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Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis

High levels of boron (B) induce DNA double-strand breaks (DSBs) in eukaryotes, including plants. Here we show a molecular pathway of high B-induced DSBs by characterizing Arabidopsis thaliana hypersensitive to excess boron mutants. Molecular analysis of the mutants revealed that degradation of a SWI...

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Autores principales: Sakamoto, Takuya, Tsujimoto-Inui, Yayoi, Sotta, Naoyuki, Hirakawa, Takeshi, Matsunaga, Tomoko M., Fukao, Yoichiro, Matsunaga, Sachihiro, Fujiwara, Toru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6290004/
https://www.ncbi.nlm.nih.gov/pubmed/30538237
http://dx.doi.org/10.1038/s41467-018-07393-6
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author Sakamoto, Takuya
Tsujimoto-Inui, Yayoi
Sotta, Naoyuki
Hirakawa, Takeshi
Matsunaga, Tomoko M.
Fukao, Yoichiro
Matsunaga, Sachihiro
Fujiwara, Toru
author_facet Sakamoto, Takuya
Tsujimoto-Inui, Yayoi
Sotta, Naoyuki
Hirakawa, Takeshi
Matsunaga, Tomoko M.
Fukao, Yoichiro
Matsunaga, Sachihiro
Fujiwara, Toru
author_sort Sakamoto, Takuya
collection PubMed
description High levels of boron (B) induce DNA double-strand breaks (DSBs) in eukaryotes, including plants. Here we show a molecular pathway of high B-induced DSBs by characterizing Arabidopsis thaliana hypersensitive to excess boron mutants. Molecular analysis of the mutants revealed that degradation of a SWItch/Sucrose Non-Fermentable subunit, BRAHMA (BRM), by a 26S proteasome (26SP) with specific subunits is a key process for ameliorating high-B-induced DSBs. We also found that high-B treatment induces histone hyperacetylation, which increases susceptibility to DSBs. BRM binds to acetylated histone residues and opens chromatin. Accordingly, we propose that the 26SP limits chromatin opening by BRM in conjunction with histone hyperacetylation to maintain chromatin stability and avoid DSB formation under high-B conditions. Interestingly, a positive correlation between the extent of histone acetylation and DSB formation is evident in human cultured cells, suggesting that the mechanism of DSB induction is also valid in animals.
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spelling pubmed-62900042018-12-13 Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis Sakamoto, Takuya Tsujimoto-Inui, Yayoi Sotta, Naoyuki Hirakawa, Takeshi Matsunaga, Tomoko M. Fukao, Yoichiro Matsunaga, Sachihiro Fujiwara, Toru Nat Commun Article High levels of boron (B) induce DNA double-strand breaks (DSBs) in eukaryotes, including plants. Here we show a molecular pathway of high B-induced DSBs by characterizing Arabidopsis thaliana hypersensitive to excess boron mutants. Molecular analysis of the mutants revealed that degradation of a SWItch/Sucrose Non-Fermentable subunit, BRAHMA (BRM), by a 26S proteasome (26SP) with specific subunits is a key process for ameliorating high-B-induced DSBs. We also found that high-B treatment induces histone hyperacetylation, which increases susceptibility to DSBs. BRM binds to acetylated histone residues and opens chromatin. Accordingly, we propose that the 26SP limits chromatin opening by BRM in conjunction with histone hyperacetylation to maintain chromatin stability and avoid DSB formation under high-B conditions. Interestingly, a positive correlation between the extent of histone acetylation and DSB formation is evident in human cultured cells, suggesting that the mechanism of DSB induction is also valid in animals. Nature Publishing Group UK 2018-12-11 /pmc/articles/PMC6290004/ /pubmed/30538237 http://dx.doi.org/10.1038/s41467-018-07393-6 Text en © The Author(s) 2018 Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Sakamoto, Takuya
Tsujimoto-Inui, Yayoi
Sotta, Naoyuki
Hirakawa, Takeshi
Matsunaga, Tomoko M.
Fukao, Yoichiro
Matsunaga, Sachihiro
Fujiwara, Toru
Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis
title Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis
title_full Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis
title_fullStr Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis
title_full_unstemmed Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis
title_short Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis
title_sort proteasomal degradation of brahma promotes boron tolerance in arabidopsis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6290004/
https://www.ncbi.nlm.nih.gov/pubmed/30538237
http://dx.doi.org/10.1038/s41467-018-07393-6
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