Transposon-mediated genic rearrangements underlie variation in small RNA pathways

Abstract

AbstractTransposable elements (TEs) are parasitic DNA sequences that insert into the host genome and can cause alterations in host gene structure and expression. Host organisms cope with the often detrimental consequences caused by recent transposition and develop mechanisms that repress TE activities. In the nematodeCaenorhabditis elegans, a small interfering RNA (siRNA) pathway dependent on the helicase ERI-6/7 primarily silences long terminal repeat retrotransposons and recent genes of likely viral origin. By studying gene expression variation among wildC. elegansstrains, we discovered that structural variants and transposon remnants at theeri-6/7locus alter its expression incisand underlie atrans-acting expression quantitative trait locus affecting non-conserved genes and pseudogenes. Multiple insertions of thePolintonDNA transposon (also known asMavericks) reshuffled theeri-6/7locus in different configurations, separating theeri-6anderi-7exons and causing the inversion oferi-6as seen in the reference N2 genome. In the inverted configuration, gene function was previously shown to be repaired by unusualtrans-splicing mediated by direct repeats flanking the inversion. We show that these direct repeats originated from terminal inverted repeats specific toC. elegans Polintons. Thistrans-splicing event occurs infrequently compared tocis-splicing to novel downstream exons, thus affecting the production of ERI-6/7. DiversePolinton-induced structural variations display regulatory effects within the locus and on targets of ERI-6/7-dependent siRNA pathways. Our findings highlight the role of host-transposon interactions in driving rapid host genome diversification among natural populations and shed light on evolutionary novelty in genes and splicing mechanisms.