Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation

In Arabidopsis, brassinosteroids (BR) are major growth-promoting hormones, which integrate with the heterotrimeric guanine nucleotide-binding protein (G-protein) signals and cooperatively modulate cell division and elongation. However, the mechanisms of interaction between BR and G-protein are not w...

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Main Authors: Ting Zhang, Pengbo Xu, Wenxiu Wang, Sheng Wang, Julie C. Caruana, Hong-Quan Yang, Hongli Lian
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2017.02225/full
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author Ting Zhang
Pengbo Xu
Wenxiu Wang
Sheng Wang
Julie C. Caruana
Hong-Quan Yang
Hongli Lian
author_facet Ting Zhang
Pengbo Xu
Wenxiu Wang
Sheng Wang
Julie C. Caruana
Hong-Quan Yang
Hongli Lian
author_sort Ting Zhang
collection DOAJ
description In Arabidopsis, brassinosteroids (BR) are major growth-promoting hormones, which integrate with the heterotrimeric guanine nucleotide-binding protein (G-protein) signals and cooperatively modulate cell division and elongation. However, the mechanisms of interaction between BR and G-protein are not well understood. Here, we show that the G-protein β subunit AGB1 directly interacts with the BR transcription factor BES1 in vitro and in vivo. An AGB1-null mutant, agb1-2, displays BR hyposensitivity and brassinazole (BRZ, BR biosynthesis inhibitor) hypersensitivity, which suggests that AGB1 positively mediates the BR signaling pathway. Moreover, we demonstrate that AGB1 synergistically regulates expression of BES1 target genes, including the BR biosynthesis genes CPD and DWF4 and the SAUR family genes required for promoting cell elongation. Further, Western blot analysis of BES1 phosphorylation states indicates that the interaction between AGB1 and BES1 alters the phosphorylation status of BES1 and increases the ratio of dephosphorylated to phosphorylated BES1, which leads to accumulation of dephosphorylated BES1 in the nucleus. Finally, AGB1 promotes BES1 binding to BR target genes and stimulates the transcriptional activity of BES1. Taken together, our results demonstrate that AGB1 positively regulates cell elongation by affecting the phosphorylation status and transcriptional activity of BES1.
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spelling doaj.art-d90bfdd669a842f4956b6a90a4bbab9d2022-12-22T01:15:09ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-01-01810.3389/fpls.2017.02225325769Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell ElongationTing Zhang0Pengbo Xu1Wenxiu Wang2Sheng Wang3Julie C. Caruana4Hong-Quan Yang5Hongli Lian6School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaState Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, ChinaSchool of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD, United StatesState Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, ChinaKey Laboratory of Urban Agriculture (South), School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, ChinaIn Arabidopsis, brassinosteroids (BR) are major growth-promoting hormones, which integrate with the heterotrimeric guanine nucleotide-binding protein (G-protein) signals and cooperatively modulate cell division and elongation. However, the mechanisms of interaction between BR and G-protein are not well understood. Here, we show that the G-protein β subunit AGB1 directly interacts with the BR transcription factor BES1 in vitro and in vivo. An AGB1-null mutant, agb1-2, displays BR hyposensitivity and brassinazole (BRZ, BR biosynthesis inhibitor) hypersensitivity, which suggests that AGB1 positively mediates the BR signaling pathway. Moreover, we demonstrate that AGB1 synergistically regulates expression of BES1 target genes, including the BR biosynthesis genes CPD and DWF4 and the SAUR family genes required for promoting cell elongation. Further, Western blot analysis of BES1 phosphorylation states indicates that the interaction between AGB1 and BES1 alters the phosphorylation status of BES1 and increases the ratio of dephosphorylated to phosphorylated BES1, which leads to accumulation of dephosphorylated BES1 in the nucleus. Finally, AGB1 promotes BES1 binding to BR target genes and stimulates the transcriptional activity of BES1. Taken together, our results demonstrate that AGB1 positively regulates cell elongation by affecting the phosphorylation status and transcriptional activity of BES1.http://journal.frontiersin.org/article/10.3389/fpls.2017.02225/fullBR signaling pathwayG-protein signaling pathwayBES1AGB1protein interactionphosphorylation status
spellingShingle Ting Zhang
Pengbo Xu
Wenxiu Wang
Sheng Wang
Julie C. Caruana
Hong-Quan Yang
Hongli Lian
Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation
Frontiers in Plant Science
BR signaling pathway
G-protein signaling pathway
BES1
AGB1
protein interaction
phosphorylation status
title Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation
title_full Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation
title_fullStr Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation
title_full_unstemmed Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation
title_short Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation
title_sort arabidopsis g protein β subunit agb1 interacts with bes1 to regulate brassinosteroid signaling and cell elongation
topic BR signaling pathway
G-protein signaling pathway
BES1
AGB1
protein interaction
phosphorylation status
url http://journal.frontiersin.org/article/10.3389/fpls.2017.02225/full
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