Dicer-dependent heterochromatic small RNAs in the model diatom species Phaeodactylum tricornutum

Diatoms are eukaryotic microalgae responsible for nearly half of the marine productivity. RNA interference (RNAi) is a mechanism of regulation of gene expression mediated by small RNAs (sRNAs) processed by the endoribonuclease Dicer (DCR). To date, the mechanism and physiological role of RNAi in diatoms are unknown. We mined diatom genomes and transcriptomes for key RNAi effectors and retraced their phylogenetic history. We generated DCR knockout lines in the model diatom species Phaeodactylum tricornutum and analyzed their mRNA and sRNA populations, repression-associated histone marks, and acclimatory response to nitrogen starvation. Diatoms presented a diversification of key RNAi effectors whose distribution across species suggests the presence of distinct RNAi pathways. P. tricornutum DCR was found to process 26-31-nt-long double-stranded sRNAs originating mostly from transposons covered by repression-associated epigenetic marks. In parallel, P. tricornutum DCR was necessary for the maintenance of the repression-associated histone marks H3K9me2/3 and H3K27me3. Finally, PtDCR-KO lines presented a compromised recovery post nitrogen starvation suggesting a role for P. tricornutum DCR in the acclimation to nutrient stress. Our study characterized the molecular function of the single DCR homolog of P. tricornutum suggesting an association between RNAi and heterochromatin maintenance in this model diatom species.