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Early detection and repair of damaged DNA is essential for cell functioning and survival. Although multiple cellular systems are involved in repair of single-strand DNA breaks (SSBs), it remains unknown how SSBs present in non-template strand (NT-SSBs) of DNA organized in chromatin are detected. Here the effect of NT-SSBs on transcription through chromatin by RNA polymerase II was studied. NT-SSBs hidden in nucleosome structure can induce nearly quantitative arrest of RNA polymerase. The location of the arrest sites on nucleosomal DNA suggests that formation of small intranucleosomal DNA loops causes the arrest. This mechanism likely involves relief of unconstrained DNA supercoiling accumulated during transcription through chromatin by NT-SSBs. The data suggest existence of a novel chromatin-specific mechanism allowing detection of NT-SSBs by the transcribing enzyme.