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      The Physiological and Molecular Mechanism of Abscisic Acid in Regulation of Fleshy Fruit Ripening

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          Abstract

          The ripening of fleshy fruits is coupled with the degradation of both chlorophyll and cell walls, as well as changes in the metabolism of phenylpropanoids, flavonoids, starch/sucrose, and carotenoids. These processes are controlled by phytohormones and other factors, including abscisic acid (ABA), ethylene, auxin, polyamines, sugar, and reactive oxygen species. The ripening of climacteric fruits is controlled by ethylene and non-climacteric fruit ripening is regulated mainly by ABA. Also, ABA and ethylene may interact in both types of fruit ripening. ABA concentrations in fleshy fruits are regulated in response to developmental and environmental cues and are controlled by the relative rates of ABA biosynthesis and catabolism, the former mainly via 9-cis-epoxycarotenoid dioxygenases (NCEDs) and β-glucosidases and the latter via ABA 8'-hydroxylases (CYP707As) and β-glycosyltransferases. In strawberry fruit ripening, ABA is perceived via at least two receptors, Pyrabactin resistance (PYR)/PYR-like (PYL) and putative abscisic acid receptor (ABAR), which are linked separately to the conserved signaling pathway ABA-FaPYR1-FaABIl-FaSnRK2 and the novel signaling pathway ABA-FaABAR-FaRIPK1-FaABI4. Downstream signaling components include important transcription factors, such as AREB (ABA responsive element binding protein)/ABF (ABRE binding factors ABA responsive factor), ethylene response factor (ERF), and V-myb Myeloblastosis viral oncogene homolog (MYB), as well as ripening-related genes. Finally, a comprehensive model of ABA linked to ethylene, sugar, polyamines, auxin and reactive oxygen species in the regulation of strawberry fruit ripening is proposed. Next, new integrated mechanisms, including two ABA signaling pathways, ABA and ethylene signaling pathways, and ABA/ethylene to other phytohormones are interesting and important research topics in ripening, especially in non-climacteric fruits.

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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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            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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              Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution

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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
                11 January 2021
                2020
                : 11
                : 619953
                Affiliations
                [1] 1College of Horticulture, China Agricultural University , Beijing, China
                [2] 2College of Plant Science and Technology, Beijing University of Agriculture , Beijing, China
                Author notes

                Edited by: Chunying Kang, Huazhong Agricultural University, China

                Reviewed by: Aide Wang, Shenyang Agricultural University, China; Guozheng Qin

                *Correspondence: Yuanyue Shen, sflmn@ 123456163.com

                This article was submitted to Plant Development and EvoDevo, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.619953
                7829184
                33505417
                7b392e5d-6c05-4fda-a48e-e94b0738333b
                Copyright © 2021 Bai, Huang and Shen.

                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
                : 21 October 2020
                : 09 December 2020
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 93, Pages: 9, Words: 8096
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 32030100
                Award ID: 31672125
                Funded by: Beijing Natural Science Foundation 10.13039/501100004826
                Award ID: 6171001
                Funded by: Scientific Research Project of Beijing Educational Committee
                Award ID: KM202110020006
                Funded by: Sichuan Lomon Biotechnology Co., LTD
                Award ID: 2018001
                Categories
                Plant Science
                Review

                Plant science & Botany
                fruit ripening,non-climacteric fruit,abscisic acid,ethylene,signaling transduction,review

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