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

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          Abstract

          Background

          Tomato fruit ripening is controlled by ethylene and is characterized by a shift in color from green to red, a strong accumulation of lycopene, and a decrease in β-xanthophylls and chlorophylls. The role of other hormones, such as auxin, has been less studied. Auxin is retarding the fruit ripening. In tomato, there is no study of the carotenoid content and related transcript after treatment with auxin.

          Results

          We followed the effects of application of various hormone-like substances to “Mature-Green” fruits. Application of an ethylene precursor (ACC) or of an auxin antagonist (PCIB) to tomato fruits accelerated the color shift, the accumulation of lycopene, α-, β-, and δ-carotenes and the disappearance of β-xanthophylls and chlorophyll b. By contrast, application of auxin (IAA) delayed the color shift, the lycopene accumulation and the decrease of chlorophyll a. Combined application of IAA + ACC led to an intermediate phenotype. The levels of transcripts coding for carotenoid biosynthesis enzymes, for the ripening regulator Rin, for chlorophyllase, and the levels of ethylene and abscisic acid (ABA) were monitored in the treated fruits. Correlation network analyses suggest that ABA, may also be a key regulator of several responses to auxin and ethylene treatments.

          Conclusions

          The results suggest that IAA retards tomato ripening by affecting a set of (i) key regulators, such as Rin, ethylene and ABA, and (ii) key effectors, such as genes for lycopene and β-xanthophyll biosynthesis and for chlorophyll degradation.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12870-015-0495-4) contains supplementary material, which is available to authorized users.

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          Most cited references40

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          Integration of biological networks and gene expression data using Cytoscape.

          Cytoscape is a free software package for visualizing, modeling and analyzing molecular and genetic interaction networks. This protocol explains how to use Cytoscape to analyze the results of mRNA expression profiling, and other functional genomics and proteomics experiments, in the context of an interaction network obtained for genes of interest. Five major steps are described: (i) obtaining a gene or protein network, (ii) displaying the network using layout algorithms, (iii) integrating with gene expression and other functional attributes, (iv) identifying putative complexes and functional modules and (v) identifying enriched Gene Ontology annotations in the network. These steps provide a broad sample of the types of analyses performed by Cytoscape.
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            Carotenoid biosynthesis in flowering plants.

            The general scheme of carotenoid biosynthesis has been known for more than three decades. However, molecular description of the pathway in plants began only in the 1990s after the genes for the carotenogenic enzymes were cloned. Recent data on the biochemistry of carotenogenesis and its regulation in vivo present the possibility of genetically manipulating this pathway in crop plants.
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              The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit

              In order to understand more details about the role of abscisic acid (ABA) in fruit ripening and senescence of tomato, two cDNAs (LeNCED1 and LeNCED2) which encode 9-cis-epoxycarotenoid dioxygenase (NCED) as a key enzyme in ABA biosynthesis, two cDNAs (LeACS2 and LeACS4) which encode 1-aminocyclopropane-1-carboxylic acid (ACC) synthase, and one cDNA (LeACO1) which encodes ACC oxidase involved in ethylene biosynthesis were cloned from tomato fruit using a reverse transcription-PCR (RT-PCR) approach. The relationship between ABA and ethylene during ripening was also investigated. Among six sampling times in tomato fruits, the LeNCED1 gene was highly expressed only at the breaker stage when the ABA content becomes high. After this, the LeACS2, LeACS4, and LeACO1 genes were expressed with some delay. The change in pattern of ACO activity was in accordance with ethylene production reaching its peak at the pink stage. The maximum ABA content preceded ethylene production in both the seeds and the flesh. The peak value of ABA, ACC, and ACC oxidase activity, and ethylene production all started to increase earlier in seeds than in flesh tissues, although they occurred at different ripening stages. Exogenous ABA treatment increased the ABA content in both flesh and seed, inducing the expression of both ACS and ACO genes, and promoting ethylene synthesis and fruit ripening, while treatment with fluridone or nordihydroguaiaretic acid (NDGA) inhibited them, delaying fruit ripening and softening. Based on the results obtained in this study, it was concluded that LeNCED1 initiates ABA biosynthesis at the onset of fruit ripening, and might act as an original inducer, and ABA accumulation might play a key role in the regulation of ripeness and senescence of tomato fruit.
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                Author and article information

                Contributors
                suliyan029@126.com
                gianfranco.diretto@enea.it
                epurgatt@usp.br
                danoun@lrsv.ups-tlse.fr
                mohamed.zouine@ensat.fr
                zhengguoli@cqu.edu.cn
                roustan@ensat.fr
                bouzayen@ensat.fr
                Giovanni.Giuliano@enea.it
                chervin@ensat.fr
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                8 May 2015
                8 May 2015
                2015
                : 15
                : 114
                Affiliations
                [ ]Université de Toulouse, INP-ENSA Toulouse, UMR990 Génomique et Biotechnologie des Fruits, Avenue de l’Agrobiopole, CS 32607, F-31326 Castanet-Tolosan, France
                [ ]INRA, UMR990 Génomique et Biotechnologie des Fruits, 24 Chemin de Borde Rouge, CS 52627, F-31326 Castanet-Tolosan, France
                [ ]Italian National Agency for New Technologies, Energy, and Sustainable Development, Casaccia Research Centre, 00123 Rome, Italy
                [ ]Department Food and Experimental Nutrition; NAPAN/FoRC - Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, Av. Prof. Lineu Prestes 580, Butantã, CEP 05508-000 São Paulo, SP Brazil
                [ ]Université de Toulouse; UPS; UMR 5546; Laboratoire de Recherche en Sciences Végétales (LRSV), 24 Chemin de Borde Rouge, F-31326 Castanet-Tolosan, France
                [ ]Genetic Engineering Research Centre, Bioengineering College, Chongqing University, Chongqing, 400044 PR China
                [ ]Actual address: Department of Life Sciences, Xi’an University of Arts and Science, Xi’an, 710065 PR China
                Article
                495
                10.1186/s12870-015-0495-4
                4424491
                25953041
                733ba65c-f37f-4828-bfeb-a2441252fd22
                © Su et al.; licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 22 January 2015
                : 17 April 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Plant science & Botany
                auxin,ethylene,abscisic acid,tomato,carotenoids,chlorophyll,lycopene,rin,ripening
                Plant science & Botany
                auxin, ethylene, abscisic acid, tomato, carotenoids, chlorophyll, lycopene, rin, ripening

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