboxylate N-malonyltransferase from etiolated mung bean hypocotyls. , 1992, Plant physiology.

[10]  G. Barry,et al.  Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. , 1991, The Plant cell.

[11]  A. Bennett,et al.  Regulation of tomato fruit polygalacturonase mRNA accumulation by ethylene: A Re-examination , 1998, Plant physiology.

[12]  A. Callahan,et al.  Isolation and Initial Characterization of cDNAs for mRNAs Regulated during Peach Fruit Development , 1993 .

[13]  M. Vendrell,et al.  Short-term activation of the conversion of 1-aminocyclopropane-1-carboxylic acid to ethylene in rewarmed granny Smith apples , 1993 .

[14]  D. G. Richardson,et al.  Differences in Biochemical Composition between ‘Beurre d’Anjou’ and ‘Bose’ Pears during Fruit Development and Storage1 , 1982, Journal of the American Society for Horticultural Science.

[15]  R. Fluhr,et al.  Ethylene: biosynthesis and perception , 1996 .

[16]  J. Pech,et al.  Ripening-associated biochemical traits of Cantaloupe Charentais melons expressing an antisense ACC oxidase transgene , 1997 .

[17]  R. Young,et al.  The Effect of Indole-3-acetic Acid and Other Growth Regulators on the Ripening of Avocado Fruits. , 1975, Plant physiology.

[18]  F. Mathooko Regulation of ethylene biosynthesis in higher plants by carbon dioxide , 1996 .

[19]  A. Purvis,et al.  Involvement of ethylene in chlorophyll degradation in peel of citrus fruits. , 1981, Plant physiology.

[20]  M. Ohme-Takagi,et al.  Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. , 1995, The Plant cell.

[21]  M. Serek,et al.  Inhibitors of ethylene responses in plants at the receptor level: Recent developments , 1997 .

[22]  D. Grierson,et al.  Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants , 1990, Nature.

[23]  S P Burg,et al.  Molecular requirements for the biological activity of ethylene. , 1967, Plant physiology.

[24]  E. Meyerowitz,et al.  Ethylene insensitivity conferred by Arabidopsis ERS gene. , 1995, Science.

[25]  J. Deikman Molecular mechanisms of ethylene regulation of gene transcription , 1997 .

[26]  R. Fischer,et al.  An Antisense Gene Stimulates Ethylene Hormone Production during Tomato Fruit Ripening. , 1992, The Plant cell.

[27]  D. Dilley,et al.  Induction of ethylene synthesizing competency in Granny Smith apples by exposure to low temperature in air , 1991 .

[28]  M. Vendrell Effect of abscisic acid and ethephon on several parameters of ripening in banana fruit tissue , 1985 .

[29]  S. Blankenship,et al.  ETHYLENE BINDING SITE AFFINITY IN RIPENING APPLES , 1993 .

[30]  M. Estelle,et al.  Insensitivity to Ethylene Conferred by a Dominant Mutation in Arabidopsis thaliana , 1988, Science.

[31]  M. Saltveit,et al.  The Lack of a Respiratory Rise in Muskmelon Fruit Ripening on the Plant Challenges the Definition of Climacteric Behaviour , 1993 .

[32]  S. Yang,et al.  Autoinhibition of Ethylene Production in Citrus Peel Discs : SUPPRESSION OF 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID SYNTHESIS. , 1982, Plant Physiology.

[33]  W. Schuch,et al.  Reduced ethylene synthesis in EFE antisense tomatoes has differential effects on fruit ripening processes , 1993 .

[34]  M. E. Patterson,et al.  Effects of ethephon on the respiration and ethylene evolution of sweet cherry (Prunus avium L.) fruit at different development stages. , 1994 .

[35]  J. Giovannoni Molecular Genetic Analysis of Ethylene-Regulated and Developmental Components of Tomato Fruit Ripening , 1997 .

[36]  D. G. Richardson,et al.  Effects of exogenous propylene and fruit calcium on ripening of non-chilled and chilled Anjou pears , 1996 .

[37]  J. Giovannoni,et al.  The use of transgenic and naturally occurring mutants to understand and manipulate tomato fruit ripening , 1994 .

[38]  W. Kliewer,et al.  Ethephon ((2-Chloroethyl) phosphonic Acid, Ethrel, CEPA) in Viticulture - A Review , 1984, American Journal of Enology and Viticulture.

[39]  S. Yang,et al.  Ethylene Promotes the Capability To Malonylate 1-Aminocyclopropane-1-carboxylic Acid and d-Amino Acids in Preclimacteric Tomato Fruits. , 1985, Plant physiology.

[40]  S. Yang,et al.  The Conversion of 1-(Malonylamino)cyclopropane-1-Carboxylic Acid to 1-Aminocyclopropane-1-Carboxylic Acid in Plant Tissues. , 1986, Plant physiology.

[41]  W. Mcglasson,et al.  Treatment of Fruit with Propylene gives Information about the Biogenesis of Ethylene , 1972, Nature.

[42]  Cornelius S. Barry,et al.  Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. , 1996, The Plant journal : for cell and molecular biology.

[43]  J. R. Gorny,et al.  Controlled-atmosphere Suppression of ACC Synthase and ACC Oxidase in 'Golden Delicious' Apples during Long-term Cold Storage , 1996 .

[44]  A. Bennett,et al.  The respiratory climacteric is present in Charentais (Cucumis melo cv. Reticulatus F1 Alpha) melons ripened on or off the plant , 1995 .

[45]  N. Hoffman,et al.  Promotion by Ethylene of the Capability to Convert 1-Aminocyclopropane-1-carboxylic Acid to Ethylene in Preclimacteric Tomato and Cantaloupe Fruits. , 1985, Plant physiology.

[46]  R. Saftner,et al.  Purification and Characterization of 1-Aminocyclopropane-1-Carboxylic Acid N-Malonyltransferase from Tomato Fruit , 1995, Plant physiology.

[47]  C. Frenkél,et al.  Auxin inhibition of ripening in bartlett pears. , 1973, Plant physiology.

[48]  S. Yang,et al.  Purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from apple fruit. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[49]  J. Pech,et al.  Partial purification and properties of a 36-kDa 1-aminocyclopropane-1-carboxylate N-malonyltransferase from mung bean , 1995 .

[50]  T. A. Wheaton,et al.  Carotenoids in citrus. Their accumulation induced by ethylene , 1972 .

[51]  J. Alonso,et al.  A Putative Vacuolar Processing Protease Is Regulated by Ethylene and also during Fruit Ripening in Citrus Fruit , 1995, Plant physiology.

[52]  E. Meyerowitz,et al.  Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. , 1993, Science.

[53]  Hsiao-Ching Yen,et al.  An Ethylene-Inducible Component of Signal Transduction Encoded by Never-ripe , 1995, Science.

[54]  P. Oeller,et al.  Reversible inhibition of tomato fruit senescence by antisense RNA. , 1991, Science.

[55]  L. Mcintosh Molecular Biology of the Alternative Oxidase , 1994, Plant physiology.

[56]  C. Hartmann,et al.  Conséquences d'un séjour au froid sur le métabolisme de l'héthylène au cours de la maturation de la poire Passe-Crassane après récolte , 1985 .

[57]  M. Kneissl,et al.  The Tomato E8 Gene Influences Ethylene Biosynthesis in Fruit but Not in Flowers , 1996, Plant physiology.

[58]  J. Pech,et al.  Isolation of a ripening and wound-induced cDNA from Cucumis melo L. encoding a protein with homology to the ethylene-forming enzyme. , 1993, European journal of biochemistry.

[59]  M. Saltveit,et al.  Morphological and Physiological Changes during Fruit Growth and Maturation of Seven Melon Cultivars , 1991 .

[60]  A. Bennett,et al.  ROLE OF CELL WALL HYDROLASES IN FRUIT RIPENING , 1991 .

[61]  Shangfa Yang,et al.  1-Aminocyclopropanecarboxylate synthase, a key enzyme in ethylene biosynthesis. , 1979, Archives of biochemistry and biophysics.

[62]  N. Hoffman,et al.  Identification of 1-(malonylamino) cyclopropane-1-carboxylic acid as a major conjugate of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor in higher plants. , 1982, Biochemical and biophysical research communications.

[63]  J. Pech,et al.  Cold-induced accumulation of 1-aminocyclopropane 1-carboxylate oxidase protein in Granny Smith apples , 1995 .

[64]  J. Ecker,et al.  Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. , 1998, Genes & development.

[65]  C Chang,et al.  The ethylene signal transduction pathway in Arabidopsis: an emerging paradigm? , 1996, Trends in biochemical sciences.

[66]  S. Tanksley,et al.  The Tomato Never-ripe Locus Regulates Ethylene-Inducible Gene Expression and Is Linked to a Homolog of the Arabidopsis ETR1 Gene , 1995, Plant physiology.

[67]  K. Thimann,et al.  THE PHYSIOLOGY OF ETHYLENE FORMATION IN APPLES. , 1959, Proceedings of the National Academy of Sciences of the United States of America.

[68]  J. Pech,et al.  Carrier-Mediated Uptake of 1-(Malonylamino)cyclopropane-1-Carboxylic Acid in Vacuoles Isolated from Catharanthus roseus Cells. , 1989, Plant physiology.

[69]  M. Saltveit,et al.  Effect of silver ions on ethylene biosynthesis by tomato fruit tissue. , 1987, Plant physiology.

[70]  Joseph R. Ecker,et al.  CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases , 1993, Cell.

[71]  S. Cordes,et al.  Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[72]  J. Bailey-Serres,et al.  Pummelo Fruit Transcript Homologous to Ripening-Induced Genes , 1995, Plant physiology.

[73]  D. Starrett,et al.  The Effect of Ethylene and Propylene Pulses on Respiration, Ripening Advancement, Ethylene-Forming Enzyme, and 1-Aminocyclopropane-1-carboxylic Acid Synthase Activity in Avocado Fruit. , 1991, Plant physiology.

[74]  W. Yip,et al.  Cyanide metabolism in relation to ethylene production in plant tissues. , 1988, Plant physiology.

[75]  M. Van Montagu,et al.  Genetic and Physiological Analysis of a New Locus in Arabidopsis That Confers Resistance to 1-Aminocyclopropane-1-Carboxylic Acid and Ethylene and Specifically Affects the Ethylene Signal Transduction Pathway , 1993, Plant physiology.

[76]  J. Cohen,et al.  Measurement of Indole-3-Acetic Acid in Peach Fruits (Prunus persica L. Batsch cv Redhaven) during Development. , 1987, Plant physiology.

[77]  A. Bennett,et al.  Molecular cloning of tomato fruit polygalacturonase: Analysis of polygalacturonase mRNA levels during ripening. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[78]  P. Boss,et al.  Analysis of the Expression of Anthocyanin Pathway Genes in Developing Vitis vinifera L. cv Shiraz Grape Berries and the Implications for Pathway Regulation , 1996, Plant physiology.

[79]  T. Solomos Cyanide-Resistant Respiration in Higher Plants , 1977 .

[80]  H J Klee,et al.  The never ripe mutation blocks ethylene perception in tomato. , 1994, The Plant cell.

[81]  S. Yang,et al.  Inhibition of ethylene production by 2,4-dinitrophenol and high temperature. , 1980, Plant physiology.

[82]  G. Bufler Ethylene-Enhanced 1-Aminocyclopropane-1-carboxylic Acid Synthase Activity in Ripening Apples. , 1984, Plant physiology.

[83]  A. Bleecker,et al.  The Ethylene Response Mediator ETR1 from Arabidopsis Forms a Disulfide-linked Dimer (*) , 1995, The Journal of Biological Chemistry.

[84]  D. Inzé,et al.  Structure and expression analyses of the S-adenosylmethionine synthetase gene family in Arabidopsis thaliana. , 1989, Gene.

[85]  E. Woltering,et al.  Investigation of Local Ethylene Emission from Intact Cherry Tomatoes by Means of Photothermal Deflection and Photoacoustic Detection. , 1995, Plant physiology.

[86]  P. Larsen,et al.  Cloning and nucleotide sequence of a s-adenosylmethionine synthetase cDNA from carnation. , 1991, Plant physiology.

[87]  E. Sisler Partial Purification of an Ethylene-binding Component from Plant Tissue. , 1980, Plant physiology.

[88]  A. Bleecker,et al.  The Mechanism of Ethylene Perception , 1996, Plant physiology.

[89]  G. Tucker,et al.  Biochemistry of Fruit Ripening , 1993, Springer Netherlands.

[90]  A. Kanellis,et al.  Suppression of cellulase and polygalacturonase and induction of alcohol dehydrogenase isoenzymes in avocado fruit mesocarp subjected to low oxygen stress. , 1991, Plant physiology.

[91]  E. Buse,et al.  Ethylene-Mediated Posttranscriptional Regulation in Ripening Avocado (Persea americana) Mesocarp Discs , 1993, Plant physiology.

[92]  S. Lurie,et al.  Reversible Inhibition of Tomato Fruit Gene Expression at High Temperature (Effects on Tomato Fruit Ripening) , 1996, Plant physiology.

[93]  J. Andrews The climacteric respiration rise in attached and detached tomato fruit , 1995 .

[94]  M. Saltveit Internal carbon dioxide and ethylene levels in ripening tomato fruit attached to or detached from the plant , 1993 .

[95]  J. Raynal,et al.  Differential Expression of ACC Oxidase Genes in Melon and Physiological Characterization of Fruit Expressing an Antisense ACC Oxidase Gene , 1997 .

[96]  H. Terai Behaviors of 1-Aminocyclopropane-1-carboxylic Acid (ACC) and ACC Synthase Responsible for Ethylene Production in Normal and Mutant (nor and rin) Tomato Fruits at Various Ripening Stages , 1993 .

[97]  M. Knee Do tomatoes on the plant behave as climacteric fruits , 1995 .

[98]  A C Cameron,et al.  A simple method for the determination of resistance to gas diffusion in plant organs. , 1982, Plant physiology.

[99]  A. Hamilton,et al.  Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene‐forming enzyme transgene , 1993 .

[100]  J. Pech,et al.  Structure and expression of three genes encoding ACC oxidase homologs from melon ( , 1996 .

[101]  M. Lay-Yee,et al.  A Full-Length cDNA Encoding 1-Aminocyclopropane-1-Carboxylate Synthase from Apple , 1995, Plant physiology.

[102]  A. Theologis,et al.  Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme for ethylene biosynthesis in plants. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[103]  D. J. James,et al.  Transgenes Display Stable Patterns of Expression in Apple Fruit and Mendelian Segregation in the Progeny , 1996, Bio/Technology.

[104]  M. Knee Development of Ethylene Biosynthesis in Pear Fruits at —1 °C , 1987 .

[105]  J. Cohen,et al.  A New 1-Aminocyclopropane-1-Carboxylic Acid-Conjugating Activity in Tomato Fruit , 1995, Plant physiology.

[106]  P. Oeller,et al.  1-aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. , 1991, Journal of molecular biology.

[107]  G. Kim,et al.  Effect of ethylene on postharvest life of strawberries , 1995 .

[108]  P. Oeller,et al.  Use of a tomato mutant constructed with reverse genetics to study fruit ripening, a complex developmental process. , 1993, Developmental genetics.

[109]  S. Shiomi,et al.  Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. , 1998, Plant physiology.

[110]  E. Goldschmidt,et al.  Ethylene induces de novo synthesis of chlorophyllase, a chlorophyll degrading enzyme, in Citrus fruit peel. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[111]  H. Mori,et al.  Cloning of a Complementary DNA for Auxin-Induced 1-Aminocyclopropane-1-carboxylate Synthase and Differential Expression of the Gene by Auxin and Wounding , 1991 .

[112]  Shangfa Yang,et al.  Effects of Fruit Detachment on Ethylene Biosynthesis and Loss of Flesh Firmness, Skin Color, and Starch in Ripening ‘Golden Delicious’ Apples , 1986, Journal of the American Society for Horticultural Science.

[113]  P. Leung,et al.  Immunopurification and Characterization of a 40-kD 1-Aminocyclopropane-1-Carboxylic Acid N-Malonyltransferase from Mung Bean Seedling Hypocotyls , 1997, Plant physiology.

[114]  G. Laties The Cyanide-Resistant, Alternative Path in Higher Plant Respiration , 1982 .

[115]  M. Vendrell,et al.  Inhibition of Ethylene Production in Banana Fruit Tissue by Ethylene Treatment , 1971 .

[116]  T. Boller,et al.  Analysis and cloning of the ethylene‐forming enzyme from tomato by functional expression of its mRNA in Xenopus laevis oocytes. , 1991, The EMBO journal.

[117]  N. Lallu,et al.  Effect of diazocyclopentadiene (DACP) on tomato fruits harvested at different ripening stages , 1994 .

[118]  Ecker The ethylene signal transduction pathway in plants , 1995, Science.

[119]  G. Ross,et al.  Antisense apple ACC-oxidase RNA reduces ethylene production in transgenic tomato fruit , 1997 .

[120]  M. Knee,et al.  Initiation of Rapid Ethylene Synthesis by Apple and Pear Fruits in Relation to Storage Temperature , 1983 .

[121]  M. Van Montagu,et al.  Cloning and sequence of two different cDNAs encoding 1-aminocyclopropane-1-carboxylate synthase in tomato. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[122]  F. B. Abeles CHAPTER 6 – Fruit Ripening, Abscission, and Postharvest Disorders , 1992 .

[123]  J. Pech,et al.  Expression of ACC oxidase antisense gene inhibits ripening of cantaloupe melon fruits , 1996, Nature Biotechnology.

[124]  Cornelius S. Barry,et al.  EFE Multigene Family in Tomato Plants: Expression and Characterization , 1993 .

[125]  G. Eric Schaller,et al.  Ethylene-Binding Sites Generated in Yeast Expressing the Arabidopsis ETR1 Gene , 1995, Science.

[126]  N. Hoffman,et al.  Ethylene biosynthesis and its regulation in higher plants , 1984 .

[127]  H. Klee Ripening Physiology of Fruit from Transgenic Tomato (Lycopersicon esculentum) Plants with Reduced Ethylene Synthesis , 1993, Plant physiology.

[128]  D. Olson,et al.  Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[129]  S. Gazit,et al.  Water-deficit Stress, Ethylene Production, and Ripening in Avocado Fruits. , 1974, Plant physiology.

[130]  W. Yip,et al.  Differential accumulation of transcripts for four tomato 1-aminocyclopropane-1-carboxylate synthase homologs under various conditions. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[131]  J. Pech,et al.  Metabolism of 1‐aminocyclopropane‐1‐carboxylic acid in ripening apple fruits , 1986 .

[132]  M. E. Patterson,et al.  Changes in jasmonic acid concentration during early development of apple fruit , 1997 .

[133]  Drake,et al.  Upregulation of two ripening-related genes from a non-climacteric plant (pepper) in a transgenic climacteric plant (tomato) , 1998 .

[134]  M. Zeroni,et al.  Autoinhibition of Ethylene Formation in Nonripening Stages of the Fruit of Sycomore Fig (Ficus sycomorus L.). , 1976, Plant physiology.

[135]  M. Lieberman Biosynthesis and Action of Ethylene , 1979 .