Competition between adjacent piRNA-producing sites autonomously shapes the repertoire and biogenesis efficiency of piRNAs

PIWI-interacting RNAs (piRNAs) are a class of small RNAs that play critical roles in silencing transposable elements (TEs). piRNAs are produced by nucleolytic processing of their single-stranded long precursor transcripts. A subset of piRNAs exhibits a strong preference for uridine (U) at their 5' end. However, not all Us within the precursor sequences are actually used to produce piRNAs, and it remains unknown how the production pattern of piRNAs is determined. Here, we conducted a comparative analysis of the small RNA sequencing data from two sibling lines of silkworm cultured cells that were separated by continuous cultivation over years. We found that the piRNA production patterns are highly changeable when the efficiency of piRNA biogenesis is low. This can be explained by competition between adjacent piRNA-producing sites, as supported by our mathematical modeling. Moreover, this competition can rationalize how piRNAs autonomously avoid deleterious mismatches to target TEs. These findings provide new insights into the intrinsic plasticity and adaptability of the piRNA system to combat diverse TE sequences.