Transcriptional landscape of small non-coding RNAs reveals diversity of categories and functions in molluscs

ABSTRACT

Small non-coding RNAs (sncRNAs) are non-coding RNA molecules that play various roles in metazoans. Among the sncRNAs, microRNAs (miRNAs) guide post-translational gene regulation during cellular development, proliferation, apoptosis, and differentiation, while PIWI-interacting RNAs (piRNAs) suppress transposon activity to safeguard the genome from detrimental insertion mutagenesis. While an increasing number of piRNAs are being identified in the soma and germlines of various organisms, they are scarcely reported in molluscs. To unravel the small RNA (sRNA) expression patterns and genomic function in molluscs, we generated a comprehensive sRNA dataset by sRNA sequencing (sRNA-seq) of eight mollusc species. Abundant miRNAs were identified and characterized in all investigated molluscs, and ubiquitous piRNAs were discovered in both somatic and gonadal tissues in six of the investigated molluscs, which are more closely associated with transposon silencing. Tens of piRNA clusters were also identified based on the genomic mapping results, which varied among different tissues and species. Our dataset serves as important reference data for future genomic and genetic studies on sRNAs in these molluscs and related species, especially in elucidating the ancestral state of piRNAs in bilaterians.

KEYWORDS:

• miRNAs
• piRNAs
• gene regulation
• transposon silencing
• molluscs

Abbreviations

miRNA: microRNA; piRNA: PIWI-interacting RNA; piRISC: piRNA-induced silencing complex; siRNA: small interfering RNA; sncRNA: small non-coding RNA; sRNA-seq: small RNA sequencing; TE: transposon element.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

S.H. designed and performed the experiments, analysed the data and drafted the manuscript. K.Y. and S.K. collected the samples and assisted with the data analysis. S.A. conceived the study, supervised the work, and co-wrote the manuscript. All authors reviewed the manuscript.

Data availability statement

The raw sequencing reads from smRNA-seq are available in the DNA Data Bank of Japan (DDBJ) Sequence Read Archive (DRA) under the accession number DRA012198.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/15476286.2024.2348893.

Additional information

Funding

This study was supported by grants from the National Key Research and Development Program of China [2018YFD0900601], the Japan Society for the Promotion of Science [JP24248034] and the Research Fellowship of the Japan Society for the Promotion of Science Postdoctoral Fellowship for Overseas Researchers [P20395].