Journal
GENES & DEVELOPMENT
Volume 24, Issue 11, Pages 1119-1132Publisher
COLD SPRING HARBOR LAB PRESS, PUBLICATIONS DEPT
DOI: 10.1101/gad.1914110
Keywords
Chromatin; histone deacetylation; DNA methylation; epigenetics; RNA polymerase I; ribosomal RNA genes
Categories
Funding
- NIH [GM60380]
- Fundacao para a Ciencia e Tecnologia, Portugal [SFRH/BD/6520/2001, SFRH/BPD/30386/2006]
- Ruth L. Kirschstein National Research Service Award
- Edward Mallinckrodt Foundation
- Fundação para a Ciência e a Tecnologia [SFRH/BPD/30386/2006, SFRH/BD/6520/2001] Funding Source: FCT
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The Arabidopsis histone deacetylase HDA6 is required to silence transgenes, transposons, and ribosomal RNA (rRNA) genes subjected to nucleolar dominance in genetic hybrids. In nonhybrid Arabidopsis thaliana, we show that a class of 45S rRNA gene variants that is normally inactivated during development fails to be silenced in hda6 mutants. In these mutants, symmetric cytosine methylation at CG and CHG motifs is reduced, and spurious RNA polymerase II (Pol II) transcription occurs throughout the intergenic spacers. The resulting sense and antisense spacer transcripts facilitate a massive overproduction of siRNAs that, in turn, direct de novo cytosine methylation of corresponding gene sequences. However, the resulting de novo DNA methylation fails to suppress Pol I or Pol II transcription in the absence of HDA6 activity; instead, euchromatic histone modifications typical of active genes accumulate. Collectively, the data reveal a futile cycle of unregulated transcription, siRNA production, and siRNA-directed DNA methylation in the absence of HDA6-mediated histone deacetylation. We propose that spurious Pol II transcription throughout the intergenic spacers in hda6 mutants, combined with losses of histone deacetylase activity and/or maintenance DNA methylation, eliminates repressive chromatin modifications needed for developmental rRNA gene dosage control.
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