Abstract
Methylcytosine-binding proteins decipher the epigenetic information encoded by DNA methylation and provide a link between DNA methylation, modification of chromatin structure, and gene silencing. VARIANT IN METHYLATION 1 (VIM1) encodes an SRA (SET- and RING-associated) domain methylcytosine-binding protein in Arabidopsis thaliana, and loss of VIM1 function causes centromere DNA hypomethylation and centromeric heterochromatin decondensation in interphase. In the Arabidopsis genome, there are five VIM genes that share very high sequence similarity and encode proteins containing a PHD domain, two RING domains, and an SRA domain. To gain further insight into the function and potential redundancy among the VIM proteins, we investigated strains combining different vim mutations and transgenic vim knock-down lines that down-regulate multiple VIM family genes. The vim1 vim3 double mutant and the transgenic vim knock-down lines showed decreased DNA methylation primarily at CpG sites in genic regions, as well as repeated sequences in heterochromatic regions. In addition, transcriptional silencing was released in these plants at most heterochromatin regions examined. Interestingly, the vim1 vim3 mutant and vim knock-down lines gained ectopic CpHpH methylation in the 5S rRNA genes against a background of CpG hypomethylation. The vim1 vim2 vim3 triple mutant displayed abnormal morphological phenotypes including late flowering, which is associated with DNA hypomethylation of the 5′ region of FWA and release of FWA gene silencing. Our findings demonstrate that VIM1, VIM2, and VIM3 have overlapping functions in maintenance of global CpG methylation and epigenetic transcriptional silencing.
Highlights
DNA cytosine methylation is an epigenetic mark important for many processes including parental imprinting, X chromosome inactivation, and the silencing of transposable elements [1,2,3]
We previously demonstrated that the VIM1 (VARIANT IN METHYLATION 1) protein from the flowering plant Arabidopsis thaliana binds DNA that contains methylated cytosine and is required for complete methylation and compaction of centromeric DNA
We show that VIM1 works in concert with two related proteins, VIM2 and VIM3, to maintain cytosine methylation at centromeres but throughout the genome
Summary
DNA cytosine methylation is an epigenetic mark important for many processes including parental imprinting, X chromosome inactivation, and the silencing of transposable elements [1,2,3]. DNA cytosine methylation in plants can occur at CpHpG and CpHpH (where H = A, T, or C) as well as CpG sites. Several MBD proteins in mammals, including methyl-CpG-binding protein 1 (MeCP1), MeCP2, MBD2, and MBD4 have been identified with high affinity for methylated DNA, and the biological importance of mammalian methylcytosine-binding proteins has been shown in the wide range of severe phenotypes by mutations of these genes [8,9,10]. Among 13 MBD proteins in the Arabidopsis proteome, three (AtMBD5, AtMBD6, and AtMBD7) have been shown to bind symmetrically methylated CpG sites in vitro [11,12,13]. Developmental defects have been observed in lines carrying a lossof-function mutation of AtMBD9 or a transgene directing RNAi against AtMBD11 transcripts, the role of any AtMBD proteins in epigenetic regulation remains to be defined [14,15]
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