Extensive Copy-Number Variation of Young Genes across Stickleback Populations

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After a locus is duplicated in a genome, individuals from a population instantaneously differ in the number of copies of this locus producing a copy-number variation (CNV). Over time, the joint effects of selection and other evolutionary forces will act to either eliminate the extra genetic copy or retain it. Depending on this evolutionary interplay, young duplications, including newly duplicated genes, can persist for millions of years as CNVs. CNVs may especially be prevalent between populations that have colonized and adapted to disparate environments in which selective pressures differ. Using whole genome sequences from several populations of three-spined sticklebacks that inhabit different environments, we find that a third of young duplicated genes are CNVs. These young CNV genes are enriched with environmental response functions and evolving rapidly at the molecular level, making them promising candidates for a role in the rapid ecological adaptation to novel environments.

Vyšlo v časopise: Extensive Copy-Number Variation of Young Genes across Stickleback Populations. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004830
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004830

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1. IafrateAJ, FeukL, RiveraMN, ListewnikML, DonahoePK, et al. (2004) Detection of large-scale variation in the human genome. Nature Genet 36: 949–951 doi:10.1038/ng1416

2. WaszakSM, HasinY, ZichnerT, OlenderT, KeydarI, et al. (2010) Systematic inference of copy-number genotypes from personal genome sequencing data reveals extensive olfactory receptor gene content diversity. PLoS Comput Biol 6: e1000988 doi:10.1371/journal.pcbi.1000988

3. SebatJ, LakshmiB, TrogeJ, AlexanderJ, YoungJ, et al. (2004) Large-scale copy number polymorphism in the human genome. Science 305: 525–528 doi:10.1126/science.1098918

4. RedonR, IshikawaS, FitchKR, FeukL, PerryGH, et al. (2006) Global variation in copy number in the human genome. Nature 444: 444–454 doi:10.1038/nature05329

5. KorbelJO, UrbanAE, AffourtitJP, GodwinB, GrubertF, et al. (2007) Paired-end mapping reveals extensive structural variation in the human genome. Science 318: 420–426 doi:10.1126/science.1149504

6. EmersonJJ, Cardoso-MoreiraM, BorevitzJO, LongM (2008) Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science 320: 1629–1631 doi:10.1126/science.1158078

7. FeulnerPGD, ChainFJJ, PanchalM, EizaguirreC, KalbeM, et al. (2013) Genome-wide patterns of standing genetic variation in a marine population of three-spined sticklebacks. Mol Ecol 22: 635–649 doi:10.1111/j.1365-294X.2012.05680.x

8. LynchM, SungW, MorrisK, CoffeyN, LandryCR, et al. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci USA 105: 9272–9277 doi:10.1073/pnas.0803466105

9. TurnerDJ, MirettiM, RajanD, FieglerH, CarterNP, et al. (2008) Germline rates of de novo meiotic deletions and duplications causing several genomic disorders. Nature Genet 40: 90–95 doi:10.1038/ng.2007.40

10. LipinskiKJ, FarslowJC, FitzpatrickKA, LynchM, KatjuV, et al. (2011) High spontaneous rate of gene duplication in Caenorhabditis elegans. Curr Biol 21: 306–310 doi:10.1016/j.cub.2011.01.026

11. SchriderDR, HouleD, LynchM, HahnMW (2013) Rates and genomic consequences of spontaneous mutational events in Drosophila melanogaster. Genetics 194: 937–954 doi:10.1534/genetics.113.151670

12. KatjuV, BergthorssonU (2013) Copy-number changes in evolution: rates, fitness effects and adaptive significance. Front Genet 4: 273 doi:10.3389/fgene.2013.00273

13. PerryGH, DominyNJ, ClawKG, LeeAS, FieglerH, et al. (2007) Diet and the evolution of human amylase gene copy number variation. Nature Genet 39: 1256–1260 doi:10.1038/ng2123

14. CookDE, LeeTG, GuoX, MelitoS, WangK, et al. (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338: 1206–1209 doi:10.1126/science.1228746

15. IskowRC, GokcumenO, LeeC (2012) Exploring the role of copy number variants in human adaptation. TIG 28: 245–257 doi:10.1016/j.tig.2012.03.002

16. KondrashovFA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc R Soc Lond [Biol] 279: 5048–5057 doi:10.1098/rspb.2012.1108

17. LynchM, ConeryJS (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155.

18. KorbelJO, KimPM, ChenX, UrbanAE, WeissmanS, et al. (2008) The current excitement about copy-number variation: how it relates to gene duplications and protein families. Current Opinion in Structural Biology 18: 366–374 doi:10.1016/j.sbi.2008.02.005

19. JuanD, RicoD, Marques-BonetT, Fernandez-CapetilloO, ValenciaA (2013) Late-replicating CNVs as a source of new genes. Biology Open. doi:10.1242/bio.20136924

20. LongM, VanKurenNW, ChenS, VibranovskiMD (2013) New gene evolution: little did we know. Annu Rev Genet 47: 307–333 doi:10.1146/annurev-genet-111212-133301

21. Ohno S (1970) Evolution by gene duplication. Springer-Verlag. 1 pp.

22. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press.1 pp.

23. LongM, BetránE, ThorntonK, WangW (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4: 865–875 doi:10.1038/nrg1204

24. ConantGC, WolfeKH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9: 938–950 doi:10.1038/nrg2482

25. KhalturinK, HemmrichG, FrauneS, AugustinR, BoschTCG (2009) More than just orphans: are taxonomically-restricted genes important in evolution? TIG 25: 404–413 doi:10.1016/j.tig.2009.07.006

26. ColbourneJK, PfrenderME, GilbertD, ThomasWK, TuckerA, et al. (2011) The ecoresponsive genome of Daphnia pulex. Science 331: 555–561 doi:10.1126/science.1197761

27. TautzD, Domazet-LošoT (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12: 692–702 doi:10.1038/nrg3053

28. PeichelCL, NerengKS, OhgiKA, ColeBL, ColosimoPF, et al. (2001) The genetic architecture of divergence between threespine stickleback species. Nature 414: 901–905 doi:10.1038/414901a

29. GibsonG (2005) Evolution. The synthesis and evolution of a supermodel. Science 307: 1890–1891 doi:10.1126/science.1109835

30. JonesFC, GrabherrMG, ChanYF, RussellP, MauceliE, et al. (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484: 55–61 doi:10.1038/nature10944

31. HohenlohePA, BasshamS, EtterPD, StifflerN, JohnsonEA, et al. (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6: e1000862 doi:10.1371/journal.pgen.1000862

32. RoestiM, HendryAP, SalzburgerW, BernerD (2012) Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs. Mol Ecol 21: 2852–2862 doi:10.1111/j.1365-294X.2012.05509.x

33. DeagleBE, JonesFC, AbsherDM, KingsleyDM, ReimchenTE (2013) Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome-wide single nucleotide polymorphism genotyping. Mol Ecol 22: 1917–1932 doi:10.1111/mec.12215

34. WilliamsonSH, HernandezR, Fledel-AlonA, ZhuL, NielsenR, et al. (2005) Simultaneous inference of selection and population growth from patterns of variation in the human genome. Proc Natl Acad Sci USA 102: 7882–7887 doi:10.1073/pnas.0502300102

35. BoykoAR, WilliamsonSH, IndapAR, DegenhardtJD, HernandezRD, et al. (2008) Assessing the evolutionary impact of amino acid mutations in the human genome. PLoS Genet 4: e1000083 doi:10.1371/journal.pgen.1000083

36. ProuxE, StuderRA, MorettiS, Robinson-RechaviM (2009) Selectome: a database of positive selection. Nucleic Acids Res 37: D404–D407 doi:10.1093/nar/gkn768

37. MorettiS, LaurenczyB, GharibWH, CastellaB, KuzniarA, et al. (2013) Selectome update: quality control and computational improvements to a database of positive selection. Nucleic Acids Res 42: D917–21 doi:10.1093/nar/gkt1065

38. SharpAJ, LockeDP, McGrathSD, ChengZ, BaileyJA, et al. (2005) Segmental duplications and copy-number variation in the human genome. Am J Hum Genet 77: 78–88 doi:10.1086/431652

39. CooperGM, NickersonDA, EichlerEE (2007) Mutational and selective effects on copy-number variants in the human genome. Nature Genet 39: S22–S29 doi:10.1038/ng2054

40. TeshimaKM, InnanH (2004) The effect of gene conversion on the divergence between duplicated genes. Genetics 166: 1553–1560.

41. KatjuV, BergthorssonU (2010) Genomic and population-level effects of gene conversion in Caenorhabditis paralogs. Genes (Basel) 1: 452–468 doi:10.3390/genes1030452

42. HiraiwaM (1999) Cathepsin A/protective protein: an unusual lysosomal multifunctional protein. Cell Mol Life Sci 56: 894–907.

43. HsingLC, RudenskyAY (2005) The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol Rev 207: 229–241 doi:10.1111/j.0105-2896.2005.00310.x

44. ChanYF, MarksME, JonesFC, VillarrealG, ShapiroMD, et al. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302–305 doi:10.1126/science.1182213

45. FawcettJA, InnanH (2013) The role of gene conversion in preserving rearrangement hotspots in the human genome. TIG 29: 561–568 doi:10.1016/j.tig.2013.07.002

46. PerryGH, TchindaJ, McGrathSD, ZhangJ, PickerSR, et al. (2006) Hotspots for copy number variation in chimpanzees and humans. Proc Natl Acad Sci USA 103: 8006–8011 doi:10.1073/pnas.0602318103

47. Kehrer-SawatzkiH, CooperDN (2008) Comparative analysis of copy number variation in primate genomes. Cytogenet Genome Res 123: 288–296 doi:10.1159/000184720

48. OrtiG, BellMA, ReimchenTE, MeyerA (1994) Global survey of mitochondrial DNA sequences in the threespine stickleback: evidence for recent migrations. Evolution 48: 608–622.

49. SchriderDR, HahnMW (2010) Gene copy-number polymorphism in nature. Proc R Soc Lond [Biol] 277: 3213–3221 doi:10.1073/pnas.0710524104

50. GuryevV, SaarK, AdamovicT, VerheulM, van HeeschSAAC, et al. (2008) Distribution and functional impact of DNA copy number variation in the rat. Nature Genet 40: 538–545 doi:10.1038/ng.141

51. Marques-BonetT, GirirajanS, EichlerEE (2009) The origins and impact of primate segmental duplications. TIG 25: 443–454 doi:10.1016/j.tig.2009.08.002

52. SudmantPH, KitzmanJO, AntonacciF, AlkanC, MaligM, et al. (2010) Diversity of human copy number variation and multicopy genes. Science 330: 641–646 doi:10.1126/science.1197005

53. KimPM, LamHYK, UrbanAE, KorbelJO, AffourtitJ, et al. (2008) Analysis of copy number variants and segmental duplications in the human genome: Evidence for a change in the process of formation in recent evolutionary history. Genome Res 18: 1865–1874 doi:10.1101/gr.081422.108

54. GazaveE, DarreF, Morcillo-SuarezC, Petit-MartyN, CarrenoA, et al. (2011) Copy number variation analysis in the great apes reveals species-specific patterns of structural variation. Genome Res 21: 1626–1639 doi:10.1101/gr.117242.110

55. GhanemN, Uring-LambertB, AbbalM, HauptmannG, LefrancMP, et al. (1988) Polymorphism of MHC class III genes: definition of restriction fragment linkage groups and evidence for frequent deletions and duplications. Hum Genet 79: 209–218.

56. SjödinP, JakobssonM (2012) Population genetic nature of copy number variation. Methods Mol Biol 838: 209–223 doi:_10.1007/978-1-61779-507-7_10

57. XuL, HouY, BickhartDM, SongJ, Van TassellCP, et al. (2014) A genome-wide survey reveals a deletion polymorphism associated with resistance to gastrointestinal nematodes in Angus cattle. Funct Integr Genomics 14: 333–9 doi:10.1007/s10142-014-0371-6

58. MilinskiM, GriffithsS, WegnerKM, ReuschTBH, Haas-AssenbaumA, et al. (2005) Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proc Natl Acad Sci USA 102: 4414–4418 doi:10.1073/pnas.0408264102

59. EizaguirreC, LenzTL, TraulsenA, MilinskiM (2009) Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecology Letters 12: 5–12 doi:10.1111/j.1461-0248.2008.01247.x

60. EizaguirreC, LenzTL, SommerfeldRD, HarrodC, KalbeM, et al. (2011) Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes. Evol Ecol 25: 605–622 doi:10.1007/s10682-010-9424-z

61. HussainA, SaraivaLR, KorschingSI (2009) Positive Darwinian selection and the birth of an olfactory receptor clade in teleosts. Proc Natl Acad Sci USA 106: 4313–4318 doi:10.1073/pnas.0803229106

62. HashiguchiY, NishidaM (2007) Evolution of trace amine associated receptor (TAAR) gene family in vertebrates: lineage-specific expansions and degradations of a second class of vertebrate chemosensory receptors expressed in the olfactory epithelium. Mol Biol Evol 24: 2099–2107 doi:10.1093/molbev/msm140

63. HashiguchiY, FurutaY, NishidaM (2008) Evolutionary patterns and selective pressures of odorant/pheromone receptor gene families in teleost fishes. PLoS ONE 3: e4083 doi:10.1371/journal.pone.0004083

64. ZhangYE, LandbackP, VibranovskiM, LongM (2012) New genes expressed in human brains: Implications for annotating evolving genomes. Bioessays 34: 982–991 doi:10.1002/bies.201200008

65. FlicekP, AmodeMR, BarrellD, BealK, BrentS, et al. (2012) Ensembl 2012. Nucleic Acids Res 40: D84–D90 doi:10.1093/nar/gkr991

66. AbyzovA, UrbanAE, SnyderM, GersteinM (2011) CNVnator: An approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing. Genome Res 21: 974–984 doi:10.1101/gr.114876.110

67. ChenK, WallisJW, McLellanMD, LarsonDE, KalickiJM, et al. (2009) BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nature Methods 6: 677–681 doi:10.1038/nmeth.1363

68. RauschT, ZichnerT, SchlattlA, StützAM, BenesV, et al. (2012) DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics 28: i333–i339 doi:10.1093/bioinformatics/bts378

69. YeK, SchulzMH, LongQ, ApweilerR, NingZ (2009) Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25: 2865–2871 doi:10.1093/bioinformatics/btp394

70. Team RC (2013) R: a language and environment for statistical computing.

71. VilellaAJ, SeverinJ, Ureta-VidalA, HengL, DurbinR, et al. (2008) EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327–335 doi:10.1101/gr.073585.107

72. QuinlanAR, HallIM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842 doi:10.1093/bioinformatics/btq033

73. BryantD, MoultonV (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21: 255–265 doi:10.1093/molbev/msh018

74. HusonDH, BryantD (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267 doi:10.1093/molbev/msj030

75. DePristoMA, BanksE, PoplinR, GarimellaKV, MaguireJR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genet 43: 491–498 doi:10.1038/ng.806

76. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079 doi:10.1093/bioinformatics/btp352

77. BrowningSR, BrowningBL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81: 1084–1097 doi:10.1086/521987

78. DanecekP, AutonA, AbecasisG, AlbersCA, BanksE, et al. (2011) The variant call format and VCFtools. Bioinformatics 27: 2156–2158 doi:10.1093/bioinformatics/btr330

79. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829 doi:10.1101/gr.074492.107

80. HuangX, MadanA (1999) CAP3: A DNA sequence assembly program. Genome Res 9: 868–877.

81. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410 doi:10.1016/S0022-2836(05)80360-2

82. ConesaA, GötzS, García-GómezJM, TerolJ, TalónM, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676 doi:10.1093/bioinformatics/bti610

83. SaraivaLR, KorschingSI (2007) A novel olfactory receptor gene family in teleost fish. Genome Res 17: 1448–1457 doi:10.1101/gr.6553207

84. AlexaA, RahnenführerJ, LengauerT (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600–1607 doi:10.1093/bioinformatics/btl140

85. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25: 402–408 doi:10.1006/meth.2001.1262

86. WegnerKM, KalbeM, RauchG, KurtzJ, SchaschlH, et al. (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15: 1153–1164 doi:10.1111/j.1365-294X.2006.02855.x

87. SchmittgenTD, LivakKJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 1101–1108 doi:10.1038/nprot.2008.73

88. RanwezV, HarispeS, DelsucF, DouzeryEJP (2011) MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS ONE 6: e22594 doi:10.1371/journal.pone.0022594

89. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591 doi:10.1093/molbev/msm088

90. GuoB, ChainFJ, Bornberg-BauerE, LederEH, MeriläJ (2013) Genomic divergence between nine- and three-spined sticklebacks. BMC Genomics 14: 756 doi:10.1186/1471-2164-14-756

91. ZhengY, ZhaoL, GaoJ, FeiZ (2011) iAssembler: a package for de novo assembly of Roche-454/Sanger transcriptome sequences. BMC Bioinformatics 12: 453 doi:10.1186/1471-2105-12-453

92. SawyerS (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6: 526–538.

93. McGrathCL, CasolaC, HahnMW (2009) Minimal effect of ectopic gene conversion among recent duplicates in four mammalian genomes. Genetics 182: 615–622 doi:10.1534/genetics.109.101428