Footprints of X-to-Y Gene Conversion in Recent Human Evolution

Molecular Biology and Evolution

Volumn 27, Issue 3, 2010, Pages 714-725

  Trombetta, Beniamino ^a   Cruciani, Fulvio ^a   Underhill, Peter A ^b   Sellitto, Daniele ^c   Scozzari, Rosaria ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CNR   (Italy)

Author keywords

DbSNP; Gene conversion hot spot; Human sex chromosomes; MSY; Segmental duplications

Indexed keywords

GENOMIC DNA; PALINDROMIC DNA;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; EVOLUTION; GENE; GENE CONVERSION; GENE SEQUENCE; HUMAN; MAJOR CLINICAL STUDY; MALE; PARALOGY; PCDH11Y GENE; POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TBL1Y GENE; VCY GENE; Y CHROMOSOME;

CADHERINS; CHROMOSOMES, HUMAN, X; CHROMOSOMES, HUMAN, Y; DNA MUTATIONAL ANALYSIS; EVOLUTION, MOLECULAR; GENE CONVERSION; HUMANS; NUCLEAR PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSDUCIN;

EID: 77249085126     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp231     Document Type: Article

References (62)

1. Adams SM, King TE, Bosch E, Jobling MA. 2006. The case of the unreliable SNP: recurrent back-mutation of Y-chromosomal marker P25 through gene conversion. Forensic Sci Int. 159: 14-20.
2. Armengol L, Pujana MA, Cheung J, Scherer SW, Estivill X. 2003. Enrichment of segmental duplications in regions of breaks of synteny between the human and mouse genomes suggest their involvement in evolutionary rearrangements. Hum Mol Genet. 12:2201-2208.
3. Arnheim N, Calabrese P, Tiemann-Boege I. 2007. Mammalian meiotic recombination hot spots. Annu Rev Genet. 41:369-399.
4. Bailey JA, Eichler EE. 2006. Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet. 7:552-564.
5. Bailey JA, Gu Z, Clark RA, Reinert K, Samonte RV, Schwartz S, Adams MD, Myers EW, Li PW, Eichler EE. 2002. Recent segmental duplications in the human genome. Science 297: 1003-1007.
6. Bailey JA, Yavor AM, Massa HF, Trask BJ, Eichler EE. 2001. Segmental duplications: organization and impact within the current human genome project assembly. Genome Res. 11:1005-1017.
7. Benovoy D, Drouin G. 2009. Ectopic gene conversions in the human genome. Genomics 93:27-32.
8. Bhowmick BK, Satta Y, Takahata N. 2007. The origin and evolution of human ampliconic gene families and ampliconic structure. Genome Res. 17:441-450.
9. Bosch E, Hurles ME, Navarro A, Jobling MA. 2004. Dynamics of a human interparalog gene conversion hotspot. Genome Res. 14:835-844.
10. Bussaglia E, Clermont O, Tizzano E, et al. (11 co-authors). 1995. A frame-shift deletion in the survival motor neuron gene in Spanish spinal muscular atrophy patients. Nat Genet. 11:335-337.
11. Chen DC, Saarela J, Clark RA, Miettinen T, Chi A, Eichler EE, Peltonen L, Palotie A. 2004. Segmental duplications flank the multiple sclerosis locus on chromosome 17q. Genome Res. 14:1483-1492.
12. Chen J-M, Cooper DN, Chuzhanova N, Férec C, Patrinos GP. 2007. Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet. 8:762-775.
13. Chen J-M, Férec C, Cooper DN. 2009. Closely spaced multiple mutations as potential signatures of transient hypermutability in human genes. Hum Mutat. 30:1435-1448.
14. Cheng Z, Ventura M, She X, et al. (12 co-authors). 2005. A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature 437:88-93.
15. Cheung J, Estivill X, Khaja R, MacDonald JR, Lau K, Tsui L-C, Scherer SW. 2003. Genome-wide detection of segmental duplications and potential assembly errors in the human genome sequence. Genome Biol. 4:R25.
16. Cruciani F, La Fratta R, Santolamazza P, et al. (19 co-authors). 2004. Phylogeographic analysis of haplogroup E3b (E-M215) Y chromosomes reveals multiple migratory events within and out of Africa. Am J Hum Genet. 74:1014-1022.
17. Cruciani F, La Fratta R, Torroni A, Underhill PA, Scozzari R. 2006. Molecular dissection of the Y chromosome haplogroup E-M78 (E3b1a): a posteriori evaluation of a microsatellite-network-based approach through six new biallelic markers. Hum Mutat. 27:831-832.
18. Cruciani F, La Fratta R, Trombetta B, et al. (24 co-authors). 2007. Tracing past human male movements in northern/eastern Africa and western Eurasia: new clues from Y-chromosomal haplogroups E-M78 and J-M12. Mol Biol Evol. 24:1300-1311.
19. Cruciani F, Santolamazza P, Shen P, et al. (16 co-authors). 2002. A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes. Am J Hum Genet. 70:1197-1214.
20. Eichler EE. 2001. Recent duplication, domain accretion and the dynamic mutation of the human genome. Trends Genet. 17: 661-669.
21. Eickbush TH, Eickbush DG. 2007. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477-485.
22. Estivill X, Cheung J, Pujana MA, Nakabayashi K, Scherer SW, Tsui L-C. 2002. Chromosomal regions containing high-density and ambig uously mapped putative single nucleotide polymorphisms (SNPs) correlate with segmental duplications in the human genome. Hum Mol Genet. 11:1987-1995.
23. Garcia-Moreno J, Mindell DP. 2000. Rooting a phylogeny with homologous genes on opposite sex chromosomes (gametologs): a case study using avian CHD. Mol Biol Evol. 17:1826-1832.
24. Giordano M, Marchetti C, Chiorboli E, Bona G, Momigliano Richiardi P. 1997. Evidence for gene conversion in the generation of extensive polymorphism in the promoter of the growth hormone gene. Hum Genet. 100:249-255.
25. Gupta PK, Adamtziki E, Budde U, et al. (12 co-authors). 2005. Gene conversions are a common cause of von Willebrand disease. Br J Haematol. 130:752-758.
26. Hallast P, Nagirnaja L, Margus T, Laan M. 2005. Segmental duplications and gene conversion: human luteinizing hor-mone/chorionic gonadotropin b gene cluster. Genome Res. 15: 1535-1546.
27. Hammer MF, Blackmer F, Garrigan D, Nachman MW, Wilder JA. 2003.Human population structure and its effects on sampling Y chromosome sequence variation. Genetics 164:1495-1509.
28. Hurles M. 2002. Are 100,000 "SNPs" useless? Science 298:1509a.
29. Hurles ME, Willey D, Matthews L, Hussain SS. 2004. Origin of chromosomal rearrangement hotspots in the human genome: evidence from the AZFa deletion hotspots. Genome Biol. 5:R55
30. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921
31. International SNP Map Working Group. 2001. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409:928-933.
32. Karafet TM, Mendez FL, Meilerman MB, Underhill PA, Zegura SL, Hammer MF. 2008. New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res. 18:830-838.
33. Lahn BT, Page DC. 1999. Four evolutionary strata on the human X chromosome. Science 286:964-967.
34. Lahn BT, Page DC. 2000. A human sex-chromosomal gene family expressed in male germ cells and encoding variably charged proteins. Hum Mol Genet. 9:311-319.
35. Larkin MA, Blackshields G, Brown NP, et al. (13 co-authors). 2007. ClustalW and ClustalX version 2.0. Bioinformatics 23:2947-2948.
36. Lemaitre C, Braga MDV, Gautier C, Sagot M-F, Tannier E, Marais GAB. 2009. Footprints of inversions at present and past pseudoautosomal boundaries in human sex chromosomes. Genome Biol Evol. 1:56-66.
37. Li W-H, Wu C-I, Luo C-C. 1984. Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J Mol Evol. 21:58-71.
38. Marais G, Galtier N. 2003. Sex chromosomes: how X-Y recombination stops. Curr Biol. 13:R641-R643.
39. Nei M. 1987. Molecular evolutionary genetics. New York: Columbia University Press.
40. Pentao L, Wise CA, Chinault AC, Patel PI, Lupski JR. 1992. Charcot-Marie-Tooth type 1A duplication appears to arise from recombination at repeat sequences flanking the 1.5 Mb monomer unit. Nat Genet. 2:292-300.
41. Ptak SE, Roeder AD, Stephens M, Gilad Y, Pääbo S, Przeworski M. 2004.Absence of the TAP2 human recombination hotspot in chimpanzees. PLoS Biol. 2:849-855.
42. Repping S,van Daalen SKM, Brown LG, et al. (11 co-authors). 2006. High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nat Genet. 38:463-467.
43. Reyniers E, Van Thienen M-N, Meire F, De Boulle K, Devries K, Kestelijn P, Willems PJ. 1995. Gene conversion between red and defective green opsin gene in blue cone monochromacy. Genomics 29:323-328.
44. Roesler J, Curnutte JT, Rae J, Barrett D, Patino P, Chanock SJ, Goerlach A. 2000. Recombination events between the p47-phox gene and its highly homologous pseudogenes are the main cause of autosomal recessive chronic granulomatous disease. Blood 95:2150-2156.
45. Ross MT, Grafham DV, Coffey AJ, etal. (282 co-authors). 2005. The DNA sequence of the human X chromosome. Nature 434:325-337.
46. Rosser ZH, Balaresque P, Jobling M.A. 2009. Gene conversion between the X chromosome and the male-specific region of the Ychromosome at a translocation hotspot. Am J Hum Genet. 85:130-134.
47. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497.
48. Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Page DC. 2003. Abundant gene conversion between arms of palindromes in human and ape Ychromosomes. Nature 423:873-876.
49. Samonte RV, Eichler EE. 2002. Segmental duplications and the evolution of the primate genome. Nat Rev Genet. 3:65-72.
50. She X, Jiang Z, Clark RA, Liu G, Cheng Z, Tuzun E, Church DM, Sutton G, Halpern AL, Eichler EE. 2004. Shotgun sequence assembly and recent segmental duplications within the human genome. Nature 431:927-930.
51. Shen P, Wang F, Underhill PA, et al. (13 co-authors). 2000. Population genetic implications from sequence variation in four Y chromosome genes. Proc Natl Acad Sci USA. 97:7354-7359.
52. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, et al. (40 co-authors). 2003. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825-837.
53. Slattery JP, Sanner-Wachter L, O'Brien SJ. 2000. Novel gene conversion between X-Y homologues located in the non-recombining region of the Y chromosome in Felidae (Mammalia). Proc Natl Acad Sci USA. 97:5307-5312.
54. Stankiewicz P, Shaw CJ, Withers M, Inoue K, Lupski JR. 2004. Serial segmental duplications during primate evolution result in complex human genome architecture. Genome Res. 14:2209-2220.
55. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
56. Underhill PA, Passarino G, Lin AA, Shen P, Mirazón Lahr M, Foley RA, Oefner PJ, Cavalli-Sforza LL. 2001. The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann Hum Genet. 65:43-62.
57. Underhill PA, Shen P, Lin AA, et al. (21 co-authors). 2000. Y chromosome sequence variation and the history of human populations. Nat Genet. 26:358-361. (Pubitemid 30824621)
58. Van Esch H, Hollanders K, Badisco L, Melotte C, Van Hummelen P, Vermeesch JR, Devriendt K, Fryns J-P, Marynen P, Froyen G. 2005. Deletion of VCX-A due to NAHR plays a major role in the occurrence of mental retardation in patients with X-linked ichthyosis. Hum Mol Genet. 14:1795-1803.
59. Vázquez N, Lehrnbecher T, Chen R, Christensen BL, Gallin JI, Malech H, Holland S, Zhu S, Chanock SJ. 2001. Mutational analysis of patients with p47-phox-deficient chronic granulo-matous disease: the significance of recombination events between the p47-phox gene (NCF1) and its highly homologous pseudogenes. Exp Hematol. 29:234-243.
60. Visser R, Shimokawa O, Harada N, Kinoshita A, Ohta T, Niikawa N, Matsumoto N. 2005. Identification of a 3.0-Kb major recombination hotspot in patients with Sotos syndrome who carry a common 1.9-Mb microdelection. Am J Hum Genet. 76:52-67.
61. Winckler W, Myers SR, Richter DJ, et al. (11 co-authors). 2005. Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308:107-111.
62. Zhang L, Lu HHS, Chung W-y, Yang J, Li W-H. 2005. Patterns of segmental duplication in the human genome. Mol Biol Evol. 22:135-141.