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H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis

Acclimation to high temperature increases plants’ tolerance of subsequent lethal high temperatures. Although epigenetic regulation of plant gene expression is well studied, how plants maintain a memory of environmental changes over time remains unclear. Here, we show that JUMONJI (JMJ) proteins, dem...

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Autores principales: Yamaguchi, Nobutoshi, Matsubara, Satoshi, Yoshimizu, Kaori, Seki, Motohide, Hamada, Kouta, Kamitani, Mari, Kurita, Yuko, Nomura, Yasuyuki, Nagashima, Kota, Inagaki, Soichi, Suzuki, Takamasa, Gan, Eng-Seng, To, Taiko, Kakutani, Tetsuji, Nagano, Atsushi J., Satake, Akiko, Ito, Toshiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8190089/
https://www.ncbi.nlm.nih.gov/pubmed/34108473
http://dx.doi.org/10.1038/s41467-021-23766-w
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author Yamaguchi, Nobutoshi
Matsubara, Satoshi
Yoshimizu, Kaori
Seki, Motohide
Hamada, Kouta
Kamitani, Mari
Kurita, Yuko
Nomura, Yasuyuki
Nagashima, Kota
Inagaki, Soichi
Suzuki, Takamasa
Gan, Eng-Seng
To, Taiko
Kakutani, Tetsuji
Nagano, Atsushi J.
Satake, Akiko
Ito, Toshiro
author_facet Yamaguchi, Nobutoshi
Matsubara, Satoshi
Yoshimizu, Kaori
Seki, Motohide
Hamada, Kouta
Kamitani, Mari
Kurita, Yuko
Nomura, Yasuyuki
Nagashima, Kota
Inagaki, Soichi
Suzuki, Takamasa
Gan, Eng-Seng
To, Taiko
Kakutani, Tetsuji
Nagano, Atsushi J.
Satake, Akiko
Ito, Toshiro
author_sort Yamaguchi, Nobutoshi
collection PubMed
description Acclimation to high temperature increases plants’ tolerance of subsequent lethal high temperatures. Although epigenetic regulation of plant gene expression is well studied, how plants maintain a memory of environmental changes over time remains unclear. Here, we show that JUMONJI (JMJ) proteins, demethylases involved in histone H3 lysine 27 trimethylation (H3K27me3), are necessary for Arabidopsis thaliana heat acclimation. Acclimation induces sustained H3K27me3 demethylation at HEAT SHOCK PROTEIN22 (HSP22) and HSP17.6C loci by JMJs, poising the HSP genes for subsequent activation. Upon sensing heat after a 3-day interval, JMJs directly reactivate these HSP genes. Finally, jmj mutants fail to maintain heat memory under fluctuating field temperature conditions. Our findings of an epigenetic memory mechanism involving histone demethylases may have implications for environmental adaptation of field plants.
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spelling pubmed-81900892021-07-01 H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis Yamaguchi, Nobutoshi Matsubara, Satoshi Yoshimizu, Kaori Seki, Motohide Hamada, Kouta Kamitani, Mari Kurita, Yuko Nomura, Yasuyuki Nagashima, Kota Inagaki, Soichi Suzuki, Takamasa Gan, Eng-Seng To, Taiko Kakutani, Tetsuji Nagano, Atsushi J. Satake, Akiko Ito, Toshiro Nat Commun Article Acclimation to high temperature increases plants’ tolerance of subsequent lethal high temperatures. Although epigenetic regulation of plant gene expression is well studied, how plants maintain a memory of environmental changes over time remains unclear. Here, we show that JUMONJI (JMJ) proteins, demethylases involved in histone H3 lysine 27 trimethylation (H3K27me3), are necessary for Arabidopsis thaliana heat acclimation. Acclimation induces sustained H3K27me3 demethylation at HEAT SHOCK PROTEIN22 (HSP22) and HSP17.6C loci by JMJs, poising the HSP genes for subsequent activation. Upon sensing heat after a 3-day interval, JMJs directly reactivate these HSP genes. Finally, jmj mutants fail to maintain heat memory under fluctuating field temperature conditions. Our findings of an epigenetic memory mechanism involving histone demethylases may have implications for environmental adaptation of field plants. Nature Publishing Group UK 2021-06-09 /pmc/articles/PMC8190089/ /pubmed/34108473 http://dx.doi.org/10.1038/s41467-021-23766-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Yamaguchi, Nobutoshi
Matsubara, Satoshi
Yoshimizu, Kaori
Seki, Motohide
Hamada, Kouta
Kamitani, Mari
Kurita, Yuko
Nomura, Yasuyuki
Nagashima, Kota
Inagaki, Soichi
Suzuki, Takamasa
Gan, Eng-Seng
To, Taiko
Kakutani, Tetsuji
Nagano, Atsushi J.
Satake, Akiko
Ito, Toshiro
H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis
title H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis
title_full H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis
title_fullStr H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis
title_full_unstemmed H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis
title_short H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis
title_sort h3k27me3 demethylases alter hsp22 and hsp17.6c expression in response to recurring heat in arabidopsis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8190089/
https://www.ncbi.nlm.nih.gov/pubmed/34108473
http://dx.doi.org/10.1038/s41467-021-23766-w
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