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

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

doi:10.7554/elife.58533

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.

Highlights

In eukaryotes, chromatin accessibility is modified by DNA methylation, the covalent modification of histone proteins and the deposition of histone variants
To gain further knowledge about these processes in Arabidopsis, we investigated the function of two sequence-related histone demethylases, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6)
We found that our elf6-C plants displayed an early flowering phenotype characterized by a reduced number of rosette leaves at bolting (Jeong et al, 2009; Noh et al, 2004)

Summary

Introduction

Chromatin accessibility is modified by DNA methylation, the covalent modification of histone proteins and the deposition of histone variants. These epigenetic modifications allow the establishment of specific transcriptional states in response to environmental or developmental cues. While in most cases environmentally-induced chromatin changes are transient, epigenetic changes induced during development are often stably inherited through mitotic divisions, so that cell identity is maintained and individual cells or tissues do not revert to previous developmental states. A key chromatin modification implicated in these responses is the post-translational modification of histone tails, which are associated with active or inactive transcriptional states.

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