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

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 cas...

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Bibliographic Details
Published in:Genome research 2018-01, Vol.28 (1), p.52-65
Main Authors: Mohammed, Jaaved, Flynt, Alex S, Panzarino, Alexandra M, Mondal, Md Mosharrof Hossain, DeCruz, Matthew, Siepel, Adam, Lai, Eric C
Format: Article
Language:English
Subjects:
3' Untranslated Regions
Animals
Antisense RNA
Biosynthesis
Birth
Drosophila
Drosophila - genetics
Evolution
Evolution, Molecular
Gene Expression Profiling
Genetic Loci
Insects
MicroRNAs
MicroRNAs - genetics
miRNA
Phylogeny
Positive selection
Species
Species Specificity
Splicing
Subpopulations
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Summary: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.
ISSN:1088-9051
1549-5469
DOI:10.1101/gr.226068.117