The evolution of RNA interference among Metazoa

Abstract

In Animals, three main RNA interference mechanisms have been described so far, which respectively maturate three types of small noncoding RNAs (sncRNAs): miRNAs, piRNAs and endo-siRNAs. The diversification of these mechanisms is deeply linked with the evolution of the Argonaute gene superfamily since each type of sncRNA is loaded by a specific Argonaute homolog protein. Moreover, other protein families play pivotal roles in the maturation of sncRNAs, like the DICER ribonuclease family, whose DICER1 and DICER2 paralogs maturate respectively miRNAs and endo-siRNAs. Among Metazoa, the distribution of these families has been only studied in major groups, and there are very few data for clades like Lophotrochozoa. Thus, we here inferred the evolutionary history of the animal Argonaute and DICER families including 43 lophotrochozoan species. Phylogenetic analyses along with newly sequenced sncRNA libraries depicted a loss of the endo-siRNA pathway along the Lophotrochozoa evolution, with the absence of DICER2 in Nematoda and Polyzoa, and with the absence of DICER2 and the Argonaute homolog in the rest of Trochozoa phyla. On the contrary, early diverging phyla, Platyhelminthes and Syndermata, showed a complete endo-siRNA pathway. On the other hand, miRNAs were revealed the most conserved and ubiquitous mechanism of the metazoan RNA interference machinery, confirming their pivotal role in animal cell regulation.SignificanceThe RNA interference (RNAi) pathway is one of the most important regulatory systems and it has been pointed out as a source of many evolutionary novelties. Lophotrochozoa comprehends a notable fraction of the animals’ body plans, but an analysis of the main animal RNAi mechanisms has never been attempted. In this study we were able to depict novel patterns in the evolution of RNAi in Lophotrochozoan animals through the phylogenetic inference of Argonaute and DICER families and the analysis and sequencing of new small RNA libraries. These results strengthen the significance of the miRNA pathway among Metazoa and give support to some highly debated phylogenetic hypotheses within Lophotrochozoa.