School of Life Science, University of Warwick, Coventry, United Kingdom
Juan Sebastian Ramirez-Prado
Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France
Sho Ohno
School of Life Science, University of Warwick, Coventry, United Kingdom; Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, Japan
Ying Huang
Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France
Alexander Dawson
School of Life Science, University of Warwick, Coventry, United Kingdom
Korawit Opassathian
School of Life Science, University of Warwick, Coventry, United Kingdom
Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France
Federico Ariel
Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France
Cecile Raynaud
Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France
Anjar Wibowo
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
Josquin Daron
Department of Molecular Genetics, The Ohio State University, Columbus, United States
Minako Ueda
Institute of Transformative Bio-Molecules, Nagoya University, Nagoya, Japan; Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan
David Latrasse
Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France
R Keith Slotkin
Donald Danforth Plant Science Center, St. Louis, United States; Division of Biological Sciences, University of Missouri, Columbia, United States
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
Moussa Benhamed
Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay, France; Université de Paris, Institute of Plant Sciences Paris-Saclay (IPS2), F-75006, Paris, France
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.