Widespread transposon co-option in the <i>Caenorhabditis</i> germline regulatory network.

Carelli, Francesco Nicola; Cerrato, Chiara; Dong, Yan; Appert, Alex; Dernburg, Abby; Ahringer, Julie · Sci Adv · 2022

basic_science · Level V

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Abstract

The movement of selfish DNA elements can lead to widespread genomic alterations with potential to create novel functions. We show that transposon expansions in <i>Caenorhabditis</i> nematodes led to extensive rewiring of germline transcriptional regulation. We find that about one-third of <i>Caenorhabditis elegans</i> germline-specific promoters have been co-opted from two related miniature inverted repeat transposable elements (TEs), CERP2 and CELE2. These promoters are regulated by HIM-17, a THAP domain-containing transcription factor related to a transposase. Expansion of CERP2 occurred before radiation of the <i>Caenorhabditis</i> genus, as did fixation of mutations in HIM-17 through positive selection, whereas CELE2 expanded only in <i>C. elegans</i>. Through comparative analyses in <i>Caenorhabditis briggsae</i>, we find not only evolutionary conservation of most CERP2 co-opted promoters but also a substantial fraction that are species-specific. Our work reveals the emergence and evolutionary conservation of a novel transcriptional network driven by TE co-option with a major impact on regulatory evolution.