HP1 proteins are major components of heterochromatin, which is generally 
perceived to be an inert and transcriptionally inactive chromatin structure. 
Yet, HP1 binding to chromatin is highly dynamic and robust silencing of 
heterochromatic genes can involve RNA processing. Here, we demonstrate by a 
combination of in vivo and in vitro experiments that the fission yeast HP1(Swi6) 
protein guarantees tight repression of heterochromatic genes through RNA 
sequestration and degradation. Stimulated by positively charged residues in the 
hinge region, RNA competes with methylated histone H3K9 for binding to the 
chromodomain of HP1(Swi6). Hence, HP1(Swi6) binding to RNA is incompatible with 
stable heterochromatin association. We propose a model in which an ensemble of 
HP1(Swi6) proteins functions as a heterochromatin-specific checkpoint, capturing 
and priming heterochromatic RNAs for the RNA degradation machinery. Sustaining a 
functional checkpoint requires continuous exchange of HP1(Swi6) within 
heterochromatin, which explains the dynamic localization of HP1 proteins on 
heterochromatin.