Deep experimental profiling of microRNA diversity, deployment, and evolution across the Drosophila genus

Abstract

To assess miRNA evolution across the genus, we analyzed several billion small RNA reads across 12 fruit fly species. These data permit comprehensive curation of species- and clade-specific variation in miRNA identity, abundance, and processing. Among well-conserved miRNAs, we observed unexpected cases of clade-specific variation in 5' end precision, occasional antisense loci, and putatively noncanonical loci. We also used strict criteria to identify a large set (649) of novel, evolutionarily restricted miRNAs. Within the bulk collection of species-restricted miRNAs, two notable subpopulations are splicing-derived mirtrons and testes-restricted, recently evolved, clustered (TRC) canonical miRNAs. We quantified miRNA birth and death using our annotation and a phylogenetic model for estimating rates of miRNA turnover. We observed striking differences in birth and death rates across miRNA classes defined by biogenesis pathway, genomic clustering, and tissue restriction, and even identified flux heterogeneity among clades. In particular, distinct molecular rationales underlie the distinct evolutionary behavior of different miRNA classes. Mirtrons are associated with high rates of 3' untemplated addition, a mechanism that impedes their biogenesis, whereas TRC miRNAs appear to evolve under positive selection. Altogether, these data reveal miRNA diversity among species and principles underlying their emergence and evolution.

Widespread gene duplication and adaptive evolution in the RNA interference pathways of the Drosophila obscura group

“…In addition, sex-chromosome drive is widespread in the obscura group: X-chromosome drive was first described in D. obscura, and has also been reported in pseudoobscura, persimilis, affinis, azteca, subobscura and athabasca [54] and is mediated through a testisspecific function (Y-bearing sperm have reduced function). Finally, a testis-specific class of hairpin (endo) siRNAs is required for male fertility in D. melanogaster [56], testes-restricted clustered miRNAs show rapid evolutionary turnover and are represented in large numbers in D. pseudoobscura [57], and suppression of sex-specific duplicates of S-Lap1 via a small-RNA mechanism has recently been implicated in the meiotic drive mechanism of D. pseudoobscura [58]. In this context, it is also interesting to note that Ago2 is involved in directing heterochromatin formation in Drosophila dosage compensation [10][11][12], and that in D.…”

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“…A conservation analysis was first conducted to identify all miRNAs in the D. melanogaster genome. All mature miRNAs from the 12 Drosophila subspecies {Kozomara, 2014 #28} were mapped on the D. melanogaster genome and the miRNA loci then determined using criteria based upon the identification of miRNA hairpin-like secondary structures (specifically: adjusted minimal folding free energy (aMFE) < −20 and no branching adjacent to the miRNA/miRNA* duplex) a similar approach as in {Mohammed, 2018 #4633}. We then determined all 7 and 8nt seed regions for all mature miRNAs.…”

Cloudy with a Chance of Insights: Context Dependent Gene Regulation and Implications for the Evolution of Gene Expression

“…Micro RNAs (miRNAs), another group of non-coding RNAs, have been shown to directly modulate histone modifications and thus the chromatin accessibility to allow transcription of target genes [60]. Since miRNAs are highly tissue specifically expressed [61][62][63], these molecules provide an excellent mechanism to facilitate tissue specific chromatin accessibility.…”

“…Comparative studies in five mammals [136] and twelve Drosophila species [62] revealed that also non-coding RNA molecules evolve in a highly context dependent manner. For instance, high turnover rates have been associated with the underlying molecular mechanisms involved in miRNA maturation [62].…”