Recombination Drives Vertebrate Genome Contraction
Selective and/or neutral processes may govern variation in DNA content and, ultimately, genome size. The observation in several organisms of a negative correlation between recombination rate and intron size could be compatible with a neutral model in which recombination is mutagenic for length changes. We used whole-genome data on small insertions and deletions within transposable elements from chicken and zebra finch to demonstrate clear links between recombination rate and a number of attributes of reduced DNA content. Recombination rate was negatively correlated with the length of introns, transposable elements, and intergenic spacer and with the rate of short insertions. Importantly, it was positively correlated with gene density, the rate of short deletions, the deletion bias, and the net change in sequence length. All these observations point at a pattern of more condensed genome structure in regions of high recombination. Based on the observed rates of small insertions and deletions and assuming that these rates are representative for the whole genome, we estimate that the genome of the most recent common ancestor of birds and lizards has lost nearly 20% of its DNA content up until the present. Expansion of transposable elements can counteract the effect of deletions in an equilibrium mutation model; however, since the activity of transposable elements has been low in the avian lineage, the deletion bias is likely to have had a significant effect on genome size evolution in dinosaurs and birds, contributing to the maintenance of a small genome. We also demonstrate that most of the observed correlations between recombination rate and genome contraction parameters are seen in the human genome, including for segregating indel polymorphisms. Our data are compatible with a neutral model in which recombination drives vertebrate genome size evolution and gives no direct support for a role of natural selection in this process.
Vyšlo v časopise:
Recombination Drives Vertebrate Genome Contraction. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002680
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002680
Souhrn
Selective and/or neutral processes may govern variation in DNA content and, ultimately, genome size. The observation in several organisms of a negative correlation between recombination rate and intron size could be compatible with a neutral model in which recombination is mutagenic for length changes. We used whole-genome data on small insertions and deletions within transposable elements from chicken and zebra finch to demonstrate clear links between recombination rate and a number of attributes of reduced DNA content. Recombination rate was negatively correlated with the length of introns, transposable elements, and intergenic spacer and with the rate of short insertions. Importantly, it was positively correlated with gene density, the rate of short deletions, the deletion bias, and the net change in sequence length. All these observations point at a pattern of more condensed genome structure in regions of high recombination. Based on the observed rates of small insertions and deletions and assuming that these rates are representative for the whole genome, we estimate that the genome of the most recent common ancestor of birds and lizards has lost nearly 20% of its DNA content up until the present. Expansion of transposable elements can counteract the effect of deletions in an equilibrium mutation model; however, since the activity of transposable elements has been low in the avian lineage, the deletion bias is likely to have had a significant effect on genome size evolution in dinosaurs and birds, contributing to the maintenance of a small genome. We also demonstrate that most of the observed correlations between recombination rate and genome contraction parameters are seen in the human genome, including for segregating indel polymorphisms. Our data are compatible with a neutral model in which recombination drives vertebrate genome size evolution and gives no direct support for a role of natural selection in this process.
Zdroje
1. CarvalhoABClarkAG 1999 Intron size and natural selection. Nature 401 344
2. ComeronJMKreitmanM 2000 The correlation between intron length and recombination in Drosophila: Dynamic equilibrium between mutational and selective forces. Genetics 156 1175 1190
3. ICGSC 2004 Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432 695 716
4. ComeronJMKreitmanM 2002 Population, evolutionary and genomic consequences of interference selection. Genetics 161 389 410
5. VinogradovAE 2004 Compactness of human housekeeping genes: selection for economy or genomic design? Trends in Genetics 20 248 253
6. VinogradovAE 2006 “Genome design” model: Evidence from conserved intronic sequence in human-mouse comparison. Genome Research 16 347 354
7. GregoryTR 2002 A bird's-eye view of the C-value enigma: Genome size, cell size, and metabolic rate in the class aves. Evolution 56 121 130
8. AndrewsCBMackenzieSAGregoryTR 2009 Genome size and wing parameters in passerine birds. Proceedings of the Royal Society B-Biological Sciences 276 55 61
9. LynchMConeryJS 2003 The origins of genome complexity. Science 302 1401 1404
10. PetrovDASangsterTAJohnstonJSHartlDLShawKL 2000 Evidence for DNA loss as a determinant of genome size. Science 287 1060 1062
11. PetrovDA 2002 Mutational equilibrium model of genome size evolution. Theoretical Population Biology 61 531 544
12. KongAGudbjartssonDFSainzJJonsdottirGMGudjonssonSA 2002 A high-resolution recombination map of the human genome. Nature Genetics 31 241 247
13. GroenenMAMWahlbergPFoglioMChengHHMegensHJ 2009 A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Research 19 510 519
14. BackstromNForstmeierWSchielzethHMelleniusHNamK 2010 The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Research 20 485 495
15. GregoryTR 2011 Animal Genome Size Database. http://www.genomesize.com
16. EllegrenH 2010 Evolutionary stasis: the stable chromosomes of birds. Trends in Ecology & Evolution 25 283 291
17. GriffinDKRobertsonLBWTempestHGSkinnerBM 2007 The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenetic and Genome Research 117 64 77
18. SjödinPBataillonTSchierupMH 2010 Insertion and deletion processes in recent human history. PLoS One 5 e8650
19. PetrovDALozovskayaERHartlDL 1996 High intrinsic rate of DNA loss in Drosophila. Nature 384 346 349
20. AbrusanGKrambeckHJJunierTGiordanoJWarburtonPE 2008 Biased distributions and decay of long interspersed nuclear elements in the chicken genome. Genetics 178 573 581
21. LiuGEJiangLTianFZhuBSongJZ 2009 Calibration of mutation rates reveals diverse subfamily structure of galliform CR1 repeats. Genome Biology and Evolution 1 119 130
22. VandergonTLReitmanM 1994 Evolution of chicken repeat 1 (CR1) elements: evidence for ancient subfamilies and multiple progenitors. Molecular Biology and Evolution 11 886 898
23. WickerTRobertsonJSSrSFeltusFAVM 2005 The repetitive landscape of the chicken genome. Genome Research 15 126 136
24. JeffreysAJNeumannR 2009 The rise and fall of a human recombination hot spot. Nature Genetics 41 625 629
25. PtakSEHindsDAKoehlerKNickelBPatilN 2005 Fine-scale recombination patterns differ between chimpanzees and humans. Nature Genetics 37 429 434
26. WincklerWMyersSRRichterDJOnofrioRCMcDonaldGJ 2005 Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308 107 111
27. WarrenWCClaytonDFEllegrenHArnoldAPHillierLW 2010 The genome of a songbird. Nature 464 757 762
28. NabholzBKunstnerAWangRJarvisEEllegrenH 2011 Dynamic evolution of base composition: causes and consequences in avian phylogenomics. Molecular Biology and Evolution 28 2197 2210
29. DalloulRALongJAZiminAVAslamLBealK 2010 Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis. PLoS Biology 8 e1000475
30. NamKMugalCNabholzBSchielzethHWolfJB 2010 Molecular evolution of genes in avian genomes. Genome Biology 11 R68
31. LunterGPontingCPHeinJ 2006 Genome-wide identification of human functional DNA using a neutral indel model. PLoS Computational Biology 2 e5
32. PetrovDAHartlDL 1998 High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Molecular Biology and Evolution 15 293 302
33. MillsREPittardWSMullaneyJMFarooqUCreasyTH 2011 Natural genetic variation caused by small insertions and deletions in the human genome. Genome Research 21 830 839
34. TaylorMSPontingCPCopleyRR 2004 Occurrence and consequences of coding sequence insertions and deletions in mammalian genomes. Genome Research 14 555 566
35. TajimaF 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 585 595
36. RomiguierJRanwezVDouzeryEJGaltierN 2010 Contrasting GC-content dynamics across 33 mammalian genomes: relationship with life-history traits and chromosome sizes. Genome Research 20 1001 1009
37. GregoryTR 2003 Is small indel bias a determinant of genome size? Trends in Genetics 19 485 488
38. OrganCLShedlockAMMeadeAPagelMEdwardsSV 2007 Origin of avian genome size and structure in non-avian dinosaurs. Nature 446 180 184
39. ShedlockAMBotkaCWZhaoSShettyJZhangT 2007 Phylogenomics of nonavian reptiles and the structure of the ancestral amniote genome. Proceedings of the National Academy of Sciences of the United States of America 104 2767 2772
40. BurtDW 2005 Chicken genome: Current status and future opportunities. Genome Research 15 1692 1698
41. EllegrenH 2005 The avian genome uncovered. Trends in Ecology & Evolution 20 180 186
42. BurtDW 2002 Origin and evolution of avian microchromosomes. Cytogenetic and Genome Research 96 97 112
43. QumsiyehMB 1994 Evolution of number and morphology of mammalian chromosomes. Journal of Heredity 85 455 465
44. BegunDJAquadroCF 1992 Levels of naturally-occurring DNA polymorphism correlate with recombination rates in Drosophila-melanogaster. Nature 356 519 520
45. LercherMJHurstLD 2002 Human SNP variability and mutation rate are higher in regions of high recombination. Trends in Genetics 18 337 340
46. NachmanMW 2001 Single nucleotide polymorphisms and recombination rate in humans. Trends in Genetics 17 481 485
47. NachmanMWBauerVLCrowellSLAquadroCF 1998 DNA variability and recombination rates at X-linked loci in humans. Genetics 150 1133 1141
48. HellmannIEbersbergerIPtakSEPaaboSPrzeworskiM 2003 A neutral explanation for the correlation of diversity with recombination rates in humans. American Journal of Human Genetics 72 1527 1535
49. KulathinalRJBennetttSMFitzpatrickCLNoorMAF 2008 Fine-scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. Proceedings of the National Academy of Sciences of the United States of America 105 10051 10056
50. CutterADMosesAM 2011 Polymorphism, divergence, and the role of recombination in Saccharomyces cerevisiae genome evolution. Molecular Biology and Evolution 28 1745 1754
51. HuangSWFriedmanRYuNYuALiWH 2005 How strong is the mutagenicity of recombination in mammals? (vol 22, pg 426, 2005). Molecular Biology and Evolution 22 1157 1157
52. KeinanAReichD 2010 Human population differentiation is strongly correlated with local recombination rate. PLoS Genetics 6 e1000886
53. NoorMA 2008 Mutagenesis from meiotic recombination is not a primary driver of sequence divergence between Saccharomyces species. Molecular Biology and Evolution 25 2439 2444
54. StevisonLSNoorMAF 2010 Genetic and evolutionary correlates of fine-scale recombination rate variation in Drosophila persimilis. Journal of Molecular Evolution 71 332 345
55. BebenekKKunkelTA 2004 Functions of DNA polymerases. DNA Repair and Replication 69 137 165
56. AlbertsonTMOgawaMBugniJMHaysLEChenY 2009 DNA polymerase epsilon and delta proofreading suppress discrete mutator and cancer phenotypes in mice. Proceedings of the National Academy of Sciences of the United States of America 106 17101 17104
57. FortuneJMPavlovYIWelchCMJohanssonEBurgersPMJ 2005 Saccharomyces cerevisiae DNA polymerase delta - High fidelity for base substitutions but lower fidelity for single- and multi-base deletions. Journal of Biological Chemistry 280 29980 29987
58. HicksWM 2010 Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329 82 85
59. SchmittMWMatsumotoYLoebLA 2009 High fidelity and lesion bypass capability of human DNA polymerase delta. Biochimie 91 1163 1172
60. MaloiselLFabreFGangloffS 2008 DNA polymerase delta is preferentially recruited during homologous recombination to promote heteroduplex DNA extension. Molecular and Cellular Biology 28 1373 1382
61. OliverJLBernaola-GalvanPCarpenaPRoman-RoldanR 2001 Isochore chromosome maps of eukaryotic genomes. Gene 276 47 56
62. BernardiGCostantiniMAulettaF 2007 Isochore patterns and gene distributions in fish genomes. Genomics 90 364 371
63. CarelsNBernardiG 2000 The compositional organization and the expression of the Arabidopsis genome. FEBS Letters 472 302 306
64. AdamsMDCelnikerSEHoltRAEvansCAGocayneJD 2000 The genome sequence of Drosophila melanogaster. Science 287 2185 2195
65. VersteegRvan SchaikBDCvan BatenburgMFRoosMMonajemiR 2003 The human transcriptome map reveals extremes in gene density, intron length, GC content, and repeat pattern for domains of highly and weakly expressed genes. Genome Research 13 1998 2004
66. DuretLMouchiroudDGautierC 1995 Statistical analysis of vertebrate sequences reveals that long genes are scarce in GC-rich isochores. Journal of Molecular Evolution 40 308 317
67. BernardiG 1995 The human genome: Organization and evolutionary history. Annual Review of Genetics 29 445 476
68. DuretLGaltierN 2009 Biased gene conversion and the evolution of mammalian genomic landscapes. Annual Review of Genomics and Human Genetics 10 285 311
69. MaraisG 2003 Biased gene conversion: implications for genome and sex evolution. Trends in Genetics 19 330 338
70. MeunierJDuretL 2004 Recombination drives the evolution of GC-content in the human genome. Molecular Biology and Evolution 21 984 990
71. GaltierNPiganeauGMouchiroudDDuretL 2001 GC-content evolution in mammalian genomes: The biased gene conversion hypothesis. Genetics 159 907 911
72. SmukowskiCSNoorMAF 2011 Recombination rate variation in closely related species. Heredity 107 496 508
73. KvikstadEMTyekuchevaSChiaromonteFMakovaKD 2007 A macaque's-eye view of human insertions and deletions: Differences in mechanisms. PLoS Computational Biology 3 1772 1782
74. PollardKSHubiszMJRosenbloomKRSiepelA 2010 Detection of nonneutral substitution rates on mammalian phylogenies. Genome Research 20 110 121
75. MakovaKDYangSChiaromonteF 2004 Insertions and deletions are male biased too: A whole-genome analysis in rodents. Genome Research 14 567 573
76. SmitAHubleyRGreenP 1996–2004 (1996–2004) RepeatMasker http://www.repeatmasker.org
77. JurkaJ 2000 Repbase Update - a database and an electronic journal of repetitive elements. Trends in Genetics 16 418 420
78. YangZH 2007 PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24 1586 1591
79. ChurakovGGrundmannNKuritzinABrosiusJMakalowskiW 2010 A novel web-based TinT application and the chronology of the Primate Alu retroposon activity. BMC Evolutionary Biology 10 376
80. BatesDMSarkarD 2007 lme4: Linear mixed-effects models using S4 classes. pp. R package version 0.9975-9912
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 5
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Inactivation of a Novel FGF23 Regulator, FAM20C, Leads to Hypophosphatemic Rickets in Mice
- Genome-Wide Association of Pericardial Fat Identifies a Unique Locus for Ectopic Fat
- Slowing Replication in Preparation for Reduction
- An Essential Role for Katanin p80 and Microtubule Severing in Male Gamete Production