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Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.)

BACKGROUND: Grape is highly sensitive to gibberellin (GA), which is crucial during seed and berry development (SBD) either by itself or by interacting with other hormones, such as auxin, Abscisic acid (ABA), and Cytokinin (CK). However, no systematic analysis of GA metabolic and signal transduction...

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Autores principales: Wang, Wenran, Bai, Yunhe, Koilkonda, Padmalatha, Guan, Le, Zhuge, Yaxian, Wang, Xicheng, Liu, Zhongjie, Jia, Haifeng, Wang, Chen, Fang, Jinggui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7441673/
https://www.ncbi.nlm.nih.gov/pubmed/32825825
http://dx.doi.org/10.1186/s12870-020-02591-1
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author Wang, Wenran
Bai, Yunhe
Koilkonda, Padmalatha
Guan, Le
Zhuge, Yaxian
Wang, Xicheng
Liu, Zhongjie
Jia, Haifeng
Wang, Chen
Fang, Jinggui
author_facet Wang, Wenran
Bai, Yunhe
Koilkonda, Padmalatha
Guan, Le
Zhuge, Yaxian
Wang, Xicheng
Liu, Zhongjie
Jia, Haifeng
Wang, Chen
Fang, Jinggui
author_sort Wang, Wenran
collection PubMed
description BACKGROUND: Grape is highly sensitive to gibberellin (GA), which is crucial during seed and berry development (SBD) either by itself or by interacting with other hormones, such as auxin, Abscisic acid (ABA), and Cytokinin (CK). However, no systematic analysis of GA metabolic and signal transduction (MST) pathway has been undertaken in grapevine. RESULTS: In this study, total endogenous GA(3) content significantly decreased during SBD, and a total of 48 known genes in GA metabolic (GAM; 31) and signal transduction (ST; 17) pathways were identified in this process. In the GAM pathway, out of 31 genes, VvGA20ox1–1, VvGA3ox4–1, and VvGA2ox1–1 may be the major factors interacting at the green-berry stage (GBS) accompanied with higher accumulation rate. GA biosynthesis was greater than GA inactivation at GBS, confirming the importance of seeds in GA synthesis. The visible correlation between endogenous GA(3) content and gene expression profiles suggested that the transcriptional regulation of GA biosynthesis pathway genes was a key mechanism of GA accumulation at the stone-hardening stage (SHS). Interestingly, we observed a negative feedback regulation between VvGA3oxs-VvGAI1–4, VvGA2oxs-VvGAI1–4, and VvGID1B-VvGAI1–4 in maintaining the balance of GA(3) content in berries. Moreover, 11 miRNAs may be involved in the modulation of GA MST pathway by mediating their target genes, such as VvGA3ox, VvGID1B, and VvGAMYB. Many genes in auxin, ABA, and CK MST pathways were further identified and found to have a special pattern in the berry, and the crosstalk between GA and these hormones may modulate the complex process during SBD through the interaction gene network of the multihormone pathway. Lastly, based on the expression characterization of multihormone MST pathway genes, a proposed model of the GA-mediated multihormone regulatory network during SBD was proposed. CONCLUSIONS: Our results provided novel insights into GA-mediated regulatory networks during SBD in grape. The complexity of GA-mediated multihormone ST in SBD was also elucidated, thereby providing valuable information for future functional characterizations of specific genes in grape.
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spelling pubmed-74416732020-08-24 Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.) Wang, Wenran Bai, Yunhe Koilkonda, Padmalatha Guan, Le Zhuge, Yaxian Wang, Xicheng Liu, Zhongjie Jia, Haifeng Wang, Chen Fang, Jinggui BMC Plant Biol Research Article BACKGROUND: Grape is highly sensitive to gibberellin (GA), which is crucial during seed and berry development (SBD) either by itself or by interacting with other hormones, such as auxin, Abscisic acid (ABA), and Cytokinin (CK). However, no systematic analysis of GA metabolic and signal transduction (MST) pathway has been undertaken in grapevine. RESULTS: In this study, total endogenous GA(3) content significantly decreased during SBD, and a total of 48 known genes in GA metabolic (GAM; 31) and signal transduction (ST; 17) pathways were identified in this process. In the GAM pathway, out of 31 genes, VvGA20ox1–1, VvGA3ox4–1, and VvGA2ox1–1 may be the major factors interacting at the green-berry stage (GBS) accompanied with higher accumulation rate. GA biosynthesis was greater than GA inactivation at GBS, confirming the importance of seeds in GA synthesis. The visible correlation between endogenous GA(3) content and gene expression profiles suggested that the transcriptional regulation of GA biosynthesis pathway genes was a key mechanism of GA accumulation at the stone-hardening stage (SHS). Interestingly, we observed a negative feedback regulation between VvGA3oxs-VvGAI1–4, VvGA2oxs-VvGAI1–4, and VvGID1B-VvGAI1–4 in maintaining the balance of GA(3) content in berries. Moreover, 11 miRNAs may be involved in the modulation of GA MST pathway by mediating their target genes, such as VvGA3ox, VvGID1B, and VvGAMYB. Many genes in auxin, ABA, and CK MST pathways were further identified and found to have a special pattern in the berry, and the crosstalk between GA and these hormones may modulate the complex process during SBD through the interaction gene network of the multihormone pathway. Lastly, based on the expression characterization of multihormone MST pathway genes, a proposed model of the GA-mediated multihormone regulatory network during SBD was proposed. CONCLUSIONS: Our results provided novel insights into GA-mediated regulatory networks during SBD in grape. The complexity of GA-mediated multihormone ST in SBD was also elucidated, thereby providing valuable information for future functional characterizations of specific genes in grape. BioMed Central 2020-08-21 /pmc/articles/PMC7441673/ /pubmed/32825825 http://dx.doi.org/10.1186/s12870-020-02591-1 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Wang, Wenran
Bai, Yunhe
Koilkonda, Padmalatha
Guan, Le
Zhuge, Yaxian
Wang, Xicheng
Liu, Zhongjie
Jia, Haifeng
Wang, Chen
Fang, Jinggui
Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.)
title Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.)
title_full Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.)
title_fullStr Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.)
title_full_unstemmed Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.)
title_short Genome-wide identification and characterization of gibberellin metabolic and signal transduction (GA MST) pathway mediating seed and berry development (SBD) in grape (Vitis vinifera L.)
title_sort genome-wide identification and characterization of gibberellin metabolic and signal transduction (ga mst) pathway mediating seed and berry development (sbd) in grape (vitis vinifera l.)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7441673/
https://www.ncbi.nlm.nih.gov/pubmed/32825825
http://dx.doi.org/10.1186/s12870-020-02591-1
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