Studies of developmentally regulated heterochromatin formation and DNA elimination in the unicellular eukaryote Tetrahymena thermophila have revealed a pathway requiring both nuclear RNA interference (RNAi) and PcG proteins, providing a unique opportunity to dissect the interaction between them. Internal eliminated sequences (IES) in Tetrahymena are derived from transposable elements (TE). A wide array of potential TE are revealed in the recently sequenced Tetrahymena MIC genome. Recent transposition in Tetrahymena population is supported by TE insertion polymorphism in IES, as well as purifying selection in coding sequences of many potential TE. Nonetheless, the molecular mechanism underlying transcriptional silencing and reactivation of TE remains elusive.
RNAi and Polycomb repression play evolutionarily conserved and often coordinated roles in transcriptional silencing. Here we show transcription reactivation of IES in mutants deficient in nuclear RNAi and Polycomb repression. Importantly, transcriptional silencing and reactivation of TE-related sequences are contingent upon shunting between the noncoding RNA (ncRNA) and mRNA production pathways, which can be affected by co-transcriptional processing, nuclear RNAi, and Polycomb repression. We propose that interplay between the nuclear RNAi and Polycomb repression pathways may be a widespread phenomenon, whose ancestral role is epigenetic silencing of TE.