全部 标题 作者
关键词 摘要

PLOS ONE  2014 

SHOOT GROWTH1 Maintains Arabidopsis Epigenomes by Regulating IBM1

DOI: 10.1371/journal.pone.0084687

Full-Text   Cite this paper   Add to My Lib

Abstract:

Maintaining correct DNA and histone methylation patterns is essential for the development of all eukaryotes. In Arabidopsis, we identified SHOOT GROWTH1 (SG1), a novel protein involved in the control of gene methylation. SG1 contains both a Bromo-Adjacent Homology (BAH) domain found in several chromatin regulators and an RNA-Recognition Motif (RRM). The sg1 mutations are associated with drastic pleiotropic phenotypes. The mutants degenerate after few generations and are similar to mutants of the histone demethylase INCREASE IN BONSAI METHYLATION1 (IBM1). A methylome analysis of sg1 mutants revealed a large number of gene bodies hypermethylated in the cytosine CHG context, associated with an increase in di-methylation of lysine 9 on histone H3 tail (H3K9me2), an epigenetic mark normally found in silenced transposons. The sg1 phenotype is suppressed by mutations in genes encoding the DNA methyltransferase CHROMOMETHYLASE3 (CMT3) or the histone methyltransferase KRYPTONITE (KYP), indicating that SG1 functions antagonistically to CMT3 or KYP. We further show that the IBM1 transcript is not correctly processed in sg1, and that the functional IBM1 transcript complements sg1. Altogether, our results suggest a function for SG1 in the maintenance of genome integrity by regulating IBM1.

References

[1]  Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315–322.
[2]  Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev. Genet. 11: 204–220.
[3]  Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, et al. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153: 193–205.
[4]  Huff JT, Zilberman D (2012) Regulation of biological accuracy, precision, and memory by plant chromatin organization. Curr. Opin. Genet. Dev. 22: 132–138.
[5]  Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166–1176.
[6]  Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, et al. (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151: 167–180.
[7]  Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, et al. (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol. : CB 17: 379–384.
[8]  Inagaki S, Miura-Kamio A, Nakamura Y, Lu F, Cui X, et al. (2010) Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J. 1 29: 3496–3506.
[9]  Miura A, Nakamura M, Inagaki S, Kobayashi A, Saze H, et al. (2009) An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J. 28: 1078–1086.
[10]  Saze H, Shiraishi A, Miura A, Kakutani T (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319: 462–465.
[11]  Fan D, Dai Y, Wang X, Wang Z, He H, et al. (2012) IBM1, a JmjC domain-containing histone demethylase, is involved in the regulation of RNA-directed DNA methylation through the epigenetic control of RDR2 and DCL3 expression in Arabidopsis. Nucl. Acids Res. 40: 8905–8916.
[12]  Vlad D, Rappaport F, Simon M, Loudet O (2010) Gene transposition causing natural variation for growth in Arabidopsis thaliana. PLoS Genet. 6: e1000945.
[13]  Schiex T, Moisan A, Rouzé P (2001) EuGene: An Eucaryotic Gene Finder that combines several sources of evidence. Comp. Biol. LNCS 2066: LNCS 2066. pp. 111–125.
[14]  Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, et al. (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163: 1109–1122.
[15]  Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260: 1926–1928.
[16]  Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352–364.
[17]  Rigal M, Kevei Z, Pélissier T, Mathieu O (2012) DNA methylation in an intron of the IBM1 histone demethylase gene stabilizes chromatin modification patterns. EMBO J. 31(13): 2981–93.
[18]  Saze H, Kitayama J, Takashima K, Miura S, Harukawa Y, et al. (2013) Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin. Nat Commun. 4: 2301.
[19]  Wang X, Duan CG, Tang K, Wang B, Zhang H, et al. (2013) RNA-binding protein regulates plant DNA methylation by controlling mRNA processing at the intronic heterochromatin-containing gene IBM1. Proc Natl Acad Sci U S A. 110(38): 15467–72.
[20]  Liu X, Yu CW, Duan J, Luo M, Wang K, et al. (2012) HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis. Plant Physiol. 158: 119–129.
[21]  Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, et al. (2012) The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484: 115–119.
[22]  Sasaki T, Kobayashi A, Saze H, Kakutani T (2012) RNAi-independent de novo DNA methylation revealed in Arabidopsis mutants of chromatin remodeling gene DDM1. Plant J. 70: 750–758.
[23]  Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nature Rev. Genet. 13: 484–492.
[24]  Loudet O, Gaudon V, Trubuil A, Daniel-Vedele F (2005) Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family. TAG 110: 742–753.
[25]  Simon M, Loudet O, Durand S, Berard A, Brunel D, et al. (2008) Quantitative trait loci mapping in five new large recombinant inbred line populations of Arabidopsis thaliana genotyped with consensus single-nucleotide polymorphism markers. Genetics 178: 2253–2264.
[26]  Agorio A, Vera P (2007) ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis. Plant Cell 19: 3778–3790.
[27]  Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, et al. (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077–2080.
[28]  Mathieu O, Probst AV, Paszkowski J (2005) Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J. l 24: 2783–2791.
[29]  Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476: 105–108.

Full-Text

comments powered by Disqus