RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.

In large complex plant genomes, RNA-directed DNA methylation (RdDM) ensures that epigenetic silencing is maintained at the boundary between genes and flanking transposable elements. In maize, RdDM is dependent on Mediator of Paramutation1 (Mop1), a gene encoding a putative RNA dependent RNA polymera...

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Autores principales:	Wei Guo, Dafang Wang, Damon Lisch
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Genetics QH426-470
Acceso en línea:	https://doaj.org/article/257f523fcf9a42b2bf2d3915dbb6d095
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spelling	oai:doaj.org-article:257f523fcf9a42b2bf2d3915dbb6d0952021-12-02T20:02:41ZRNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.1553-73901553-740410.1371/journal.pgen.1009326https://doaj.org/article/257f523fcf9a42b2bf2d3915dbb6d0952021-06-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009326https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404In large complex plant genomes, RNA-directed DNA methylation (RdDM) ensures that epigenetic silencing is maintained at the boundary between genes and flanking transposable elements. In maize, RdDM is dependent on Mediator of Paramutation1 (Mop1), a gene encoding a putative RNA dependent RNA polymerase. Here we show that although RdDM is essential for the maintenance of DNA methylation of a silenced MuDR transposon in maize, a loss of that methylation does not result in a restoration of activity. Instead, heritable maintenance of silencing is maintained by histone modifications. At one terminal inverted repeat (TIR) of this element, heritable silencing is mediated via histone H3 lysine 9 dimethylation (H3K9me2), and histone H3 lysine 27 dimethylation (H3K27me2), even in the absence of DNA methylation. At the second TIR, heritable silencing is mediated by histone H3 lysine 27 trimethylation (H3K27me3), a mark normally associated with somatically inherited gene silencing. We find that a brief exposure of high temperature in a mop1 mutant rapidly reverses both of these modifications in conjunction with a loss of transcriptional silencing. These reversals are heritable, even in mop1 wild-type progeny in which methylation is restored at both TIRs. These observations suggest that DNA methylation is neither necessary to maintain silencing, nor is it sufficient to initiate silencing once has been reversed. However, given that heritable reactivation only occurs in a mop1 mutant background, these observations suggest that DNA methylation is required to buffer the effects of environmental stress on transposable elements.Wei GuoDafang WangDamon LischPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 6, p e1009326 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Genetics QH426-470
spellingShingle	Genetics QH426-470 Wei Guo Dafang Wang Damon Lisch RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.
description	In large complex plant genomes, RNA-directed DNA methylation (RdDM) ensures that epigenetic silencing is maintained at the boundary between genes and flanking transposable elements. In maize, RdDM is dependent on Mediator of Paramutation1 (Mop1), a gene encoding a putative RNA dependent RNA polymerase. Here we show that although RdDM is essential for the maintenance of DNA methylation of a silenced MuDR transposon in maize, a loss of that methylation does not result in a restoration of activity. Instead, heritable maintenance of silencing is maintained by histone modifications. At one terminal inverted repeat (TIR) of this element, heritable silencing is mediated via histone H3 lysine 9 dimethylation (H3K9me2), and histone H3 lysine 27 dimethylation (H3K27me2), even in the absence of DNA methylation. At the second TIR, heritable silencing is mediated by histone H3 lysine 27 trimethylation (H3K27me3), a mark normally associated with somatically inherited gene silencing. We find that a brief exposure of high temperature in a mop1 mutant rapidly reverses both of these modifications in conjunction with a loss of transcriptional silencing. These reversals are heritable, even in mop1 wild-type progeny in which methylation is restored at both TIRs. These observations suggest that DNA methylation is neither necessary to maintain silencing, nor is it sufficient to initiate silencing once has been reversed. However, given that heritable reactivation only occurs in a mop1 mutant background, these observations suggest that DNA methylation is required to buffer the effects of environmental stress on transposable elements.
format	article
author	Wei Guo Dafang Wang Damon Lisch
author_facet	Wei Guo Dafang Wang Damon Lisch
author_sort	Wei Guo
title	RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.
title_short	RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.
title_full	RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.
title_fullStr	RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.
title_full_unstemmed	RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.
title_sort	rna-directed dna methylation prevents rapid and heritable reversal of transposon silencing under heat stress in zea mays.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/257f523fcf9a42b2bf2d3915dbb6d095
work_keys_str_mv	AT weiguo rnadirecteddnamethylationpreventsrapidandheritablereversaloftransposonsilencingunderheatstressinzeamays AT dafangwang rnadirecteddnamethylationpreventsrapidandheritablereversaloftransposonsilencingunderheatstressinzeamays AT damonlisch rnadirecteddnamethylationpreventsrapidandheritablereversaloftransposonsilencingunderheatstressinzeamays
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RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.

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