Adaptive evolution of newly emerged micro-RNA genes in Drosophila.

How often micro-RNA (miRNA) genes emerged and how fast they evolved soon after their emergence are some of the central questions in the evolution of miRNAs. Because most known miRNA genes are ancient and highly conserved, these questions can be best answered by identifying newly emerged miRNA genes. Among the 78 miRNA genes in Drosophila reported before 2007, only 5 are confirmed to be newly emerged in the genus (although many more can be found in the newly reported data set; e.g., Ruby et al. 2007; Stark et al. 2007; Lu et al. 2008). These new miRNA genes have undergone numerous changes, even in the normally invariant mature sequences. Four of them (the miR-310/311/312/313 cluster, denoted miR-310s) were duplicated from other conserved miRNA genes. The fifth one (miR-303) appears to be a very young gene, originating de novo from a non-miRNA sequence recently. We sequenced these 5 miRNA genes and their neighboring regions from a worldwide collection of Drosophila melanogaster lines. The levels of divergence and polymorphism in these miRNA genes, vis-à-vis those of the neighboring DNA sequences, suggest that these 5 genes are evolving adaptively. Furthermore, the polymorphism pattern of miR-310s in D. melanogaster is indicative of hitchhiking under positive selection. Thus, a large number of adaptive changes over a long period of time may be essential for the evolution of newly emerged miRNA genes.

[1]  Walter Fontana,et al.  Fast folding and comparison of RNA secondary structures , 1994 .

[2]  Anton J. Enright,et al.  Human MicroRNA Targets , 2004, PLoS biology.

[3]  D. Haussler,et al.  Evolution's cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Cullen,et al.  Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha , 2005, The EMBO journal.

[5]  Manolis Kellis,et al.  Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. , 2007, Genome research.

[6]  C. Burge,et al.  Vertebrate MicroRNA Genes , 2003, Science.

[7]  Manolis Kellis,et al.  Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes. , 2007, Genome research.

[8]  Nikolaus Rajewsky,et al.  Computational identification of microRNA targets , 2004, Genome Biology.

[9]  Jian Lu,et al.  The birth and death of microRNA genes in Drosophila , 2008, Nature Genetics.

[10]  Xiaowei Wang,et al.  Systematic identification of microRNA functions by combining target prediction and expression profiling , 2006, Nucleic acids research.

[11]  L. Lim,et al.  An Abundant Class of Tiny RNAs with Probable Regulatory Roles in Caenorhabditis elegans , 2001, Science.

[12]  Debora S. Marks,et al.  Antisense-Mediated Depletion Reveals Essential and Specific Functions of MicroRNAs in Drosophila Development , 2005, Cell.

[13]  R. Russell,et al.  Principles of MicroRNA–Target Recognition , 2005, PLoS biology.

[14]  Kai Zeng,et al.  Compound tests for the detection of hitchhiking under positive selection. , 2007, Molecular biology and evolution.

[15]  Eugene Berezikov,et al.  Many novel mammalian microRNA candidates identified by extensive cloning and RAKE analysis. , 2006, Genome research.

[16]  Colin N. Dewey,et al.  Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans , 2007, PLoS biology.

[17]  Justin C. Fay,et al.  Hitchhiking under positive Darwinian selection. , 2000, Genetics.

[18]  Y. Fu,et al.  Statistical properties of segregating sites. , 1995, Theoretical population biology.

[19]  A. Pasquinelli,et al.  Regulation by let-7 and lin-4 miRNAs Results in Target mRNA Degradation , 2005, Cell.

[20]  R. Aharonov,et al.  Identification of hundreds of conserved and nonconserved human microRNAs , 2005, Nature Genetics.

[21]  R. Nielsen,et al.  Detecting Selection in Noncoding Regions of Nucleotide Sequences , 2004, Genetics.

[22]  Phillip A Sharp,et al.  siRNAs can function as miRNAs , 2003 .

[23]  Kristin C. Gunsalus,et al.  microRNA Target Predictions across Seven Drosophila Species and Comparison to Mammalian Targets , 2005, PLoS Comput. Biol..

[24]  M. Kreitman,et al.  Adaptive protein evolution at the Adh locus in Drosophila , 1991, Nature.

[25]  Adam Eyre-Walker,et al.  Adaptive protein evolution in Drosophila , 2002, Nature.

[26]  Phillip D. Zamore,et al.  Ribo-gnome: The Big World of Small RNAs , 2005, Science.

[27]  N. Rajewsky microRNA target predictions in animals , 2006, Nature Genetics.

[28]  Pardis C Sabeti,et al.  Detecting recent positive selection in the human genome from haplotype structure , 2002, Nature.

[29]  V. Kim MicroRNA biogenesis: coordinated cropping and dicing , 2005, Nature Reviews Molecular Cell Biology.

[30]  Kai Zeng,et al.  Statistical Tests for Detecting Positive Selection by Utilizing High-Frequency Variants , 2006, Genetics.

[31]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[32]  Julius Brennecke,et al.  Identification of Drosophila MicroRNA Targets , 2003, PLoS biology.

[33]  Eugene Berezikov,et al.  Cloning and expression of new microRNAs from zebrafish , 2006, Nucleic acids research.

[34]  Justin C. Fay,et al.  Testing the neutral theory of molecular evolution with genomic data from Drosophila , 2002, Nature.

[35]  Eric J Wagner,et al.  Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. , 2002, Molecular cell.

[36]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[37]  J. Pritchard,et al.  A Map of Recent Positive Selection in the Human Genome , 2006, PLoS biology.

[38]  S. Mano,et al.  Comparisons of site- and haplotype-frequency methods for detecting positive selection. , 2007, Molecular biology and evolution.

[39]  Chenhui Zhang,et al.  Adaptive genic evolution in the Drosophila genomes , 2007, Proceedings of the National Academy of Sciences.

[40]  V. Ambros,et al.  The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. , 1999, Developmental biology.

[41]  B. Cullen,et al.  A Novel Assay for Viral MicroRNA Function Identifies a Single Nucleotide Polymorphism That Affects Drosha Processing , 2006, Journal of Virology.

[42]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[43]  C. Bustamante,et al.  Distinguishing Between Selective Sweeps and Demography Using DNA Polymorphism Data , 2005, Genetics.

[44]  Wen-Hsiung Li Unbiased estimation of the rates of synonymous and nonsynonymous substitution , 2006, Journal of Molecular Evolution.

[45]  Molly Przeworski,et al.  The signature of positive selection at randomly chosen loci. , 2002, Genetics.

[46]  D. Haussler,et al.  Human-mouse alignments with BLASTZ. , 2003, Genome research.

[47]  M. Aguadé,et al.  Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. , 1999, Genetics.

[48]  C. Burge,et al.  Conserved Seed Pairing, Often Flanked by Adenosines, Indicates that Thousands of Human Genes are MicroRNA Targets , 2005, Cell.

[49]  Sudhir Kumar,et al.  Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. , 2003, Molecular biology and evolution.

[50]  C. Burge,et al.  Prediction of Mammalian MicroRNA Targets , 2003, Cell.

[51]  Byoung-Tak Zhang,et al.  Molecular Basis for the Recognition of Primary microRNAs by the Drosha-DGCR8 Complex , 2006, Cell.

[52]  Anton J. Enright,et al.  MicroRNA targets in Drosophila , 2003, Genome Biology.

[53]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[54]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..