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The microRNA toolkit of insects

ABSTRACT: Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth. Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. Previously, miRNA evolution had been linked to morphological complexity, but astonishing variation in the currently available miRNA complements of insects made this link unclear. To address this issue, we sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. Our analyses show that the variation of insect miRNAs is an artefact mainly resulting from poor sampling and inaccurate miRNA annotation, and that insects share a conserved microRNA toolkit of 65 families exhibiting very low variation. For example, the evolutionary shift toward a complete metamorphosis was accompanied only by the acquisition of three and the loss of one miRNA families.

ORGANISM(S): Blattella germanica

PROVIDER: GSE83339 | GEO | 2016/11/30

SECONDARY ACCESSION(S): PRJNA325631

REPOSITORIES: GEO

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Project description:MicroRNAs (miRNAs) are endogenous RNA molecules that contribute to the regulation of gene expression post-transcriptionally. Recently, patterns of sequence evolution and evolutionary emergence of miRNAs have been analyzed in detail. However, the extent to which miRNA expression levels vary within and between species, the role of stabilizing selection versus other evolutionary mechanisms in shaping the temporal dynamics of these changes, and how this variation might unveil the interplay between miRNAs and mRNAs remain poorly understood. This is especially true during key developmental transitions involving miRNA regulation. Combining deep-sequencing with multi-species microarrays, we assayed miRNA expression levels immediately before (≥18BPF) and after (PF) the increase in steroid hormone ecdysone that triggers metamorphosis. We did so both at the intra- and interspecific levels in the Drosophila melanogaster species group. In contrast to their sequence conservation, ~25% of the analyzed miRNAs differed significantly in expression levels at ≥18BPF and/or PF across D. melanogaster strains. Additionally, ~33% showed modifications in their pattern of expression bias between developmental timepoints. Relative to the patterns of evolution, changes in miRNA abundance at PF accumulate linearly over evolutionary time while similar changes at ≥18BPF do not. Importantly, expression levels of ≥18BPF-enriched miRNAs are the most variable within and between species and therefore the least likely to evolve under stabilizing selection, especially as compared to non-developmentally enriched miRNAs. Overall, functional attributes such as expression ubiquity are more tightly associated with lower levels of miRNA expression polymorphism at PF than at ≥18BPF. Furthermore, ≥18BPF- and PF-enriched miRNAs showed opposite patterns of covariation in expression with mRNAs, which was found to denote the type of regulatory relationship between miRNA and mRNA. By focusing on the miRNA expression levels at the onset of metamorphosis, our results have unveiled contrasting functional patterns of evolutionary divergence during ontogeny.

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The microRNA toolkit of insects

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