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PMID: 18296702 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

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

Molecular biology and evolution ·Vol. 25 ·No. 5 ·2008-05-00 ·Pages 929-38

Lu J, Fu Y, Kumar S, Shen Y, Zeng K, Xu A, Carthew R, Wu CI

Abstract

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.

MeSH Terms
Adaptation, Biological Animals Drosophila/genetics Drosophila melanogaster/genetics Evolution, Molecular Genes, Insect MicroRNAs/genetics Polymorphism, Genetic
Chemicals
MicroRNAs
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Lu Jian
Department of Ecology and Evolution, University of Chicago, USA.
Fu Yonggui
Kumar Supriya
Shen Yang
Zeng Kai
Xu Anlong
Carthew Richard
Wu Chung-I
References (55)
55 references, click to expand
  1. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.
    J Mol Evol. 1980 Dec;16(2):111-20 PMID: 7463489
  2. Statistical properties of segregating sites.
    Theor Popul Biol. 1995 Oct;48(2):172-97 PMID: 7482370
  3. siRNAs can function as miRNAs.
    Genes Dev. 2003 Feb 15;17(4):438-42 PMID: 12600936
  4. Many novel mammalian microRNA candidates identified by extensive cloning and RAKE analysis.
    Genome Res. 2006 Oct;16(10):1289-98 PMID: 16954537
  5. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex.
    Cell. 2006 Jun 2;125(5):887-901 PMID: 16751099
  6. Systematic identification of microRNA functions by combining target prediction and expression profiling.
    Nucleic Acids Res. 2006 Mar 20;34(5):1646-52 PMID: 16549876
  7. microRNA target predictions across seven Drosophila species and comparison to mammalian targets.
    PLoS Comput Biol. 2005 Jun;1(1):e13 PMID: 16103902
  8. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets.
    Cell. 2005 Jan 14;120(1):15-20 PMID: 15652477
  9. Adaptive protein evolution in Drosophila.
    Nature. 2002 Feb 28;415(6875):1022-4 PMID: 11875568
  10. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  11. Human MicroRNA targets.
    PLoS Biol. 2004 Nov;2(11):e363 PMID: 15502875
  12. Hitchhiking under positive Darwinian selection.
    Genetics. 2000 Jul;155(3):1405-13 PMID: 10880498
  13. Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells.
    Mol Cell. 2002 Jun;9(6):1327-33 PMID: 12086629
  14. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks.
    Mol Biol Evol. 2004 Jan;21(1):36-44 PMID: 12949132
  15. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha.
    EMBO J. 2005 Jan 12;24(1):138-48 PMID: 15565168
  16. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans.
    PLoS Biol. 2007 Nov 6;5(11):e310 PMID: 17988176
  17. MicroRNA biogenesis: coordinated cropping and dicing.
    Nat Rev Mol Cell Biol. 2005 May;6(5):376-85 PMID: 15852042
  18. microRNA target predictions in animals.
    Nat Genet. 2006 Jun;38 Suppl:S8-13 PMID: 16736023
  19. Identification of hundreds of conserved and nonconserved human microRNAs.
    Nat Genet. 2005 Jul;37(7):766-70 PMID: 15965474
  20. Unbiased estimation of the rates of synonymous and nonsynonymous substitution.
    J Mol Evol. 1993 Jan;36(1):96-9 PMID: 8433381
  21. A novel assay for viral microRNA function identifies a single nucleotide polymorphism that affects Drosha processing.
    J Virol. 2006 Jun;80(11):5321-6 PMID: 16699012
  22. Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11484-9 PMID: 14500911
  23. A map of recent positive selection in the human genome.
    PLoS Biol. 2006 Mar;4(3):e72 PMID: 16494531
  24. The signature of positive selection at randomly chosen loci.
    Genetics. 2002 Mar;160(3):1179-89 PMID: 11901132
  25. Detecting recent positive selection in the human genome from haplotype structure.
    Nature. 2002 Oct 24;419(6909):832-7 PMID: 12397357
  26. Computational identification of microRNA targets.
    Dev Biol. 2004 Mar 15;267(2):529-35 PMID: 15013811
  27. Cloning and expression of new microRNAs from zebrafish.
    Nucleic Acids Res. 2006 May 12;34(9):2558-69 PMID: 16698962
  28. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation.
    Dev Biol. 1999 Dec 15;216(2):671-80 PMID: 10642801
  29. Detecting selection in noncoding regions of nucleotide sequences.
    Genetics. 2004 Jun;167(2):949-58 PMID: 15238543
  30. Mfold web server for nucleic acid folding and hybridization prediction.
    Nucleic Acids Res. 2003 Jul 1;31(13):3406-15 PMID: 12824337
  31. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila.
    Genetics. 1999 Jan;151(1):239-49 PMID: 9872963
  32. Compound tests for the detection of hitchhiking under positive selection.
    Mol Biol Evol. 2007 Aug;24(8):1898-908 PMID: 17557886
  33. Human-mouse alignments with BLASTZ.
    Genome Res. 2003 Jan;13(1):103-7 PMID: 12529312
  34. Evolution of genes and genomes on the Drosophila phylogeny.
    Nature. 2007 Nov 8;450(7167):203-18 PMID: 17994087
  35. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans.
    Science. 2001 Oct 26;294(5543):858-62 PMID: 11679671
  36. Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development.
    Cell. 2005 Jul 1;121(7):1097-108 PMID: 15989958
  37. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs.
    Genome Res. 2007 Dec;17(12):1850-64 PMID: 17989254
  38. Ribo-gnome: the big world of small RNAs.
    Science. 2005 Sep 2;309(5740):1519-24 PMID: 16141061
  39. Principles of microRNA-target recognition.
    PLoS Biol. 2005 Mar;3(3):e85 PMID: 15723116
  40. Prediction of mammalian microRNA targets.
    Cell. 2003 Dec 26;115(7):787-98 PMID: 14697198
  41. Vertebrate microRNA genes.
    Science. 2003 Mar 7;299(5612):1540 PMID: 12624257
  42. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  43. Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes.
    Genome Res. 2007 Dec;17(12):1865-79 PMID: 17989255
  44. Adaptive genic evolution in the Drosophila genomes.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2271-6 PMID: 17284599
  45. Testing the neutral theory of molecular evolution with genomic data from Drosophila.
    Nature. 2002 Feb 28;415(6875):1024-6 PMID: 11875569
  46. Distinguishing between selective sweeps and demography using DNA polymorphism data.
    Genetics. 2005 Jul;170(3):1401-10 PMID: 15911584
  47. Statistical tests for detecting positive selection by utilizing high-frequency variants.
    Genetics. 2006 Nov;174(3):1431-9 PMID: 16951063
  48. Comparisons of site- and haplotype-frequency methods for detecting positive selection.
    Mol Biol Evol. 2007 Jul;24(7):1562-74 PMID: 17449894
  49. MicroRNAs: genomics, biogenesis, mechanism, and function.
    Cell. 2004 Jan 23;116(2):281-97 PMID: 14744438
  50. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation.
    Cell. 2005 Aug 26;122(4):553-63 PMID: 16122423
  51. Identification of Drosophila MicroRNA targets.
    PLoS Biol. 2003 Dec;1(3):E60 PMID: 14691535
  52. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  53. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  54. MicroRNA targets in Drosophila.
    Genome Biol. 2003;5(1):R1 PMID: 14709173
  55. The birth and death of microRNA genes in Drosophila.
    Nat Genet. 2008 Mar;40(3):351-5 PMID: 18278047
Article Info
Journal
Molecular biology and evolution
Abbr.
Mol Biol Evol
ISSN
1537-1719
DOI
10.1093/molbev/msn040
Published
2008-05-00
Epub
2008-00-22
Pages
929-38
Language
English
Region
United States
NLM ID
8501455
PMCID
PMC3707409
Subset
IM
Grants
NIGMS NIH HHS · R01 GM068743 · United States
NIGMS NIH HHS · R01 GM077581 · United States
External Links
PubMed source DOI: 10.1093/molbev/msn040 PMC Full Text View journal details
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