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Centromeres interact with the spindle apparatus to enable chromosome disjunction and typically contain thousands of tandemly arranged satellite repeats interspersed with retrotransposons. While their role has been obscure, centromeric repeats are epigenetically modified and centromere specification has a strong epigenetic component. In the yeast  Schizosaccharomyces pombe,  long heterochromatic repeats are transcribed and contribute to centromere function via RNA interference (RNAi). In the higher plant  Arabidopsis thaliana,  as in mammalian cells, centromeric satellite repeats are short (180 base pairs), are found in thousands of tandem copies, and are methylated. We have found transcripts from both strands of canonical, bulk  Arabidopsis  repeats. At least one subfamily of 180–base pair repeats is transcribed from only one strand and regulated by RNAi and histone modification. A second subfamily of repeats is also silenced, but silencing is lost on both strands in mutants in the CpG DNA methyltransferase MET1, the histone deacetylase HDA6/SIL1, or the chromatin remodeling ATPase DDM1. This regulation is due to transcription from  Athila2  retrotransposons, which integrate in both orientations relative to the repeats, and differs between strains of  Arabidopsis.  Silencing lost in  met1  or  hda6  is reestablished in backcrosses to wild-type, but silencing lost in RNAi mutants and  ddm1  is not. Twenty-four–nucleotide small interfering RNAs from centromeric repeats are retained in  met1  and  hda6,  but not in  ddm1,  and may have a role in this epigenetic inheritance. Histone H3 lysine-9 dimethylation is associated with both classes of repeats. We propose roles for transcribed repeats in the epigenetic inheritance and evolution of centromeres.

Differential Regulation of Strand-Specific Transcripts from Arabidopsis Centromeric Satellite Repeats