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

Author:

Antunez-Sanchez Javier1ORCID,Naish Matthew1ORCID,Ramirez-Prado Juan Sebastian2,Ohno Sho13,Huang Ying2,Dawson Alexander1,Opassathian Korawit1,Manza-Mianza Deborah2ORCID,Ariel Federico2,Raynaud Cecile2,Wibowo Anjar4,Daron Josquin5,Ueda Minako67,Latrasse David2,Slotkin R Keith89,Weigel Detlef4ORCID,Benhamed Moussa210,Gutierrez-Marcos Jose1ORCID

Affiliation:

1. School of Life Science, University of Warwick, Coventry, United Kingdom

2. Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France

3. Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, Japan

4. Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany

5. Department of Molecular Genetics, The Ohio State University, Columbus, United States

6. Institute of Transformative Bio-Molecules, Nagoya University, Nagoya, Japan

7. Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan

8. Donald Danforth Plant Science Center, St. Louis, United States

9. Division of Biological Sciences, University of Missouri, Columbia, United States

10. Université de Paris, Institute of Plant Sciences Paris-Saclay (IPS2), F-75006, Paris, France

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.

Funder

European Commission

Biotechnology and Biological Sciences Research Council

Japan Society for the Promotion of Science

Agence Nationale de la Recherche

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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