Adaptive evolution of testis-specific, recently evolved, clustered miRNAs in Drosophila

Mohammed, J., Bortolamiol-Becet, D., Flynt, A. S., Gronau, I., Siepel, A., Lai, E. C. (2014) Adaptive evolution of testis-specific, recently evolved, clustered miRNAs in Drosophila. RNA, 20 (8). pp. 1195-209. ISSN 1355-8382

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URL: http://www.ncbi.nlm.nih.gov/pubmed/24942624
DOI: 10.1261/rna.044644.114

Abstract

The propensity of animal miRNAs to regulate targets bearing modest complementarity, most notably via pairing with miRNA positions approximately 2-8 (the "seed"), is believed to drive major aspects of miRNA evolution. First, minimal targeting requirements have allowed most conserved miRNAs to acquire large target cohorts, thus imposing strong selection on miRNAs to maintain their seed sequences. Second, the modest pairing needed for repression suggests that evolutionarily nascent miRNAs may generally induce net detrimental, rather than beneficial, regulatory effects. Hence, levels and activities of newly emerged miRNAs are expected to be limited to preserve the status quo of gene expression. In this study, we unexpectedly show that Drosophila testes specifically express a substantial miRNA population that contravenes these tenets. We find that multiple genomic clusters of testis-restricted miRNAs harbor recently evolved miRNAs, whose experimentally verified orthologs exhibit divergent sequences, even within seed regions. Moreover, this class of miRNAs exhibits higher expression and greater phenotypic capacities in transgenic misexpression assays than do non-testis-restricted miRNAs of similar evolutionary age. These observations suggest that these testis-restricted miRNAs may be evolving adaptively, and several methods of evolutionary analysis provide strong support for this notion. Consistent with this, proof-of-principle tests show that orthologous miRNAs with divergent seeds can distinguish target sensors in a species-cognate manner. Finally, we observe that testis-restricted miRNA clusters exhibit extraordinary dynamics of miRNA gene flux in other Drosophila species. Altogether, our findings reveal a surprising tissue-directed influence of miRNA evolution, involving a distinct mode of miRNA function connected to adaptive gene regulation in the testis.

Item Type: Paper
Uncontrolled Keywords: *Adaptation, Biological Animals Base Sequence *Biological Evolution Cluster Analysis Conserved Sequence Drosophila/*genetics/*metabolism Evolution, Molecular Gene Expression Gene Expression Profiling Genetic Variation Male MicroRNAs/*genetics Molecular Sequence Data *Multigene Family Organ Specificity/genetics Phenotype Sequence Alignment Testis/*metabolism Drosophila microRNA clusters positive selection testis specific tissue specific
Subjects: organism description > animal > insect > Drosophila
evolution
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > genes, structure and function > gene expression
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > miRNA
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > miRNA
CSHL Authors:
Communities: CSHL labs > Siepel lab
Depositing User: Matt Covey
Date Deposited: 14 Jan 2015 16:42
Last Modified: 14 Jan 2015 16:42
PMCID: PMC4105746
Related URLs:
URI: http://repository.cshl.edu/id/eprint/31084

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