Systematic analysis reveals surprising roles for lincRNAs during meiosis and beyond

Long intergenic non-coding RNAs (lincRNAs) are transcripts >200 bases long, which undergo similar biosynthesis to mRNA but do not code for proteins. The disproportional number of lincRNAs expressed in testes suggests they play a major role during gametogenesis, but to-date very few were implicated in this process. We took advantage of the relatively limited number of lincRNA’s in the C. elegans genome, to systematically analyse their roles during meiosis. Using CRISPR-Cas genome engineering we completely deleted the seven lincRNA genes with significant expression in the worm’s gonad and tested the effects on central meiotic processes. Surprisingly, the vast majority of lincRNA deletions had no clear impact on these processes. The deletion of only one lincRNA, drl-1, had a clear meiotic phenotype. In this mutant the progeny is significantly smaller and higher levels of germline apoptosis is observed. We detected more RAD-51 foci in drl-1 gonads during mid-late pachytene, suggesting that double strand breaks repair is perturbed. COSA-1 foci analysis indicated that crossover designation dynamics in this mutant also differs from wild type. Removal of the lincRNA wdr-1 led to post-meiotic effects. Deletion of this gene, as well as RNA silencing, created growth delays following L1 arrest. Unexpectedly, we found this effect is the result of wdr-1 expression in the germline and not the soma. This work reveals, surprisingly, that lincRNAs with high expression in the gonad are mostly dispensable for oogenesis, yet several have critical roles in DSBR and post embryonic stages, presumably by attenuating the expression of coding genes.