Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B Monoubiquitination

Ubiquitylation is a form of post-translational modification of proteins that can alter localization, functionality, degradation, or transcriptional activity within a cell. E2 ubiquitin-conjugating enzyme (UBC) and E3 ubiquitin ligases are the primary determinants of substrate specificity in the cont...

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Main Authors: Kai Chen, Wen-Si Tang, Yong-Bin Zhou, Zhao-Shi Xu, Jun Chen, You-Zhi Ma, Ming Chen, Hai-Yan Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.555794/full
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author Kai Chen
Kai Chen
Wen-Si Tang
Yong-Bin Zhou
Zhao-Shi Xu
Jun Chen
You-Zhi Ma
Ming Chen
Hai-Yan Li
author_facet Kai Chen
Kai Chen
Wen-Si Tang
Yong-Bin Zhou
Zhao-Shi Xu
Jun Chen
You-Zhi Ma
Ming Chen
Hai-Yan Li
author_sort Kai Chen
collection DOAJ
description Ubiquitylation is a form of post-translational modification of proteins that can alter localization, functionality, degradation, or transcriptional activity within a cell. E2 ubiquitin-conjugating enzyme (UBC) and E3 ubiquitin ligases are the primary determinants of substrate specificity in the context of ubiquitin conjugation. Multiubiquitination modifies target proteins for 26S proteasome degradation, while monoubiquitination controls protein activation and localization. At present, research on the monoubiquitination, especially histone monoubiquitination, has mostly focused on model plants with relatively few on crop species. In this study, we identified 91 UBC-like genes in soybean. The chromosomal localization, phylogenetic relationships, gene structures, and putative cis-acting elements were evaluated. Furthermore, the tissue-specific expression patterns of UBC Class I genes under drought stress were also investigated. Among Class I genes, GmUBC9 induction in response to drought stress was evident, and so this gene was selected for further analysis. GmUBC9 localized to the nucleus and endoplasmic reticulum. The overexpression of GmUBC9 in Arabidopsis led to enhanced tolerance for drought conditions across a range of stages of development, while overexpression in soybean hairy roots similarly led to improvements in tolerance for drought conditions, increased proline content, and reduced MDA content in soybean seedlings compared to wild type plants. HISTONE MONOUBIQUITINATION 2 (HUB2), an E3-like protein involved in histone H2B ubiquitylation (H2Bub1), was found to interact with GmUBC9 through Y2H analysis and BiFC assays in Arabidopsis and soybean. Under drought conditions, the level of H2Bub1 increased, and transcription of drought response genes was activated in GmUBC9 transgenic Arabidopsis and soybean. In addition, GmUBC9 transgenic Arabidopsis and soybean showed a late-flowering phenotype and had increased expression levels of the flowering related genes FLC and MAF4. These findings indicate that GmUBC9 is important for drought stress response and regulation of flowering time in soybean.
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spelling doaj.art-78e605027aa447dfba3806743e8424522022-12-22T01:25:14ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-09-011110.3389/fpls.2020.555794555794Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B MonoubiquitinationKai Chen0Kai Chen1Wen-Si Tang2Yong-Bin Zhou3Zhao-Shi Xu4Jun Chen5You-Zhi Ma6Ming Chen7Hai-Yan Li8College of Life Sciences, Jilin Agricultural University, Changchun, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaCollege of Life Sciences, Jilin Agricultural University, Changchun, ChinaUbiquitylation is a form of post-translational modification of proteins that can alter localization, functionality, degradation, or transcriptional activity within a cell. E2 ubiquitin-conjugating enzyme (UBC) and E3 ubiquitin ligases are the primary determinants of substrate specificity in the context of ubiquitin conjugation. Multiubiquitination modifies target proteins for 26S proteasome degradation, while monoubiquitination controls protein activation and localization. At present, research on the monoubiquitination, especially histone monoubiquitination, has mostly focused on model plants with relatively few on crop species. In this study, we identified 91 UBC-like genes in soybean. The chromosomal localization, phylogenetic relationships, gene structures, and putative cis-acting elements were evaluated. Furthermore, the tissue-specific expression patterns of UBC Class I genes under drought stress were also investigated. Among Class I genes, GmUBC9 induction in response to drought stress was evident, and so this gene was selected for further analysis. GmUBC9 localized to the nucleus and endoplasmic reticulum. The overexpression of GmUBC9 in Arabidopsis led to enhanced tolerance for drought conditions across a range of stages of development, while overexpression in soybean hairy roots similarly led to improvements in tolerance for drought conditions, increased proline content, and reduced MDA content in soybean seedlings compared to wild type plants. HISTONE MONOUBIQUITINATION 2 (HUB2), an E3-like protein involved in histone H2B ubiquitylation (H2Bub1), was found to interact with GmUBC9 through Y2H analysis and BiFC assays in Arabidopsis and soybean. Under drought conditions, the level of H2Bub1 increased, and transcription of drought response genes was activated in GmUBC9 transgenic Arabidopsis and soybean. In addition, GmUBC9 transgenic Arabidopsis and soybean showed a late-flowering phenotype and had increased expression levels of the flowering related genes FLC and MAF4. These findings indicate that GmUBC9 is important for drought stress response and regulation of flowering time in soybean.https://www.frontiersin.org/article/10.3389/fpls.2020.555794/fullsoybeanubiquitin-conjugating enzymehistone monoubiquitinationdrought toleranceregulation of flowering
spellingShingle Kai Chen
Kai Chen
Wen-Si Tang
Yong-Bin Zhou
Zhao-Shi Xu
Jun Chen
You-Zhi Ma
Ming Chen
Hai-Yan Li
Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B Monoubiquitination
Frontiers in Plant Science
soybean
ubiquitin-conjugating enzyme
histone monoubiquitination
drought tolerance
regulation of flowering
title Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B Monoubiquitination
title_full Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B Monoubiquitination
title_fullStr Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B Monoubiquitination
title_full_unstemmed Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B Monoubiquitination
title_short Overexpression of GmUBC9 Gene Enhances Plant Drought Resistance and Affects Flowering Time via Histone H2B Monoubiquitination
title_sort overexpression of gmubc9 gene enhances plant drought resistance and affects flowering time via histone h2b monoubiquitination
topic soybean
ubiquitin-conjugating enzyme
histone monoubiquitination
drought tolerance
regulation of flowering
url https://www.frontiersin.org/article/10.3389/fpls.2020.555794/full
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