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      ABA mediates development-dependent anthocyanin biosynthesis and fruit coloration in Lycium plants

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          Abstract

          Background

          Anthocyanins, which are colored pigments, have long been used as food and pharmaceutical ingredients due to their potential health benefits, but the intermediate signals through which environmental or developmental cues regulate anthocyanin biosynthesis remains poorly understood. Fleshy fruits have become a good system for studying the regulation of anthocyanin biosynthesis, and exploring the mechanism underlying pigment metabolism is valuable for controlling fruit ripening.

          Results

          The present study revealed that ABA accumulated during Lycium fruit ripening, and this accumulation was positively correlated with the anthocyanin contents and the LbNCED1 transcript levels. The application of exogenous ABA and of the ABA biosynthesis inhibitor fluridon increased and decreased the content of anthocyanins in Lycium fruit, respectively. This is the first report to show that ABA promotes the accumulation of anthocyanins in Lycium fruits. The variations in the anthocyanin content were consistent with the variations in the expression of the genes encoding the MYB-bHLH-WD40 transcription factor complex or anthocyanin biosynthesis-related enzymes. Virus-induced LbNCED1 gene silencing significantly slowed fruit coloration and decreased both anthocyanin and ABA accumulation during Lycium fruit ripening. An qRT-PCR analysis showed that LbNCED1 gene silencing clearly reduced the transcript levels of both structural and regulatory genes in the flavonoid biosynthetic pathway.

          Conclusions

          Based on the results, a model of ABA-mediated development-dependent anthocyanin biosynthesis and fruit coloration during Lycium fruit maturation was proposed. In this model, the developmental cues transcriptionally activates LbNCED1 and thus enhances accumulation of the phytohormone ABA, and the accumulated ABA stimulates transcription of the MYB-bHLH-WD40 transcription factor complex to upregulate the expression of structural genes in the flavonoid biosynthetic pathway and thereby promoting anthocyanin production and fruit coloration. Our results provide a valuable strategy that could be used in practice to regulate the ripening and quality of fresh fruit in medicinal and edible plants by modifying the phytohormone ABA.

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          Most cited references36

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          Abscisic Acid synthesis and response.

          Abscisic acid (ABA) is one of the "classical" plant hormones, i.e. discovered at least 50 years ago, that regulates many aspects of plant growth and development. This chapter reviews our current understanding of ABA synthesis, metabolism, transport, and signal transduction, emphasizing knowledge gained from studies of Arabidopsis. A combination of genetic, molecular and biochemical studies has identified nearly all of the enzymes involved in ABA metabolism, almost 200 loci regulating ABA response, and thousands of genes regulated by ABA in various contexts. Some of these regulators are implicated in cross-talk with other developmental, environmental or hormonal signals. Specific details of the ABA signaling mechanisms vary among tissues or developmental stages; these are discussed in the context of ABA effects on seed maturation, germination, seedling growth, vegetative stress responses, stomatal regulation, pathogen response, flowering, and senescence.
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            Recent advances on the regulation of anthocyanin synthesis in reproductive organs.

            Anthocyanins represent the major red, purple, violet and blue pigments in many flowers and fruits. They attract pollinators and seed dispersers and defend plants against abiotic and biotic stresses. Anthocyanins are produced by a specific branch of the flavonoid pathway, which is differently regulated in monocot and dicot species. In the monocot maize, the anthocyanin biosynthesis genes are activated as a single unit by a ternary complex of MYB-bHLH-WD40 transcription factors (MBW complex). In the dicot Arabidopsis, anthocyanin biosynthesis genes can be divided in two subgroups: early biosynthesis genes (EBGs) are activated by co-activator independent R2R3-MYB transcription factors, whereas late biosynthesis genes (LBGs) require an MBW complex. In addition to this, a complex regulatory network of positive and negative feedback mechanisms controlling anthocyanin synthesis in Arabidopsis has been described. Recent studies have broadened our understanding of the regulation of anthocyanin synthesis in flowers and fruits, indicating that a regulatory system based on the cooperation of MYB, bHLH and WD40 proteins that control floral and fruit pigmentation is common to many dicot species. Copyright © 2011 Elsevier Ireland Ltd. All rights reserved.
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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
                1009851581@qq.com
                zhaojianhua0943@163.com
                1445033393@qq.com
                yueyin0112@aliyun.com
                gouqi2000@163.com
                muzx@nwsuaf.edu.cn
                youlongchk@163.com
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                15 July 2019
                15 July 2019
                2019
                : 19
                : 317
                Affiliations
                [1 ]GRID grid.469610.c, National Wolfberry Engineering Research Center, , Ningxia Academy of Agriculture and Forestry Sciences, ; Yinchuan, 750002 China
                [2 ]ISNI 0000 0004 1760 4150, GRID grid.144022.1, College of Life Sciences, , Northwest A&F University, ; Yangling, 712100 Shaanxi China
                Article
                1931
                10.1186/s12870-019-1931-7
                6631627
                31307384
                b920ff03-6346-45ca-8165-a549f353ef10
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
                : 18 April 2019
                : 9 July 2019
                Funding
                Funded by: the National High-tech R&D Program
                Award ID: 2013AA102606-04
                Award Recipient :
                Funded by: National Natural Science Foundation of China
                Award ID: 31660220
                Award Recipient :
                Funded by: the Project of Agricultural Breeding of New Wolfberry Varieties in Ningxia
                Award ID: 2013NYYZ0101
                Award Recipient :
                Funded by: the Self-option and Foundation of Ningxia Academy of Agriculture and Forestry Sciences
                Award ID: NKYJ-18-16
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Plant science & Botany
                lycium,fruit ripening,anthocyanins,aba,vigs
                Plant science & Botany
                lycium, fruit ripening, anthocyanins, aba, vigs

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