Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics Analysis

Shoot branching is crucial for successful plant development and plant response to environmental factors. Extensive investigations have revealed the involvement of an intricate regulatory network including hormones and sugars. Recent studies have demonstrated that two major systemic regulators—auxin...

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Main Authors: Ming Wang, Laurent Ogé, Maria-Dolores Pérez Garcia, Alexandra Launay-Avon, Gilles Clément, Jose Le Gourrierec, Latifa Hamama, Soulaiman Sakr
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.830840/full
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author Ming Wang
Ming Wang
Laurent Ogé
Maria-Dolores Pérez Garcia
Alexandra Launay-Avon
Gilles Clément
Jose Le Gourrierec
Latifa Hamama
Soulaiman Sakr
author_facet Ming Wang
Ming Wang
Laurent Ogé
Maria-Dolores Pérez Garcia
Alexandra Launay-Avon
Gilles Clément
Jose Le Gourrierec
Latifa Hamama
Soulaiman Sakr
author_sort Ming Wang
collection DOAJ
description Shoot branching is crucial for successful plant development and plant response to environmental factors. Extensive investigations have revealed the involvement of an intricate regulatory network including hormones and sugars. Recent studies have demonstrated that two major systemic regulators—auxin and sugar—antagonistically regulate plant branching. However, little is known regarding the molecular mechanisms involved in this crosstalk. We carried out two complementary untargeted approaches—RNA-seq and metabolomics—on explant stem buds fed with different concentrations of auxin and sucrose resulting in dormant and non-dormant buds. Buds responded to the combined effect of auxin and sugar by massive reprogramming of the transcriptome and metabolome. The antagonistic effect of sucrose and auxin targeted several important physiological processes, including sink strength, the amino acid metabolism, the sulfate metabolism, ribosome biogenesis, the nucleic acid metabolism, and phytohormone signaling. Further experiments revealed a role of the TOR-kinase signaling pathway in bud outgrowth through at least downregulation of Rosa hybrida BRANCHED1 (RhBRC1). These new findings represent a cornerstone to further investigate the diverse molecular mechanisms that drive the integration of endogenous factors during shoot branching.
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spelling doaj.art-c767879c76214b849b2c8e69e5ee70472022-12-22T02:59:03ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-03-011310.3389/fpls.2022.830840830840Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics AnalysisMing Wang0Ming Wang1Laurent Ogé2Maria-Dolores Pérez Garcia3Alexandra Launay-Avon4Gilles Clément5Jose Le Gourrierec6Latifa Hamama7Soulaiman Sakr8Dryland-Technology Key Laboratory of Shandong Province, College of Agronomy, Qingdao Agricultural University, Qingdao, ChinaInstitut Agro, University of Angers INRAE, IRHS, SFR QUASAV, Angers, FranceInstitut Agro, University of Angers INRAE, IRHS, SFR QUASAV, Angers, FranceInstitut Agro, University of Angers INRAE, IRHS, SFR QUASAV, Angers, FranceInstitute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRA, Université Paris-Sud, Université d’Evry, Université Paris-Saclay, Gif-sur-Yvette, FranceInstitut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, Versailles, FranceInstitut Agro, University of Angers INRAE, IRHS, SFR QUASAV, Angers, FranceInstitut Agro, University of Angers INRAE, IRHS, SFR QUASAV, Angers, FranceInstitut Agro, University of Angers INRAE, IRHS, SFR QUASAV, Angers, FranceShoot branching is crucial for successful plant development and plant response to environmental factors. Extensive investigations have revealed the involvement of an intricate regulatory network including hormones and sugars. Recent studies have demonstrated that two major systemic regulators—auxin and sugar—antagonistically regulate plant branching. However, little is known regarding the molecular mechanisms involved in this crosstalk. We carried out two complementary untargeted approaches—RNA-seq and metabolomics—on explant stem buds fed with different concentrations of auxin and sucrose resulting in dormant and non-dormant buds. Buds responded to the combined effect of auxin and sugar by massive reprogramming of the transcriptome and metabolome. The antagonistic effect of sucrose and auxin targeted several important physiological processes, including sink strength, the amino acid metabolism, the sulfate metabolism, ribosome biogenesis, the nucleic acid metabolism, and phytohormone signaling. Further experiments revealed a role of the TOR-kinase signaling pathway in bud outgrowth through at least downregulation of Rosa hybrida BRANCHED1 (RhBRC1). These new findings represent a cornerstone to further investigate the diverse molecular mechanisms that drive the integration of endogenous factors during shoot branching.https://www.frontiersin.org/articles/10.3389/fpls.2022.830840/fullbud outgrowthsucroseauxinsignaling pathwayTOR-kinase
spellingShingle Ming Wang
Ming Wang
Laurent Ogé
Maria-Dolores Pérez Garcia
Alexandra Launay-Avon
Gilles Clément
Jose Le Gourrierec
Latifa Hamama
Soulaiman Sakr
Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics Analysis
Frontiers in Plant Science
bud outgrowth
sucrose
auxin
signaling pathway
TOR-kinase
title Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics Analysis
title_full Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics Analysis
title_fullStr Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics Analysis
title_full_unstemmed Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics Analysis
title_short Antagonistic Effect of Sucrose Availability and Auxin on Rosa Axillary Bud Metabolism and Signaling, Based on the Transcriptomics and Metabolomics Analysis
title_sort antagonistic effect of sucrose availability and auxin on rosa axillary bud metabolism and signaling based on the transcriptomics and metabolomics analysis
topic bud outgrowth
sucrose
auxin
signaling pathway
TOR-kinase
url https://www.frontiersin.org/articles/10.3389/fpls.2022.830840/full
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