A new role for histone demethylases in the maintenance of plant genome integrity

Javier Antunez-Sanchez; Matthew Naish; Juan Sebastian Ramirez-Prado; Sho Ohno; Ying Huang; Alexander Dawson; Korawit Opassathian; Deborah Manza-Mianza; Federico Ariel; Cecile Raynaud; Anjar Wibowo; Josquin Daron; Minako Ueda; David Latrasse; R. Keith Slotkin; Detlef Weigel; Moussa Benhamed; Jose Gutierrez-Marcos

doi:10.7554/eLife.58533

A new role for histone demethylases in the maintenance of plant genome integrity

Javier Antunez-Sanchez
, Matthew Naish
, Juan Sebastian Ramirez-Prado
, Sho Ohno
, Ying Huang
, Alexander Dawson
, Korawit Opassathian
, Deborah Manza-Mianza
, Federico Ariel
, Cecile Raynaud
, Anjar Wibowo
, Josquin Daron
, Minako Ueda
, David Latrasse
, R. Keith Slotkin
, Detlef Weigel
, Moussa Benhamed
, Jose Gutierrez-Marcos

Warwick University
University of Cambridge
Université d'Evry-Val d'Essone
University of Leuven
Center for Plant Systems Biology
Graduate School of Agriculture
Dept. 3 (Genetics)
Universitas Airlangga
The Ohio State University
University of Montpellier
Nagoya University
Donald Danforth Plant Science Center
University of Missouri
Universite Paris Cite

Research output: Contribution to journal › Article › peer-review

52 Citations (Scopus)

Abstract

Histone modifications deposited by the Polycomb repressive complex 2 (PRC2) play a critical role in the control of growth, development, and adaptation to environmental fluctuations of most multicellular eukaryotes. The catalytic activity of PRC2 is counteracted by Jumonji-type (JMJ) histone demethylases, which shapes the genomic distribution of H3K27me3. Here, we show that two JMJ histone demethylases in Arabidopsis, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6), play distinct roles in H3K27me3 and H3K27me1 homeostasis. We show that failure to reset these chromatin marks during sexual reproduction results in the transgenerational inheritance of histone marks, which cause a loss of DNA methylation at heterochromatic loci and transposon activation. Thus, Jumonji-type histone demethylases play a dual role in plants by helping to maintain transcriptional states through development and safeguard genome integrity during sexual reproduction.

Original language	English
Article number	e58533
Pages (from-to)	1-32
Number of pages	32
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.58533
Publication status	Published - Oct 2020
Externally published	Yes

Keywords

Arabidopsis
Chromatin
DNA methylation
Epimutation
Transposon

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10.7554/eLife.58533

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Antunez-Sanchez, J., Naish, M., Ramirez-Prado, J. S., Ohno, S., Huang, Y., Dawson, A., Opassathian, K., Manza-Mianza, D., Ariel, F., Raynaud, C., Wibowo, A., Daron, J., Ueda, M., Latrasse, D., Slotkin, R. K., Weigel, D., Benhamed, M., & Gutierrez-Marcos, J. (2020). A new role for histone demethylases in the maintenance of plant genome integrity. eLife, 9, 1-32. Article e58533. https://doi.org/10.7554/eLife.58533

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title = "A new role for histone demethylases in the maintenance of plant genome integrity",

abstract = "Histone modifications deposited by the Polycomb repressive complex 2 (PRC2) play a critical role in the control of growth, development, and adaptation to environmental fluctuations of most multicellular eukaryotes. The catalytic activity of PRC2 is counteracted by Jumonji-type (JMJ) histone demethylases, which shapes the genomic distribution of H3K27me3. Here, we show that two JMJ histone demethylases in Arabidopsis, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6), play distinct roles in H3K27me3 and H3K27me1 homeostasis. We show that failure to reset these chromatin marks during sexual reproduction results in the transgenerational inheritance of histone marks, which cause a loss of DNA methylation at heterochromatic loci and transposon activation. Thus, Jumonji-type histone demethylases play a dual role in plants by helping to maintain transcriptional states through development and safeguard genome integrity during sexual reproduction.",

keywords = "Arabidopsis, Chromatin, DNA methylation, Epimutation, Transposon",

author = "Javier Antunez-Sanchez and Matthew Naish and Ramirez-Prado, \{Juan Sebastian\} and Sho Ohno and Ying Huang and Alexander Dawson and Korawit Opassathian and Deborah Manza-Mianza and Federico Ariel and Cecile Raynaud and Anjar Wibowo and Josquin Daron and Minako Ueda and David Latrasse and Slotkin, \{R. Keith\} and Detlef Weigel and Moussa Benhamed and Jose Gutierrez-Marcos",

year = "2020",

month = oct,

doi = "10.7554/eLife.58533",

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Antunez-Sanchez, J, Naish, M, Ramirez-Prado, JS, Ohno, S, Huang, Y, Dawson, A, Opassathian, K, Manza-Mianza, D, Ariel, F, Raynaud, C, Wibowo, A, Daron, J, Ueda, M, Latrasse, D, Slotkin, RK, Weigel, D, Benhamed, M & Gutierrez-Marcos, J 2020, 'A new role for histone demethylases in the maintenance of plant genome integrity', eLife, vol. 9, e58533, pp. 1-32. https://doi.org/10.7554/eLife.58533

TY - JOUR

T1 - A new role for histone demethylases in the maintenance of plant genome integrity

AU - Antunez-Sanchez, Javier

AU - Naish, Matthew

AU - Ramirez-Prado, Juan Sebastian

AU - Ohno, Sho

AU - Huang, Ying

AU - Dawson, Alexander

AU - Opassathian, Korawit

AU - Manza-Mianza, Deborah

AU - Ariel, Federico

AU - Raynaud, Cecile

AU - Wibowo, Anjar

AU - Daron, Josquin

AU - Ueda, Minako

AU - Latrasse, David

AU - Slotkin, R. Keith

AU - Weigel, Detlef

AU - Benhamed, Moussa

AU - Gutierrez-Marcos, Jose

PY - 2020/10

Y1 - 2020/10

N2 - Histone modifications deposited by the Polycomb repressive complex 2 (PRC2) play a critical role in the control of growth, development, and adaptation to environmental fluctuations of most multicellular eukaryotes. The catalytic activity of PRC2 is counteracted by Jumonji-type (JMJ) histone demethylases, which shapes the genomic distribution of H3K27me3. Here, we show that two JMJ histone demethylases in Arabidopsis, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6), play distinct roles in H3K27me3 and H3K27me1 homeostasis. We show that failure to reset these chromatin marks during sexual reproduction results in the transgenerational inheritance of histone marks, which cause a loss of DNA methylation at heterochromatic loci and transposon activation. Thus, Jumonji-type histone demethylases play a dual role in plants by helping to maintain transcriptional states through development and safeguard genome integrity during sexual reproduction.

AB - Histone modifications deposited by the Polycomb repressive complex 2 (PRC2) play a critical role in the control of growth, development, and adaptation to environmental fluctuations of most multicellular eukaryotes. The catalytic activity of PRC2 is counteracted by Jumonji-type (JMJ) histone demethylases, which shapes the genomic distribution of H3K27me3. Here, we show that two JMJ histone demethylases in Arabidopsis, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6), play distinct roles in H3K27me3 and H3K27me1 homeostasis. We show that failure to reset these chromatin marks during sexual reproduction results in the transgenerational inheritance of histone marks, which cause a loss of DNA methylation at heterochromatic loci and transposon activation. Thus, Jumonji-type histone demethylases play a dual role in plants by helping to maintain transcriptional states through development and safeguard genome integrity during sexual reproduction.

KW - Arabidopsis

KW - Chromatin

KW - DNA methylation

KW - Epimutation

KW - Transposon

UR - https://www.scopus.com/pages/publications/85096357188

U2 - 10.7554/eLife.58533

DO - 10.7554/eLife.58533

M3 - Article

C2 - 33107825

AN - SCOPUS:85096357188

SN - 2050-084X

VL - 9

SP - 1

EP - 32

JO - eLife

JF - eLife

M1 - e58533

ER -

A new role for histone demethylases in the maintenance of plant genome integrity

Abstract

Keywords

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