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

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101239074 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7404 (Electronic) Linking ISSN: 15537390 NLM ISO Abbreviation: PLoS Genet Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, c2005-

DNA Methylation* ; Gene Silencing* ; Hot Temperature*; DNA Transposable Elements/*genetics ; RNA, Plant/*genetics ; Zea mays/*genetics; Epigenesis, Genetic ; Genes, Plant ; Histones/metabolism ; Mutation ; Zea mays/growth & development ; Zea mays/physiology

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.
Competing Interests: The authors have declared that no competing interests exist.

Plant Methods. 2007 Sep 24;3:11. (PMID: 17892552)
Sci Rep. 2015 Aug 19;5:13251. (PMID: 26285801)
Nature. 2011 Apr 7;472(7341):115-9. (PMID: 21399627)
Annu Rev Plant Biol. 2009;60:43-66. (PMID: 19007329)
Plant Cell. 2018 Jun;30(6):1337-1352. (PMID: 29802212)
Nat Genet. 2016 Jun;48(6):687-93. (PMID: 27111034)
PLoS Genet. 2008 Aug 22;4(8):e1000165. (PMID: 18725928)
Genes Genet Syst. 2020 Oct 23;95(4):183-190. (PMID: 32893196)
Mol Plant. 2018 Mar 5;11(3):381-387. (PMID: 29032247)
G3 (Bethesda). 2020 May 4;10(5):1727-1743. (PMID: 32179621)
Nat Rev Mol Cell Biol. 2015 Sep;16(9):519-32. (PMID: 26296162)
Nature. 2017 Nov 2;551(7678):124-128. (PMID: 29072296)
Curr Opin Plant Biol. 2012 Nov;15(5):496-502. (PMID: 23022393)
Nature. 2009 Sep 17;461(7262):423-6. (PMID: 19734880)
EMBO Rep. 2014 Apr;15(4):446-52. (PMID: 24562611)
Mol Cell. 2014 Aug 7;55(3):495-504. (PMID: 25018018)
Mol Plant. 2010 May;3(3):594-602. (PMID: 20410255)
Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6130-5. (PMID: 11959901)
Trends Plant Sci. 2014 May;19(5):320-6. (PMID: 24618094)
Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22184-9. (PMID: 21135217)
Nat Rev Genet. 2010 Mar;11(3):204-20. (PMID: 20142834)
Plant Physiol. 2016 Aug;171(4):2648-58. (PMID: 27307257)
Essays Biochem. 2019 Dec 20;63(6):743-755. (PMID: 31652316)
Annu Rev Plant Biol. 2015;66:269-96. (PMID: 25621513)
PLoS Genet. 2019 Sep 9;15(9):e1008291. (PMID: 31498837)
Nat Rev Mol Cell Biol. 2018 Aug;19(8):489-506. (PMID: 29784956)
Curr Opin Plant Biol. 2017 Apr;36:135-141. (PMID: 28343122)
Epigenetics. 2014 Jul;9(7):980-6. (PMID: 24762702)
Nature. 2000 May 11;405(6783):203-6. (PMID: 10821279)
Nat Rev Genet. 2014 Jun;15(6):394-408. (PMID: 24805120)
Biochim Biophys Acta Gene Regul Mech. 2017 Jan;1860(1):140-148. (PMID: 27521981)
Nat Plants. 2018 Mar;4(3):181-188. (PMID: 29379150)
BMC Bioinformatics. 2008 Sep 11;9:371. (PMID: 18786255)
Nature. 2006 Jul 20;442(7100):295-8. (PMID: 16855589)
Curr Biol. 2007 Feb 20;17(4):379-84. (PMID: 17239600)
Mol Biol Evol. 2018 Jun 1;35(6):1332-1337. (PMID: 29688526)
Curr Opin Genet Dev. 2018 Apr;49:43-48. (PMID: 29525544)
Curr Biol. 2003 Dec 16;13(24):2212-7. (PMID: 14680640)
PLoS Biol. 2003 Dec;1(3):E67. (PMID: 14691539)
Curr Opin Plant Biol. 2015 Feb;23:15-24. (PMID: 25449722)
Genetics. 2006 Jan;172(1):579-92. (PMID: 16219782)
Nat Struct Mol Biol. 2009 Jul;16(7):763-8. (PMID: 19503079)
Genetics. 1995 Aug;140(4):1379-87. (PMID: 7498777)
Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8547-52. (PMID: 24912148)
PLoS Genet. 2016 May 12;12(5):e1005998. (PMID: 27171361)
Biochim Biophys Acta. 2015 Apr;1849(4):403-16. (PMID: 25086340)
Proc Natl Acad Sci U S A. 2013 Jan 29;110(5):1953-8. (PMID: 23319643)
Cell. 2013 Mar 28;153(1):193-205. (PMID: 23540698)
Plant Cell. 2000 Nov;12(11):2101-18. (PMID: 11090212)
EMBO J. 2011 May 18;30(10):1928-38. (PMID: 21487388)
PLoS Genet. 2008 Aug 15;4(8):e1000156. (PMID: 18704160)
Nat Struct Mol Biol. 2014 Jan;21(1):64-72. (PMID: 24336224)
Biochem Soc Trans. 2019 Aug 30;47(4):1187-1196. (PMID: 31278155)
Nature. 2014 Nov 27;515(7528):587-90. (PMID: 25219852)
PLoS Genet. 2015 Jan 08;11(1):e1004915. (PMID: 25569788)
PLoS Genet. 2009 Nov;5(11):e1000737. (PMID: 19936292)
PLoS Genet. 2014 Jan 30;10(1):e1004115. (PMID: 24497839)
Genetics. 2003 Mar;163(3):1109-22. (PMID: 12663548)
Science. 2009 Feb 27;323(5918):1201-5. (PMID: 19251626)
Proc Natl Acad Sci U S A. 2015 Nov 24;112(47):14728-33. (PMID: 26553984)
Nat Commun. 2017 May 17;8:15120. (PMID: 28513600)
Nat Cell Biol. 2020 Jun;22(6):621-629. (PMID: 32393884)
Curr Opin Cell Biol. 2009 Jun;21(3):367-76. (PMID: 19243928)
Planta. 2008 Dec;229(1):99-113. (PMID: 18800226)
Plant Cell Physiol. 2001 Dec;42(12):1345-54. (PMID: 11773527)
Plant Cell. 2016 Feb;28(2):314-25. (PMID: 26869701)
Nat Genet. 2005 Jun;37(6):641-4. (PMID: 15908951)
Plant Physiol. 2016 Mar;170(3):1535-48. (PMID: 26747286)
Sci Rep. 2016 Jul 27;6:30446. (PMID: 27461139)
Genetics. 1999 Jan;151(1):331-41. (PMID: 9872971)
Nature. 2009 Oct 22;461(7267):1130-4. (PMID: 19847266)
Trends Plant Sci. 2002 Nov;7(11):498-504. (PMID: 12417150)
Nat Genet. 2016 Jun;48(6):694-9. (PMID: 27111035)
Plant J. 2003 Feb;33(4):743-9. (PMID: 12609046)
Nature. 2014 Mar 6;507(7490):124-128. (PMID: 24463519)
Genetics. 2020 Jun;215(2):379-391. (PMID: 32229532)
Cell. 2014 Mar 27;157(1):95-109. (PMID: 24679529)
Nat Genet. 2013 Sep;45(9):1029-39. (PMID: 23852169)
PLoS Genet. 2020 Dec 15;16(12):e1009243. (PMID: 33320854)
Nat Commun. 2017 May 03;8:15122. (PMID: 28466841)
Mol Biol Rep. 2011 Aug;38(6):3787-94. (PMID: 21104438)
Cell. 2017 Sep 21;171(1):34-57. (PMID: 28938122)
Plant Cell Physiol. 2012 May;53(5):824-33. (PMID: 22173101)
Nat Rev Mol Cell Biol. 2014 May;15(5):340-56. (PMID: 24755934)
Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7783-8. (PMID: 8755553)
Cytogenet Genome Res. 2005;110(1-4):229-41. (PMID: 16093677)
Microbiol Spectr. 2015 Apr;3(2):MDNA3-0032-2014. (PMID: 26104710)
Plant J. 2007 Nov;52(3):391-404. (PMID: 17764504)
Genetics. 2004 Oct;168(2):961-9. (PMID: 15514067)
Plant Signal Behav. 2015;10(9):e1027851. (PMID: 26313233)
Cell Res. 2019 May;29(5):379-390. (PMID: 30778176)
Annu Rev Plant Biol. 2014;65:505-30. (PMID: 24579996)
Science. 1996 Aug 2;273(5275):654-7. (PMID: 8662558)
Plant Cell. 2016 Feb;28(2):304-13. (PMID: 26869697)
Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2214-9. (PMID: 18250331)
Nat Rev Genet. 2005 May;6(5):351-60. (PMID: 15861207)
Cell. 2007 Sep 7;130(5):851-62. (PMID: 17803908)
Nat Commun. 2018 Jan 31;9(1):460. (PMID: 29386641)
Science. 2009 Mar 20;323(5921):1600-4. (PMID: 19179494)
Curr Biol. 1996 Aug 1;6(8):959-61. (PMID: 8805314)
Plant Cell. 2001 Mar;13(3):553-70. (PMID: 11251096)
Nat Genet. 2003 Jan;33(1):102-6. (PMID: 12483211)
Genetics. 1991 Sep;129(1):261-70. (PMID: 1657702)
Science. 2012 Jun 15;336(6087):1448-51. (PMID: 22555433)
PLoS Biol. 2006 Oct;4(10):e339. (PMID: 16968137)
Nature. 2006 Aug 31;442(7106):1046-9. (PMID: 16892047)
Genes Dev. 2006 Apr 1;20(7):898-912. (PMID: 16600915)
Genetics. 2003 Oct;165(2):781-97. (PMID: 14573488)
Nat Rev Genet. 2017 Jan;18(1):5-23. (PMID: 27748375)
EMBO J. 2002 Dec 2;21(23):6549-59. (PMID: 12456661)
Genetics. 1995 Apr;139(4):1777-96. (PMID: 7789777)
Brief Funct Genomics. 2014 Jul;13(4):308-17. (PMID: 24651721)
Nat Plants. 2020 Dec;6(12):1455-1467. (PMID: 33257860)
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):14958-63. (PMID: 18815367)

0 (DNA Transposable Elements)
0 (Histones)
0 (RNA, Plant)

Date Created: 20210614 Date Completed: 20211027 Latest Revision: 20211027

20240104

PMC8224964

10.1371/journal.pgen.1009326

34125827