Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis

Abstract

SU(VAR)3-9 like histone methyltransferases control heterochromatic domains in eukaryotes. In Arabidopsis, 10 SUVH genes encode SU(VAR)3-9 homologues where SUVH1, SUVH2 and SUVH4 (KRYPTONITE) represent distinct subgroups of SUVH genes. Loss of SUVH1 and SUVH4 causes weak reduction of heterochromatic histone H3K9 dimethylation, whereas in SUVH2 null plants monoand dimethyl H3K9, mono-and dimethyl H3K27, and monomethyl H4K20, the histone methylation marks of Arabidopsis heterochromatin are significantly reduced. Like animal SU(VAR)3-9 proteins SUVH2 displays strong dosage-dependent effects. Loss of function suppresses, whereas overexpression enhances, gene silencing, causes ectopic heterochromatization and significant growth defects. Furthermore, modification of transgene silencing by SUVH2 is partially transmitted to the offspring plants. This epigenetic stability correlates with heritable changes in DNA methylation. Mutational dissection of SUVH2 indicates an implication of its N-terminus and YDG domain in directing DNA methylation to target sequences, a prerequisite for consecutive histone methylation. Gene silencing by SUVH2 depends on MET1 and DDM1, but not CMT3. In Arabidopsis, SUVH2 with its histone H3K9 and H4K20 methylation activity has a central role in heterochromatic gene silencing.

Plant SET domain-containing proteins: Structure, function and regulation

“…In Arabidopsis, SUVH4 (KYP), the best studied member of this class, represses expression of the floral homeotic gene, SUPERMAN (SUP), through its H3K9 methyltransferase activity [90]. Naumann et al [91] reported that the N-terminus and YDG domain in SUVH2 are involved in directing DNA methylation and subsequent histone methylation at its target locus so that heterochromatic methylation marks are affected in suvh2 mutant plants. Recently, Ebbs et al [92,93] showed that there is a hierarchical and locusspecific control of H3K9 di-methylation as well as non-CG DNA methylation by SUVH4, SUVH5 and SUVH6 HMT in Arabidopsis.…”

Impact of nucleosome dynamics and histone modifications on cell proliferation during Arabidopsis development

“…It is also associated with pericentromeric regions and with DNA methylation (Bernatavichute et al, 2008), another modification that contributes to chromatin remodeling. SUVH2 is important for the mono-and dimethylation of H3K9, but suvh2 mutant plants also show alterations in monoand dimethyl H3K27 and monomethyl H4K20 levels (Naumann et al, 2005).…”

LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC

“…The suvh and suvr alleles (in Columbia) contain mutations in genes related to KYP that contain SET domains predicted to methylate histone 3 (20). The mutants include a T-DNA insertion in SUVH2, a gene recently described as being essential for an array of repressive histone methylation marks (19). These mutants were examined by a combination of Northern blots and RT-PCR of nonvernalized and vernalized tissue ( Fig.…”

“…A major contributor to H3K9me2 in Arabidopsis is KRYPTONITE (KYP), a member of the Su-(var)3-9 class of histone methyltransferases first isolated from Drosophila (16) and identified in Arabidopsis through its role in transcriptional silencing of both endogenous genes and transgenes (17,18). Recently, a related protein SUVH2 was shown to have in vitro histone methyltransferase activity and to be required in vivo for H3K9, H3K27, and H4K20 methylation (19). KYP and SUVH2 are 2 of 14 members constituting the Arabidopsis SUVH͞SUVR class of proteins that contain SET domains predicted to methylate histone 3 (20).…”