Separable roles for RNAi in regulation of transposable elements and viability in the fission yeast Schizosaccharomyces japonicus

Abstract

RNA interference (RNAi) is a conserved mechanism of small RNA-mediated genome regulation commonly involved in suppression of transposable elements (TEs) through both post-transcriptional silencing, and transcriptional repression via heterochromatin assembly. The fission yeast Schizosaccharomyces pombe has been extensively utilised as a model for studying RNAi pathways. However, this species is somewhat atypical in that TEs are not major targets of RNAi, and instead small RNAs correspond primarily to non-coding pericentromeric repeat sequences, reflecting a specialised role for the pathway in promoting heterochromatin assembly in these regions. In contrast, in the related fission yeast Schizosaccharomyces japonicus, sequenced small RNAs correspond primarily to TEs. This suggests there may be fundamental differences in the operation of RNAi pathways in these two related species. To investigate these differences, we probed RNAi function in S. japonicus. Unexpectedly, and in contrast to S. pombe, we found that RNAi is essential in this species. Moreover, viability of RNAi mutants can be rescued by mutations implicated in enhancing RNAi-independent heterochromatin propagation. These rescued strains retain heterochromatic marks on TE sequences, but exhibit derepression of TEs at the post-transcriptional level. Our findings indicate that S. japonicus retains the ancestral role of RNAi in facilitating suppression of TEs via both post-transcriptional silencing and heterochromatin assembly, with specifically the heterochromatin pathway being essential for viability, likely due to a function in genome maintenance. The specialised role of RNAi in heterochromatin assembly in S. pombe appears to be a derived state that emerged after the divergence of S. japonicus.

A high-quality reference genome for the fission yeastSchizosaccharomyces osmophilus

“…We noticed that the downstream boundary of that copy of Tcry1 has been mis-annotated and its length should be 5095 bp, 40 bp longer than previously reported (see Materials and Methods). S. japonicus has a large variety of retrotransposons (Rhind et al 2011;Chapman et al 2022). However, the retrotransposons in the S. japonicus reference genome tend to have sequence errors (Rhind et al 2011).…”

Telomere-to-telomereSchizosaccharomyces japonicusgenome assembly reveals hitherto unknown genome features

“…Despite being closely related and relying on many conserved genes, several major differences with S. japonicus has made this pair of sister species emerge as a powerful evolutionary cell biology system (Alam, Gu, Reichert, Bahler, & Oliferenko, 2023 ; Gu, Yam, & Oliferenko, 2015; Makarova et al, 2016; Makarova et al, 2020; Yam, He, Zhang, Chiam, & Oliferenko, 2011). Furthermore, S. japonicus has become a standalone model organism for study of processes not present or tractable in other yeasts (Aoki et al, 2011; Chapman, Taglini, & Bayne, 2022; Furuya & Niki, 2010, 2012; Gomez-Gil et al, 2019; Gu & Oliferenko, 2019; Kinnaer, Dudin, & Martin, 2019; Lee et al, 2020; Nozaki, Furuya, & Niki, 2018; Papp, Acs-Szabo, Batta, & Miklos, 2021; Pieper, Sprenger, Teis, & Oliferenko, 2020; Rutherford et al, 2022; Wang et al, 2021; Yam, Gu, & Oliferenko, 2013).…”

Schizosaccharomyces versatilisrepresents a distinct evolutionary lineage

“…More recently, another fission yeast species, Schizosaccharomyces japonicus , has emerged both as a part of a powerful composite evolutionary cell biology model system used alongside S. pombe (Y. Gu, Yam, & Oliferenko, 2015; Makarova et al, 2016; Makarova et al, 2020; Yam, He, Zhang, Chiam, & Oliferenko, 2011) and as a valuable standalone model organism for the study of processes not apparent or tractable in other yeasts (Aoki et al, 2011; Chapman, Taglini, & Bayne, 2022; Furuya & Niki, 2010, 2012; Gomez-Gil et al, 2019; Y. Gu & Oliferenko, 2019; Kinnaer, Dudin, & Martin, 2019; Lee et al, 2020; Nozaki, Furuya, & Niki, 2018; Papp, Acs-Szabo, Batta, & Miklos, 2021; Pieper, Sprenger, Teis, & Oliferenko, 2020; Rutherford, Harris, Oliferenko, & Wood, 2022; Wang et al, 2021; Yam, Gu, & Oliferenko, 2013).…”