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Evolution of microRNA transcriptome at the onset of Drosophila metamorphosis

ABSTRACT: 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.

OTHER RELATED OMICS DATASETS IN: PRJNA246456PRJNA240207PRJNA239466

ORGANISM(S): Drosophila simulans Drosophila yakuba Drosophila melanogaster

PROVIDER: GSE57438 | GEO | 2014/08/06

SECONDARY ACCESSION(S): PRJNA246456

REPOSITORIES: GEO

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Project description:Background: MicroRNAs (miRNAs) repress target genes at the post-transcriptional level, and function in the development and cell-lineage pathways of host species. Tissue-specific expression of miRNAs is highly relevant to their physiological roles in the corresponding tissues. However, to date, few miRNAs have been spatially identified in the silkworm. Results: We establish for the first time the spatial expression patterns of nearly 100 miRNAs in multiple normal tissues (organs) of Bombyx mori females and males using microarray and Northern-blotting analyses. In total, only 10 miRNAs were universally distributed (including bmo-let-7 and bmo-bantam), while the majority were expressed exclusively or preferentially in specific tissue types (e.g. bmo-miR-275 and bmo-miR-1). We additionally examined the developmental patterns of miRNA expression during metamorphosis of the body wall, silk glands, midgut and fat body. In total, 63 miRNAs displayed significant alterations in abundance in at least 1 tissue during the developmental transition from larvae to pupae (e.g. bmo-miR-263b and bmo-miR-124). Expression patterns of five miRNAs were significantly increased during metamorphosis in all four tissues (e.g. bmo-miR-27 and bmo-miR-305). Conclusions: In this study, we conducted preliminary spatial measurements of several miRNAs in the silkworm. Periods of rapid morphological change were associated with alterations in miRNA expression patterns in the body wall, silk glands, midgut and fat body during metamorphosis. Accordingly, we propose that this ubiquitous or tissue-specific expression of miRNAs supports their critical roles in tissue specification. The results obtained should facilitate future functional analyses. To determine the global spatial expression patterns of miRNAs in silkworm, we designed a DNA oligonucleotide-based microarray examining 92 unique miRNAs with 106 antisense probes. To determine the extent of tissue-specific changes during the specific developmental events, we assessed changes in miRNA expression in four individual tissues and organs (body wall, silk glands, midgut and fat body) from the larval to pupal stages.

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Evolution of microRNA transcriptome at the onset of Drosophila metamorphosis

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