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      Do Non-climacteric Fruits Share a Common Ripening Mechanism of Hormonal Regulation?

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          Abstract

          Fleshy fruits have been traditionally categorized into climacteric (CL) and non-climacteric (NC) groups. CL fruits share a common ripening mechanism of hormonal regulation, i.e., the ethylene regulation, whereas whether NC fruits share a common mechanism remains controversial. Abscisic acid (ABA) has been commonly thought to be a key regulator in NC fruit ripening; however, besides ABA, many other hormones have been increasingly suggested to play crucial roles in NC fruit ripening. NC fruits vary greatly in their organ origin, constitution, and structure. Development of different organs may be different in the pattern of hormonal regulation. It has been well demonstrated that the growth and development of strawberry, the model of NC fruits, is largely controlled by a hormonal communication between the achenes and receptacle; however, not all NC fruits contain achenes. Accordingly, it is particularly important to understand whether strawberry is indeed able to represent a universal mechanism for the hormonal regulation of NC fruit ripening. In this mini-review, we summarized the recent research advance on the hormone regulation of NC ripening in relation to fruit organ origination, constitution, and structure, whereby analyzing and discussing whether NC fruits may share a common mechanism of hormonal regulation.

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          Most cited references74

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          BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS.

          Jasmonic acid and its derivatives can modulate aspects of fruit ripening, production of viable pollen, root growth, tendril coiling, and plant resistance to insects and pathogens. Jasmonate activates genes involved in pathogen and insect resistance, and genes encoding vegetative storage proteins, but represses genes encoding proteins involved in photosynthesis. Jasmonic acid is derived from linolenic acid, and most of the enzymes in the biosynthetic pathway have been extensively characterized. Modulation of lipoxygenase and allene oxide synthase gene expression in transgenic plants raises new questions about the compartmentation of the biosynthetic pathway and its regulation. The activation of jasmonic acid biosynthesis by cell wall elicitors, the peptide systemin, and other compounds will be related to the function of jasmonates in plants. Jasmonate modulates gene expression at the level of translation, RNA processing, and transcription. Promoter elements that mediate responses to jasmonate have been isolated. This review covers recent advances in our understanding of how jasmonate biosynthesis is regulated and relates this information to knowledge of jasmonate modulated gene expression.
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            Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening.

            Elucidating the mechanisms involved in ripening of climacteric fruit and the role that ethylene plays in the process are key to understanding fruit production and quality. In this review, which is based largely on research in tomato, particular attention is paid to the role of specific isoforms of ACC synthase and ACC oxidase in controlling ethylene synthesis during the initiation and subsequent autocatalytic phase of ethylene production during ripening. Recent information on the structure and role of six different putative ethylene receptors in tomato is discussed, including evidence supporting the receptor inhibition model for ripening, possible differences in histidine kinase activity between receptors, and the importance of receptor LeETR4 in ripening. A number of ethylene-regulated ripening-related genes are discussed, including those involved in ethylene synthesis, fruit texture, and aroma volatile production, as well as experiments designed to elucidate the ethylene signalling pathway from receptor through intermediate components similar to those found in Arabidopsis, leading to transcription factors predicted to control the expression of ethylene-regulated genes.
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              Abscisic acid plays an important role in the regulation of strawberry fruit ripening.

              The plant hormone abscisic acid (ABA) has been suggested to play a role in fruit development, but supporting genetic evidence has been lacking. Here, we report that ABA promotes strawberry (Fragaria ananassa) fruit ripening. Using a newly established Tobacco rattle virus-induced gene silencing technique in strawberry fruit, the expression of a 9-cis-epoxycarotenoid dioxygenase gene (FaNCED1), which is key to ABA biosynthesis, was down-regulated, resulting in a significant decrease in ABA levels and uncolored fruits. Interestingly, a similar uncolored phenotype was observed in the transgenic RNA interference (RNAi) fruits, in which the expression of a putative ABA receptor gene encoding the magnesium chelatase H subunit (FaCHLH/ABAR) was down-regulated by virus-induced gene silencing. More importantly, the uncolored phenotype of the FaNCED1-down-regulated RNAi fruits could be rescued by exogenous ABA, but the ABA treatment could not reverse the uncolored phenotype of the FaCHLH/ABAR-down-regulated RNAi fruits. We observed that down-regulation of the FaCHLH/ABAR gene in the RNAi fruit altered both ABA levels and sugar content as well as a set of ABA- and/or sugar-responsive genes. Additionally, we showed that exogenous sugars, particularly sucrose, can significantly promote ripening while stimulating ABA accumulation. These data provide evidence that ABA is a signal molecule that promotes strawberry ripening and that the putative ABA receptor, FaCHLH/ABAR, is a positive regulator of ripening in response to ABA.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                09 June 2022
                2022
                : 13
                : 923484
                Affiliations
                [1] 1Institute of Horticulture Crops, Xinjiang Academy of Agricultural Sciences , Urumqi, China
                [2] 2College of Horticulture, China Agricultural University , Beijing, China
                Author notes

                Edited by: Jose A. Mercado, University of Malaga, Spain

                Reviewed by: Lida Fuentes-Viveros, Pontifical Catholic University of Valparaíso, Chile

                *Correspondence: Qing Hao, haoqingxj@ 123456sohu.com

                These authors have contributed equally to this work and share first authorship

                This article was submitted to Crop and Product Physiology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2022.923484
                9218805
                35755638
                7d58e9cd-2d62-42db-80ab-392f513491da
                Copyright © 2022 Fan, Wang, Hao and Jia.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 April 2022
                : 20 May 2022
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 74, Pages: 9, Words: 7396
                Funding
                Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;
                Award ID: 31872086
                Funded by: National Key Research and Development Program , doi 10.13039/501100012166;
                Award ID: 2019YFD1000204
                Funded by: the National Key Research and Development Program
                Award ID: 2019YFD1000803
                Funded by: Beijing Science and Technology Innovation and Service Capacity
                Award ID: CEFF-PXM2019_014207_000032
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                ripening mechanism,non-climacteric fruit,ripening,hormonal regulation,crosstalk

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