Carotenoid accumulation during tomato fruit ripening is modulated by the auxin-ethylene balance

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Su, Liyan ^a,g   Diretto, Gianfranco ^c   Purgatto, Eduardo ^d   Danoun, Saïda ^e   Zouine, Mohamed ^a,b   Li, Zhengguo ^f   Roustan, Jean Paul ^a,b   Bouzayen, Mondher ^a,b   Giuliano, Giovanni ^c   Chervin, Christian ^a,b  

^a GRENOBLE INSTITUTE OF TECHNOLOGY   (France)

^b Centre National de la Recherche Scientifique   (France)

^c ENEA C R CASACCIA   (Italy)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e UNIVERSITÉ DE TOULOUSE   (France)

^f CHONGQING UNIVERSITY   (China)

^g XI'AN UNIVERSITY OF ARTS AND SCIENCE   (China)

Author keywords

Abscisic acid; Auxin; Carotenoids; Chlorophyll; Ethylene; Lycopene; Rin; Ripening; Tomato

Indexed keywords

LYCOPERSICON ESCULENTUM;

ABSCISIC ACID; CARBOXYLESTERASE; CAROTENOID; CHLOROPHYLL; CHLOROPHYLLASE; ETHYLENE; ETHYLENE DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; MESSENGER RNA; PLANT PROTEIN;

BIOSYNTHESIS; DRUG EFFECTS; FRUIT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PIGMENTATION; TOMATO;

ABSCISIC ACID; BIOSYNTHETIC PATHWAYS; CARBOXYLIC ESTER HYDROLASES; CAROTENOIDS; CHLOROPHYLL; ETHYLENES; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; INDOLEACETIC ACIDS; LYCOPERSICON ESCULENTUM; PIGMENTATION; PLANT PROTEINS; RNA, MESSENGER;

EID: 85019238594     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0495-4     Document Type: Article

References (41)

1. Tromas A, Perrot-Rechenmann C. Recent progress in auxin biology. Comptes Rendus Biologies. 2010;333:297-306.
2. Giovannoni JJ. Fruit ripening mutants yield insights into ripening control. Current Opinion Plant Biology. 2007;10:283-9.
3. Cohen J. In vitro tomato fruit cultures demonstrate a role for indole-3-acetic acid in regulating fruit ripening. J Am Soc Hortic Sci. 1996;121:520-4.
4. Davies C, Boss P, Robinson S. Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol. 1997;115:1155-61.
5. Given N, Venis M, Grierson D. Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta. 1988;174:402-6.
6. Vendrell M. Dual effect of 2,4-D on ethylene production and ripening of tomato fruit tissue. Physiol Plant. 1985;64:559-63.
7. Muday GK, Rahman A, Binder BM. Auxin and ethylene: collaborators or competitors? Trends Plant Science. 2012;17:181-95.
8. Ecarnot M, Baczyk P, Tessarotto L, Chervin C. Rapid phenotyping of the tomato fruit model, Micro-Tom, with a portable VIS-NIR spectrometer. Plant Physiol Biochem. 2013;70:159-63.
9. Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM. Carotenoid biosynthesis during tomato fruit development evidence for tissue-specific gene expression. Plant Physiol. 1994;105:405-13.
10. Egea I, Bian W, Barsan C, Jauneau A, Pech JC, Latche A, et al. Chloroplast-to-chromoplast transition in tomato fruit: spectral confocal microscopy analyses of carotenoids and chlorophylls in isolated plastids and time-lapse recording on intact live tissue. Ann Bot. 2011;108:291-7.
11. Hirschberg J. Carotenoid biosynthesis in flowering plants. Current Opinion Plant Biology. 2001;4:210-8.
12. Giuliano G. Plant carotenoids: genomics meets multi-gene engineering. Current Opinion Plant Biology. 2014;19:111-7.
13. Ji K, Kai W, Zhao B, Sun Y, Yuan B, Dai S, et al. SlNCED1 and SlCYP707A2: key genes involved in ABA metabolism during tomato fruit ripening. J Exp Bot. 2014;65:5243-55.
14. Giuliano G, Bartley GE, Scolnik PA. Regulation of carotenoid biosynthesis during tomato development. The Plant Cell. 1993;5:379-87.
15. Fantini E, Falcone G, Frusciante S, Giliberto L, Giuliano G. Dissection of tomato lycopene biosynthesis through virus-induced gene silencing. Plant Physiol. 2013;163:986-98.
16. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol. 2011;157:1568-79.
17. Fujisawa M, Nakano T, Shima Y, Ito Y. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. The Plant Cell. 2013;25:371-86.
18. Ronen G, Cohen M, Zamir D, Hirschberg J. Regulation of caroteniod biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. The Plant Journal. 1999;17:341-51.
19. Ronen G, Carmel-Goren L, Zamir D, Hirschberg J. An alternative pathway to beta -carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. ProcNatlAcadSci U S A. 2000;97:11102-7.
20. Rosati C, Aquilani R, Dharmapuri S, Pallara P, Marusic C, Tavazza R, et al. Metabolic engineering of beta-carotene and lycopene content in tomato fruit. The Plant Journal. 2000;24:413-9.
21. Ma C, Ma B, He J, Hao Q, Lu X, Wang L. Regulation of carotenoid content in tomato by silencing of lycopene β/ε-cyclase genes. Plant Mol Biol Report. 2011;29:117-24.
22. Oono Y, Ooura C, Rahman A, Aspuria ET, Hayashi K, Tanaka A, et al. p-Chlorophenoxyisobutyric acid impairs auxin response in Arabidopsis root. Plant Physiol. 2003;133:1135-47.
23. Liotenberg S, North H, Marion-Poll A. Molecular biology and regulation of abscisic acid biosynthesis in plants. Plant Physiol Biochem. 1999;37:341-50.
24. Taylor IB, Burbidge A, Thompson AJ. Control of abscisic acid synthesis. J Exp Bot. 2000;51:1563-74.
25. Zhang M, Yuan B, Leng P. The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot. 2009;60:1579-88.
26. Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J. Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. The Plant Journal. 2008;53:717-30.
27. Saltveit ME. Effect of ethylene on quality of fresh fruits and vegetables. Postharvest Biology and Technology. 1999;15:279-92.
28. Frenkel C, Garrison SA. Initiation of lycopene synthesis in the tomato mutant rin as influenced by oxygen and ethylene interactions. HortSci. 1976;11:20-1.
29. Jacob-Wilk D, Holland D, Goldschmidt EE, Riov J, Eyal Y. Chlorophyll breakdown by chlorophyllase: isolation and functional expression of the Chlase1 gene from ethylene-treated Citrus fruit and its regulation during development. The Plant Journal. 1999;20:653-61.
30. Harpaz-Saad S, Azoulay T, Arazi T, Ben-Yaakov E, Mett A, Shiboleth YM, et al. Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. The Plant Cell. 2007;19:1007-22.
31. Diretto G, Al-Babili S, Tavazza R, Scossa F, Papacchioli V, Migliore M, et al. Transcriptional-metabolic networks in β-carotene-enriched potato tubers: the long and winding road to the golden phenotype. Plant Physiol. 2010;154:899-912.
32. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc. 2007;2:2366-82.
33. Neuman H, Galpaz N, Cunningham Jr FX, Zamir D, Hirschberg J. The tomato mutation nxd1 reveals a gene necessary for neoxanthin biosynthesis and demonstrates that violaxanthin is a sufficient precursor for abscisic acid biosynthesis. The Plant Journal. 2014;78:80-93.
34. Pirrello J, Jaimes-Miranda F, Sanchez-Ballesta MT, Tournier B, Khalil-Ahmad Q, Regad F, et al. Sl-ERF2, a tomato ethylene response factor involved in ethylene response and seed germination. Plant Cell Physiol. 2006;47:1195-205.
35. Orzaez D, Mirabel S, Wieland WH, Granell A. Agroinjection of tomato fruits. A tool for rapid functional analysis of transgenes directly in fruit. Plant Physiol. 2006;140:3-11.
36. Liu M, Diretto G, Pirrello J, Roustan JP, Li Z, Giuliano G, et al. The chimeric repressor version of an Ethylene Response Factor (ERF) family member, Sl-ERF.B3, shows contrasting effects on tomato fruit ripening. New Phytol. 2014;203:206-18.
37. Forcat S, Bennett MH, Mansfield JW, Grant MR. A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods. 2008;4:16.
38. Jaulneau V, Lafitte C, Jacquet C, Fournier S, Salamagne S, Briand X, et al. Ulvan, a sulfated polysaccharide from green algae, activates plant immunity through the jasmonic acid signaling pathway. J Biomed Biotechnol. 2010;2010:525291.
39. Chervin C, Deluc L. Ethylene signalling receptors and transcription factors over the grape berry development: gene expression profiling. Vitis. 2010;49:129-36.
40. Vaillé J. La Statistique au service des Données: quelques macros Excel pour faire de l'analyse exploratoire des données. 2010, Modulad n°43, http://www.modulad.fr/index.htm
41. Bramley PM. Regulation of carotenoid formation during tomato fruit ripening and development. J Exp Bot. 2002;53:2107-13.