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.

Repression of CHROMOMETHYLASE 3 Prevents Epigenetic Collateral Damage in Arabidopsis

“…Complex mechanisms are required to specifically silence mutagenic TEs rather than endogenous genes (Antunez-Sanchez et al, 2020;Deng et al, 2016;Lee et al, 2021;Lister et al, 2008;Papareddy et al, 2020;Saze and Kakutani, 2011;Williams et al, 2015;Zhang et al, 2020). Mechanisms regulating epigenome homeostasis are of paramount importance during Arabidopsis embryogenesis due to highly dynamic cell cycle and transcriptional activities, as well as the establishment of cell lineages that will produce all future cell types including the gametes.…”

“…M ethylation of DNA encoding transposable elements (TE) is required to silence their expression and consequently prevent them from mobilizing and mutagenizing genomes (Kato et al, 2003;Law and Jacobsen, 2010). Complex mechanisms have evolved to balance the high degree of sensitivity needed to direct methylation and silencing of TEs with the precision required to prevent ectopic methylation of endogenous genes (Antunez-Sanchez et al, 2020;Ito et al, 2015;Papareddy et al, 2020;Saze and Kakutani, 2011;Williams et al, 2015;Zhang et al, 2020). However, little is known about the mechanisms of epigenome homeostasis during embryogenesis when organisms are particularly vulnerable to TE-induced mutagenesis, as well as the establishment of potentially deleterious epimutations that can persist through many cell divisions and even across generations (Henderson and Jacobsen, 2007;Mathieu et al, 2007;Probst et al, 2009;Saze et al, 2003;Scheid et al, 1998).…”

Repression of CHROMOMETHYLASE 3 prevents epigenetic collateral damage in Arabidopsis

“…Methylation of DNA encoding transposable elements (TE) is required to silence their expression and consequently prevent them from mobilizing and mutagenizing genomes ( Kato et al, 2003 ; Law and Jacobsen, 2010 ). Complex mechanisms have evolved to balance the high degree of sensitivity needed to direct methylation and silencing of TEs with the precision required to prevent ectopic methylation of endogenous genes ( Antunez-Sanchez et al, 2020 ; Ito et al, 2015 ; Papareddy et al, 2020 ; Saze and Kakutani, 2011 ; Williams et al, 2015 ; Zhang et al, 2020 ). However, little is known about the mechanisms of epigenome homeostasis during embryogenesis when organisms are particularly vulnerable to TE-induced mutagenesis, as well as the establishment of potentially deleterious epimutations that can persist through many cell divisions and even across generations ( Henderson and Jacobsen, 2007 ; Mathieu et al, 2007 ; Probst et al, 2009 ; Saze et al, 2003 ; Mittelsten Scheid et al, 1998 ).…”

Role of Chromatin Architecture in Plant Stress Responses: An Update

“…As PRC2 is absent in the sperm, the H3K27me3 demethylation by JMJ proteins is supposed to occur globally, whereas in somatic tissues, H3K27 demethylases occupy the border of H3K27me3 domains in presence of PRC2 ( Yan et al, 2018 ). ELF6 and REF6 play important roles in H3K27me3 and H3K27me1 homeostasis ( Antunez-Sanchez et al, 2020 ). elf6 ref6 jmj13 mutant showed elevated levels of H3K27me3 in the sperm when compared to wild type, suggesting the role of active demethylation by JMJ proteins in contribution to paternal H3K27me3 resetting.…”