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      Regulation of fleshy fruit ripening: from transcription factors to epigenetic modifications

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          Abstract

          Fleshy fruits undergo a complex ripening process, developing organoleptic fruit traits that attract herbivores and maximize seed dispersal. Ripening is the terminal stage of fruit development and involves a series of physiological and biochemical changes. In fleshy fruits, ripening always involves a drastic color change triggered by the accumulation of pigments and degradation of chlorophyll, softening caused by cell wall remodeling, and flavor formation as acids and sugars accumulate alongside volatile compounds. The mechanisms underlying fruit ripening rely on the orchestration of ripening-related transcription factors, plant hormones, and epigenetic modifications. In this review, we discuss current knowledge of the transcription factors that regulate ripening in conjunction with ethylene and environmental signals (light and temperature) in the model plant tomato ( Solanum lycopersicum) and other fleshy fruits. We emphasize the critical roles of epigenetic regulation, including DNA methylation and histone modification as well as RNA m 6 A modification, which has been studied intensively. This detailed review was compiled to provide a comprehensive description of the regulatory mechanisms of fruit ripening and guide new strategies for its effective manipulation.

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          Most cited references131

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          A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening.

          A major component in the regulatory network controlling fruit ripening is likely to be the gene at the tomato Colorless non-ripening (Cnr) locus. The Cnr mutation results in colorless fruits with a substantial loss of cell-to-cell adhesion. The nature of the mutation and the identity of the Cnr gene were previously unknown. Using positional cloning and virus-induced gene silencing, here we demonstrate that an SBP-box (SQUAMOSA promoter binding protein-like) gene resides at the Cnr locus. Furthermore, the Cnr phenotype results from a spontaneous epigenetic change in the SBP-box promoter. The discovery that Cnr is an epimutation was unexpected, as very few spontaneous epimutations have been described in plants. This study demonstrates that an SBP-box gene is critical for normal ripening and highlights the likely importance of epialleles in plant development and the generation of natural variation.
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            A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus.

            Tomato plants harboring the ripening-inhibitor (rin) mutation yield fruits that fail to ripen. Additionally, rin plants display enlarged sepals and loss of inflorescence determinacy. Positional cloning of the rin locus revealed two tandem MADS-box genes (LeMADS-RIN and LeMADS-MC), whose expression patterns suggested roles in fruit ripening and sepal development, respectively. The rin mutation alters expression of both genes. Gene repression and mutant complementation demonstrate that LeMADS-RIN regulates ripening, whereas LeMADS-MC affects sepal development and inflorescence determinacy. LeMADS-RIN demonstrates an agriculturally important function of plant MADS-box genes and provides molecular insight into nonhormonal (developmental) regulation of ripening.
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              Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening.

              Ripening of tomato fruits is triggered by the plant hormone ethylene, but its effect is restricted by an unknown developmental cue to mature fruits containing viable seeds. To determine whether this cue involves epigenetic remodeling, we expose tomatoes to the methyltransferase inhibitor 5-azacytidine and find that they ripen prematurely. We performed whole-genome bisulfite sequencing on fruit in four stages of development, from immature to ripe. We identified 52,095 differentially methylated regions (representing 1% of the genome) in the 90% of the genome covered by our analysis. Furthermore, binding sites for RIN, one of the main ripening transcription factors, are frequently localized in the demethylated regions of the promoters of numerous ripening genes, and binding occurs in concert with demethylation. Our data show that the epigenome is not static during development and may have been selected to ensure the fidelity of developmental processes such as ripening. Crop-improvement strategies could benefit by taking into account not only DNA sequence variation among plant lines, but also the information encoded in the epigenome.
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                Author and article information

                Journal
                Hortic Res
                Hortic Res
                hr
                Horticulture Research
                Oxford University Press
                2662-6810
                2052-7276
                2022
                11 February 2022
                11 February 2022
                : 9
                : uhac013
                Affiliations
                [1 ]National Key Laboratory of Crop Biology, Shandong Collaborative Innovation Center of Fruit & Vegetable Quality and Efficient Production, College of Horticulture Science and Engineering, Shandong Agricultural University , Tai-An, Shandong 271018, China
                [2 ]Shandong Provincial Key Laboratory of Plant Stress, College of Life Sciences, Shandong Normal University , Jinan 250014, China
                [3 ]State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University , Tai-An, 271018, China
                Author notes

                Equal contribution.

                Article
                uhac013
                10.1093/hr/uhac013
                9035223
                35147185
                a69f7a26-31ef-43bc-b50b-e54f3ccba94d
                © The Author(s) 2022. Published by Oxford University Press on behalf of Nanjing Agricultural University

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 6 September 2021
                : 1 December 2021
                : 16 April 2022
                Page count
                Pages: 12
                Categories
                Review Article

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