Interactions between ethylene and auxin are crucial to the control of grape (Vitis vinifera L.) berry ripening

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Böttcher, Christine ^a   Burbidge, Crista A ^a   Boss, Paul K ^a   Davies, Christopher ^a  

^a CSIRO   (Australia)

Author keywords

Aminoethoxyvinylglycine; Auxin; Biosynthesis; Ethrel; Ethylene; Interaction; Ripening; Vitis vinifera

Indexed keywords

VITACEAE; VITIS; VITIS VINIFERA;

AMINOETHOXYVINYLGLYCINE; DRUG DERIVATIVE; ETHEPHON; ETHYLENE; ETHYLENE DERIVATIVE; GLYCINE; INDOLEACETIC ACID DERIVATIVE; MESSENGER RNA; ORGANOPHOSPHORUS COMPOUND; PHYTOHORMONE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; DRUG EFFECT; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYLOGENY; VITIS;

ARABIDOPSIS; BIOSYNTHETIC PATHWAYS; ETHYLENES; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GLYCINE; INDOLEACETIC ACIDS; ORGANOPHOSPHORUS COMPOUNDS; PHYLOGENY; PLANT GROWTH REGULATORS; PLANT PROTEINS; RNA, MESSENGER; TRANSCRIPTION, GENETIC; VITIS;

EID: 84890624243     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-222     Document Type: Article

References (84)

1. Rashotte AM, Chae HS, Maxwell BB, Kieber JJ. The interaction of cytokinin with other signals. Physiol Plant 2005, 123(2):184-194.
2. Rolland F, Moore B, Sheen J. Sugar sensing and signaling in plants. Plant Cell 2002, 14(suppl 1):S185-S205. 151255, 12045277.
3. Teale WD, Ditengou FA, Dovzhenko AD, Li X, Molendijk AM, Ruperti B, Paponov I, Palme K. Auxin as a model for the integration of hormonal signal processing and transduction. Mol Plant 2008, 1(2):229-237. 10.1093/mp/ssn006, 19825535.
4. Weiss D, Ori N. Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 2007, 144(3):1240-1246. 10.1104/pp.107.100370, 1914132, 17616507.
5. Zhang S, Wei Y, Lu Y, Wang X. Mechanisms of brassinosteroids interacting with multiple hormones. Plant Signal Behav 2009, 4(12):1117-1120. 10.4161/psb.4.12.9903, 2819435, 20514225.
6. Böttcher C, Davies C. Hormonal control of grape berry development and ripening. The Biochemistry of the Grape Berry, vol. 1 2012, 194-217. Sharjah: Bentham Science, Gerós H, Chaves MM, Delrot S.
7. Vendrell M, Palomer X. Hormonal control of fruit ripening in climacteric fruit. Acta Hortic 1998, 463:325-334.
8. Tucker GA. Introduction. Biochemistry of Fruit Ripening 1993, 1-51. London: Chapman and Hall, Seymour GB, Taylor JE, Tucker GA.
9. Iannetta PPM, Laarhoven L-J, Medina-Escobar N, James EK, McManus MT, Davies HV, Harren FJM. Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit. Physiol Plant 2006, 127(2):247-259.
10. Wang H, Huang H, Huang X. Differential effects of abscisic acid and ethylene on the fruit maturation of Litchi chinensis Sonn. Plant Growth Regul 2007, 52(3):189-198.
11. Alleweldt G, Koch R. Ethylene content in ripening grape berries. Vitis 1977, 16:263-271.
12. Chervin C, El-Kereamy A, Roustan J-P, Latché A, Lamon J, Bouzayen M. Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 2004, 167(6):1301-1305.
13. Düring H, Alleweldt G, Koch R. Studies on hormonal control of ripening in berries and grape vines. Acta Hortic 1978, 80:397-405.
14. Pilati S, Perazzolli M, Malossini A, Cestaro A, Demattè L, Fontana P, Dal Ri A, Viola R, Velasco R, Moser C. Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at vèraison. BMC Genomics 2007, 8(1):428. 10.1186/1471-2164-8-428, 2228314, 18034875.
15. Böttcher C, Harvey KE, Boss PK, Davies C. Ripening of grape berries can be advanced or delayed by reagents that either reduce or increase ethylene levels. Funct Plant Biol 2013, 40(6):566-581.
16. Coombe BG, Hale CR. The hormone content of ripening grape berries and the effects of growth substance treatments. Plant Physiol 1973, 51(4):629-634. 10.1104/pp.51.4.629, 366320, 16658384.
17. Hale CR, Coombe BG, Hawker JS. Effects of ethylene and 2-chloroethylphosphonic acid on the ripening of grapes. Plant Physiol 1970, 45(5):620-623. 10.1104/pp.45.5.620, 396475, 16657356.
18. Ban T, Ishimaru M, Kobayashi S, Shiozaki S, Goto-Yamamoto N, Horiuchi S. Abscisic acid and 2,4-dichlorophenoxyacetic acid affect the expression of anthocyanin biosynthetic pathway genes in 'Kyoho' grape berries. J Hortic Sci Biotechnol 2003, 78:586-589.
19. Böttcher C, Boss PK, Davies C. Acyl substrate preferences of an IAA-amido synthetase account for variations in grape (Vitis vinifera L.) berry ripening caused by different auxinic compounds indicating the importance of auxin conjugation in plant development. J Exp Bot 2011, 62(12):4267-4280. 10.1093/jxb/err134, 3153680, 21543520.
20. Böttcher C, Harvey K, Forde CG, Boss PK, Davies C. Auxin treatment of pre-veraison grape (Vitis vinifera L.) berries both delays ripening and increases the synchronicity of sugar accumulation. Aust J Grape Wine Res 2011, 17(1):1-8.
21. Böttcher C, Boss PK, Davies C. Delaying Riesling grape berry ripening with a synthetic auxin affects malic acid metabolism and sugar accumulation, and alters wine sensory characters. Funct Plant Biol 2012, 39(9):745-753.
22. Davies C, Boss PK, Robinson SP. Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and aters the expression of developmentally regulated genes. Plant Physiol 1997, 115(3):1155-1161. 158580, 12223864.
23. Hale CR. Growth and senescence of the grape berry. Aust J Agric Res 1968, 19(6):939-945.
24. Buta JG, Spaulding DW. Changes in indole-3-acetic acid and abscisic acid levels during tomato (Lycopersicon esculentum Mill.) fruit development and ripening. J Plant Growth Regul 1994, 13(3):163-166.
25. Mapelli S, Frova C, Torti G, Soressi GP. Relationship between set, development and activities of growth regulators in tomato fruits. Plant Cell Physiol 1978, 19(7):1281-1288.
26. Purgatto E, Oliveira do Nascimento JR, Lajolo FM, Cordenunsi BR. The onset of starch degradation during banana ripening is concomitant to changes in the content of free and conjugated forms of indole-3-acetic acid. J Plant Physiol 2002, 159(10):1105-1111.
27. Archbold DD, Dennis FG. Quantification of free ABA and free and conjugated IAA in strawberry achene and receptacle tissue during fruit development. J Am Soc Hortic Sci 1984, 109:330-335.
28. Symons GM, Chua Y-J, Ross JJ, Quittenden LJ, Davies NW, Reid JB. Hormonal changes during non-climacteric ripening in strawberry. J Exp Bot 2012, 63(13):4741-4750. 10.1093/jxb/ers147, 3428006, 22791823.
29. Böttcher C, Keyzers RA, Boss PK, Davies C. Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3-1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. J Exp Bot 2010, 61(13):3615-3625. 10.1093/jxb/erq174, 20581124.
30. Cawthon DL, Morris JR. Relationship of seed number and maturity to berry development, fruit maturation, hormonal changes, and uneven ripening of 'Concord' (Vitis labrusca L.) grapes. J Am Soc Hortic Sci 1982, 107(6):1097-1104.
31. Inaba A, Ishida M, Sobajima Y. Changes in endogenous hormone concentrations during berry development in relation to the ripening of Delaware grapes. J Jpn Soc Hortic Sci 1976, 45(3):245-252.
32. Zhang X, Luo G, Wang R, Wang J, Himelrick DG. Growth and developmental responses of seeded and seedless grape berries to shoot girdling. J Am Soc Hortic Sci 2003, 128(3):316-323.
33. Frenkel C. Involvement of peroxidase and indole-3-acetic acid oxidase isozymes from pear, tomato, and blueberry fruit in ripening. Plant Physiol 1972, 49(5):757-763. 10.1104/pp.49.5.757, 366047, 16658043.
34. Dunlap JR, Slovin JP, Cohen JD. Indole-3-acetic acid, ethylene, and abscisic acid metabolism in developing muskmelon (Cucumis melo L.) fruit. Plant Growth Regul 1996, 19(1):45-54.
35. Östin A, Kowalyczk M, Bhalerao RP, Sandberg G. Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol 1998, 118(1):285-296. 10.1104/pp.118.1.285, 34867, 9733548.
36. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 2005, 17(2):616-627. 10.1105/tpc.104.026690, 548830, 15659623.
37. Morgan PW, Hall WC. Effect of 2,4-dichlorophenoxyacetic acid on the production of ethylene by cotton and grain sorghum. Physiol Plant 1962, 15(3):420-427.
38. Yoshii H, Imaseki H. Regulation of auxin-induced ethylene biosynthesis. Repression of inductive formation of 1-aminocyclopropane-1-carboxylate synthase by ethylene. Plant Cell Physiol 1982, 23(4):639-649.
39. Abel S, Nguyen MD, Chow W, Theologis A. ASC4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana: Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. J Biol Chem 1995, 270(32):19093-19099. 10.1074/jbc.270.32.19093, 7642574.
40. Raghavan C, Ong EK, Dalling MJ, Stevenson TW. Regulation of genes associated with auxin, ethylene and ABA pathways by 2,4-dichlorophenoxyacetic acid in Arabidopsis. Funct Integr Genomics 2006, 6(1):60-70. 10.1007/s10142-005-0012-1, 16317577.
41. Tsuchisaka A, Theologis A. Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 2004, 136:2982-3000. 10.1104/pp.104.049999, 523360, 15466221.
42. Li J, Yuan R. NAA and ethylene regulate expression of genes related to ethylene biosynthesis, perception, and cell wall degradation during fruit abscission and ripening in 'Delicious' apples. J Plant Growth Regul 2008, 27(3):283-295.
43. Kondo S, Isuzugawa K, Kobayashi S, Mattheis J. Aroma volatile emission and expression of 1-aminocyclopropane-1-carboxylate (ACC) synthase and ACC oxidase genes in pears treated with 2,4-DP. Postharvest Biol Technol 2006, 41(1):22-31.
44. Trainotti L, Tadiello A, Casadoro G. The involvement of auxin in the ripening of climacteric fruits comes of age: The hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 2007, 58(12):3299-3308. 10.1093/jxb/erm178, 17925301.
45. Ziliotto F, Corso M, Rizzini FM, Rasori A, Botton A, Bonghi C. Grape berry ripening delay induced by a pre-véraison NAA treatment is paralleled by a shift in the expression pattern of auxin- and ethylene-related genes. BMC Plant Biol 2012, 12(1):185. 10.1186/1471-2229-12-185, 3564861, 23046684.
46. Agustí M, Gariglio N, Castillo A, Juan M, Almela V, Martínez-Fuentes A, Mesejo C. Effect of the synthetic auxin 2,4-DP on fruit development of loquat. Plant Growth Regul 2003, 41(2):129-132.
47. Agustí M, Juan M, Mesejo C, Martínez-Fuentes A, Almela V. Persimmon fruit size and climacteric encouraged by 3,5,6-trichloro-2-pyridyloxyacetic acid. J Hortic Sci Biotechnol 2004, 79(2):171-174.
48. Kondo S, Settsu K, Jitratham A. How application times of 2,4-DP influence the ripening capacity of 'La France' pears. HortScience 2004, 39(1):101-104.
49. Ohmiya A. Effects of auxin on growth and ripening of mesocarp discs of peach fruit. Sci Hortic 2000, 84(3-4):309-319.
50. Yuan R, Carbaugh DH. Effects of NAA, AVG, and 1-MCP on ethylene biosynthesis, preharvest fruit drop, fruit maturity, and quality of 'Golden Supreme' and 'Golden Delicious' apples. HortScience 2007, 42(1):101-105.
51. Růžička K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 2007, 19(7):2197-2212. 10.1105/tpc.107.052126, 1955700, 17630274.
52. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 2007, 19(7):2186-2196. 10.1105/tpc.107.052100, 1955695, 17630275.
53. Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM. A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 2005, 17(8):2230-2242. 10.1105/tpc.105.033365, 1182485, 15980261.
54. Zhong GY, Burns JK. Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol 2003, 53(6):117-131.
55. Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, et al. The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci 2011, 108(45):18512-18517. 10.1073/pnas.1108434108, 3215075, 22025724.
56. Stepanova AN, Yun J, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 2011, 23(11):3961-3973. 10.1105/tpc.111.088047, 3246335, 22108406.
57. Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci 2011, 108(45):18518-18523. 10.1073/pnas.1108436108, 3215067, 22025721.
58. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie D-Y, Doležal K, Schlereth A, Jürgens G, Alonso JM. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 2008, 133(1):177-191. 10.1016/j.cell.2008.01.047, 18394997.
59. Tao Y, Ferrer J-L, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 2008, 133(1):164-176. 10.1016/j.cell.2008.01.049, 2442466, 18394996.
60. Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 2001, 291(5502):306-309. 10.1126/science.291.5502.306, 11209081.
61. Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, Barazesh S, Cohen JD, Malcomber S, McSteen P. vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in Maize. Plant Cell 2011, 23(2):550-566. 10.1105/tpc.110.075267, 3077783, 21335375.
62. Muday GK, Rahman A, Binder BM. Auxin and ethylene: collaborators or competitors?. Trends Plant Sci 2012, 17(4):181-195. 10.1016/j.tplants.2012.02.001, 22406007.
63. Stepanova AN, Alonso JM. Ethylene signaling and response: where different regulatory modules meet. Curr Opin Plant Biol 2009, 12(5):548-555. 10.1016/j.pbi.2009.07.009, 19709924.
64. Peat TS, Böttcher C, Newman J, Lucent D, Cowieson N, Davies C. Crystal structure of an indole-3-acetic acid amido synthetase from grapevine involved in auxin homeostasis. Plant Cell 2012, 24(11):4525-4538. 10.1105/tpc.112.102921, 3531850, 23136372.
65. Binder BM, O'Malley RC, Wang W, Moore JM, Parks BM, Spalding EP, Bleecker AB. Arabidopsis seedling growth response and recovery to ethylene. A kinetic analysis. Plant Physiol 2004, 136(2):2913-2920. 10.1104/pp.104.050369, 523353, 15466220.
66. Ireland HS, Yao J-L, Tomes S, Sutherland PW, Nieuwenhuizen N, Gunaseelan K, Winz RA, David KM, Schaffer RJ. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant J 2013, 73(6):1044-1056. 10.1111/tpj.12094, 23236986.
67. Boller T, Herner RC, Kende H. Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid. Planta 1979, 145(3):293-303. 10.1007/BF00454455, 24317737.
68. Yamagami T, Tsuchisaka A, Yamada K, Haddon WF, Harden LA, Theologis A. Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J Biol Chem 2003, 278(49):49102-49112. 10.1074/jbc.M308297200, 12968022.
69. Adams DO, Yang SF. Ethylene biosynthesis: Identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad Sci 1979, 76(1):170-174. 10.1073/pnas.76.1.170, 382898, 16592605.
70. Capitani G, Hohenester E, Feng L, Storici P, Kirsch JF, Jansonius JN. Structure of 1-aminocyclopropane-1-carboxylate synthase, a key enzyme in the biosynthesis of the plant hormone ethylene. J Mol Biol 1999, 294(3):745-756. 10.1006/jmbi.1999.3255, 10610793.
71. Theologis A. One rotten apple spoils the whole bushel: The role of ethylene in fruit ripening. Cell 1992, 70(2):181-184. 10.1016/0092-8674(92)90093-R, 1638627.
72. Soeno K, Goda H, Ishii T, Ogura T, Tachikawa T, Sasaki E, Yoshida S, Fujioka S, Asami T, Shimada Y. Auxin biosynthesis inhibitors, identified by a genomics-based approach, provide insights into auxin biosynthesis. Plant Cell Physiol 2010, 51(4):524-536. 10.1093/pcp/pcq032, 20234049.
73. Liu H, Ying Y-Y, Zhang L, Gao Q-H, Li J, Zhang Z, Fang J-G, Duan K. Isolation and characterization of two YUCCA flavin monooxygenase genes from cultivated strawberry (Fragaria × ananassa Duch.). Plant Cell Rep 2012, 31(8):1425-1435. 10.1007/s00299-012-1258-4, 22491872.
74. Liu K, Kang B-C, Jiang H, Moore SL, Li H, Watkins CB, Setter TL, Jahn MM. A GH3-like gene, CcGH3, isolated from Capsicum chinense L. fruit is regulated by auxin and ethylene. Plant Mol Biol 2005, 58(4):447-464. 10.1007/s11103-005-6505-4, 16021332.
75. Chung M-Y, Vrebalov J, Alba R, Lee J, McQuinn R, Chung J-D, Klein P, Giovannoni J. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SIAP2a, is a negative regulator of fruit ripening. Plant J 2010, 64(6):936-947. 10.1111/j.1365-313X.2010.04384.x, 21143675.
76. Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, De Maagd RA. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 2011, 23(3):923-941. 10.1105/tpc.110.081273, 3082273, 21398570.
77. Bajguz A, Piotrowska A. Conjugates of auxin and cytokinin. Phytochemistry 2009, 70(8):957-969. 10.1016/j.phytochem.2009.05.006, 19524990.
78. Korasick DA, Enders TA, Strader LC. Auxin biosynthesis and storage forms. J Exp Bot 2013, 64(9):2541-2555. 10.1093/jxb/ert080, 23580748.
79. Chervin C, Terrier N, Ageorges A, Ribes F, Kuapunyakoon T. Influence of ethylene on sucrose accumulation in grape berry. Am J Enol Vitic 2006, 57(4):511-513.
80. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948. 10.1093/bioinformatics/btm404, 17846036.
81. Felsenstein J. PHYLIP: Phylogeny inference package (Version 3.2). Cladistics 1989, 5:164-166.
82. Davies C, Robinson SP. Sugar accumulation in grape berries - Cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol 1996, 111(1):275-283. 10.1104/pp.111.1.275, 157835, 8685267.
83. Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR. Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol 2006, 140(1):150-158. 1326039, 16361521.
84. Whelan JA, Russell NB, Whelan MA. A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 2003, 278(1-2):261-269.