PIWI genes and piRNAs are ubiquitously expressed in mollusks and show patterns of lineage-specific adaptation

Abstract

PIWI proteins and PIWI-interacting RNAs (piRNAs) suppress transposon activity in animals, thus protecting their genomes from detrimental insertion mutagenesis. Here, we reveal that PIWI genes and piRNAs are ubiquitously expressed in mollusks, similar to the situation in arthropods. We describe lineage-specific adaptations of transposon composition in piRNA clusters in the great pond snail and the pacific oyster, likely reflecting differential transposon activity in gastropods and bivalves. We further show that different piRNA clusters with unique transposon composition are dynamically expressed during oyster development. Finally, bioinformatics analyses suggest that different populations of piRNAs presumably bound to different PIWI paralogs participate in homotypic and heterotypic ping-pong amplification loops in a tissue- and sex-specific manner. Together with recent findings from other animal species, our results support the idea that somatic piRNA expression represents the ancestral state in metazoans.

Evolutionary implications of the microRNA- and piRNA complement of Lepidodermella squamata (Gastrotricha)

“…Interestingly, homotypic ping-pong amplification was also described in the oyster Crassostrea gigas , suggest that piRNA processing patterns in L. squamata is different than in nematodes, but, instead, very similar to what was recently reported for mollusks [65] (a spiralian) and comparable in size to the piRNA complement in flatworms [41,44] . Accordingly, the piRNA data indicate that Gastrotricha ( L. squamata ) are more closely related to Platyhelminthes within Spiralia rather than to Nematoda within Ecdysozoa.…”

“…Aub-bound sequences tend to start with uridine, while AGO3-associated piRNAs show 10A, but no 5' bias [64] . A similar heterotypic ping-pong amplification cycle was also recently described in mollusks, where two different PIWI proteins bind sense and antisense transcripts, respectively [65] . These two proteins bind piRNAs of 29-30 nt (with 1U bias) and 24-25 nt (with 10A bias), respectively.…”

“…The small non-coding RNA pathways are best described for C. elegans [52] . A systematic survey for protein repertoires directly involved in RNA interference pathways was performed using a curated set of 65 RNAi proteins as queries (see supplementary table S1). We found putative orthologs of most C. elegans…”

“…For instance, mouse piRNAs bound to MILI or MIWI2 show mean lengths of 26 and 28 nt, respectively [66]. 1U-biased piRNAs in L. squamata tend to be slightly longer than in the majority of animals analyzed to date[65][66][67] . They are very similar to what was previously reported in the planarian S. mediterranea[41] , where bands of 31-32 nt were identified by both sequencing and Northern blot analyses.…”

PIWI-piRNA pathway-mediated transposable element repression inHydrasomatic stem cells

“…The strongest 10 base pair overlap was found when comparing sense Hyli piRNAs and antisense Hywi piRNAs as expected. However, all possible combinations showed some degree of 10 base pair overlap, which suggested that the ping-pong mechanism can occur with any combination of PIWI proteins including homotypic ping-pong, which has also been documented in Drosophila, mice, and mollusks (Aravin et al 2008;Zhang et al 2012;Jehn et al 2018). Overall, this demonstrates that piRNAs expressed in the ESCs are processed by the ping-pong biogenesis pathway (Brennecke et al 2007) (Iwasaki et al 2015).…”