Genome-wide microRNA screening in Nile tilapia reveals pervasive isomiRs\u2019 transcription, sex-biased arm switching and increasing complexity of expression throughout development

Danillo Pinhal,James G Patton,Ney Lemke,Cesar Martins,Luiz A Bovolenta,Alexandre W S Hilsdorf,Arthur C Oliveira,Pedro G Nachtigall,Simon Moxon,Marcio L Acencio

doi:10.1038/s41598-018-26607-x

Abstract

MicroRNAs (miRNAs) are key regulators of gene expression in multicellular organisms. The elucidation of miRNA function and evolution depends on the identification and characterization of miRNA repertoire of strategic organisms, as the fast-evolving cichlid fishes. Using RNA-seq and comparative genomics we carried out an in-depth report of miRNAs in Nile tilapia (Oreochromis niloticus), an emergent model organism to investigate evo-devo mechanisms. Five hundred known miRNAs and almost one hundred putative novel vertebrate miRNAs have been identified, many of which seem to be teleost-specific, cichlid-specific or tilapia-specific. Abundant miRNA isoforms (isomiRs) were identified with modifications in both 5p and 3p miRNA transcripts. Changes in arm usage (arm switching) of nine miRNAs were detected in early development, adult stage and even between male and female samples. We found an increasing complexity of miRNA expression during ontogenetic development, revealing a remarkable synchronism between the rate of new miRNAs recruitment and morphological changes. Overall, our results enlarge vertebrate miRNA collection and reveal a notable differential ratio of miRNA arms and isoforms influenced by sex and developmental life stage, providing a better picture of the evolutionary and spatiotemporal dynamics of miRNAs.

Highlights

MicroRNAs are small non-coding RNA molecules found in animals, plants and some eukaryotic viruses, which increase the robustness of biological processes by reinforcing transcriptional regulation
The miRNA regulation strength in animals is greatly dependent on the amount of complementarity between miRNA seed region and miRNA recognition elements (MREs) at the messenger RNAs (mRNAs) transcript
If a sequence was present in miRBase, it was considered a known miRNA; otherwise, it was described as a novel miRNA

Summary

Introduction

MicroRNAs (miRNAs) are small non-coding RNA molecules found in animals, plants and some eukaryotic viruses, which increase the robustness of biological processes by reinforcing transcriptional regulation. They play key roles in organismal development and in tissue homeostasis, and control a wide diversity of processes including body patterning, tissue differentiation, cell cycle regulation and carcinogenesis[1,2]. These small non-coding RNAs have a negative regulatory role on protein-coding gene expression. ARS has been proposed to be a common and imperative phenomenon of miRNA diversification[2]

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Conclusion