Abstract
RNAi is an evolutionarily fluid mechanism with dramatically different activities across animal phyla. One major group where there has been little investigation is annelid worms. Here, the small RNAs of the polychaete developmental model Capitella teleta are profiled across development. As is seen with nearly all animals, nearly 200 microRNAs were found with 58 high-confidence novel species. Greater miRNA diversity was associated with later stages consistent with differentiation of tissues. Outside miRNA, a distinct composition of other small RNA pathways was found. Unlike many invertebrates, an endogenous siRNA pathway was not observed, indicating pathway loss relative to basal planarians. No processively generated siRNA-class RNAs could be found arising from dsRNA precursors. This has a significant impact on RNAi technology development for this group of animals. Unlike the apparent absence of siRNAs, a significant population of piRNAs was observed. For many piRNAs, phasing and ping-pong biogenesis pathways were identified. Interestingly, piRNAs were found to be highly expressed during early development, suggesting a potential role in regulation in metamorphosis. Critically, the configuration of RNAi factors in C. teleta is found in other annelids and mollusks, suggesting that similar biology is likely to be present in the wider clade. This study is the first in providing comprehensive analysis of small RNAs in annelids.
Highlights
RNA interference (RNAi) is a widely applied genetic technology based on fundamental gene regulatory mechanisms, where small RNAs induce complementary transcript degradation or destruction
The absence of siAgo is correlated with C. teleta only having a single Dicer protein that is related to miRNA processing rather than small-interfering RNAs (siRNAs) processing (Figure 1A)
C. teleta Ago possesses the same slicer residues as D. melanogaster Ago1 and Ago2; this is expected as miRNAs, when pairing extensively with a target, can direct slicing. This comprehensive analysis of small RNA populations in the marine annelid C. teleta shows the presence of only two RNA classes, miRNAs and PIWI-interacting RNAs (piRNAs), with an apparent loss of endogenous siRNAs
Summary
RNA interference (RNAi) is a widely applied genetic technology based on fundamental gene regulatory mechanisms, where small RNAs induce complementary transcript degradation or destruction. Among the three major classes of RNAi, miRNAs are the most conserved with sequences shared in most animals (Wienholds and Plasterk, 2005) In comparison, both endogenously expressed siRNAs (endo-siRNAs) and piRNAs show almost no conservation even at the species level, presumably due to their role in silencing invasive nucleic acids (Wynant et al, 2017). Both endogenously expressed siRNAs (endo-siRNAs) and piRNAs show almost no conservation even at the species level, presumably due to their role in silencing invasive nucleic acids (Wynant et al, 2017) In addition to these conservation patterns, each class is defined by loading into a distinct class of Argonaute/PIWI (Ago/PIWI) proteins.
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