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Significance Transcription occurs at chromosomal sites known as active transcription sites (ATS). We report that ATS can exist in two classes when assessed at key regulatory genes in their natural context: these “iATS” and “cATS” possess incomplete and complete nascent transcripts, respectively. Frequencies of the two classes are patterned within the developing tissue in a gene-, developmental stage-, and sex-specific manner, revealing ATS class regulation. Moreover, cATS frequency, not iATS frequency, corresponds to mRNA abundance, indicating that regulation of ATS class impacts gene expression. The iATS signature—presence of a long first intron but lacking exons—suggests slowing or pausing of transcriptional progression midway through the gene. We suggest that ATS class regulation can pattern gene expression during development.

Two classes of active transcription sites and their roles in developmental regulation