Condensin-mediated chromosome condensation is essential for
genome stability upon cell division. Genetic studies have indicated that the association of
condensin with
chromatin is intimately linked to gene transcription, but what transcription-associated feature(s) direct(s) the accumulation of
condensin remains unclear. Here we show in fission yeast that
condensin becomes strikingly enriched at
RNA Pol III-transcribed genes when Swd2.2 and Sen1, two factors involved in the transcription process, are simultaneously deleted. Sen1 is an
ATP-dependent helicase whose orthologue in Saccharomyces cerevisiae contributes both to terminate transcription of some
RNA Pol II transcripts and to antagonize the formation of
DNA:
RNA hybrids in the genome. Using two independent mapping techniques, we show that
DNA:
RNA hybrids form in abundance at Pol III-transcribed genes in fission yeast but we demonstrate that they are unlikely to faciliate the recruitment of
condensin. Instead, we show that Sen1 forms a stable and abundant complex with
RNA Pol III and that Swd2.2 and Sen1 antagonize both the interaction of
RNA Pol III with
chromatin and
RNA Pol III-dependent transcription. When Swd2.2 and Sen1 are lacking, the increased concentration of
RNA Pol III and
condensin at Pol III-transcribed genes is accompanied by the accumulation of
topoisomerase I and II and by local
nucleosome depletion, suggesting that Pol III-transcribed genes suffer topological stress. We provide evidence that this topological stress contributes to recruit and/or stabilize
condensin at Pol III-transcribed genes in the absence of Swd2.2 and Sen1. Our data challenge the idea that a processive
RNA polymerase hinders the binding of
condensin and suggest that transcription-associated topological stress could in some circumstances facilitate the association of
condensin.