The piRNA cluster torimochi is an expanding transposon in cultured silkworm cells

<jats:p>PIWI proteins and PIWI-interacting RNAs (piRNAs) play a central role in repressing transposable elements in animal germ cells. It is thought that piRNAs are mainly produced from discrete genomic loci named piRNA clusters, which often contain many “dead” transposon remnants from past invasions and have heterochromatic features. In the genome of silkworm ovary-derived cultured cells called BmN4, a well-established model for piRNA research, <jats:italic>torimochi</jats:italic> was previously annotated as a unique and specialized genomic region that can capture transgenes and produce new piRNAs bearing a trans-silencing activity. However, the sequence identity of <jats:italic>torimochi</jats:italic> has remained elusive. Here, we carefully characterized <jats:italic>torimochi</jats:italic> by utilizing the updated silkworm genome sequence and the long-read sequencer MinION. We found that <jats:italic>torimochi</jats:italic> is in fact a full-length gypsy-like LTR retrotransposon, which is exceptionally active and has massively expanded its copy number in BmN4 cells. Many copies of <jats:italic>torimochi</jats:italic> in BmN4 cells have features of open chromatin and the ability to produce piRNAs. Therefore, <jats:italic>torimochi</jats:italic> may represent a young, growing piRNA cluster, which is still “alive” and active in transposition yet capable of trapping other transposable elements to produce <jats:italic>de novo</jats:italic> piRNAs.</jats:p>