Gene Conversion Violates the Stepwise Mutation Model for Microsatellites in Y-Chromosomal Palindromic Repeats

Human Mutation

Volumn 35, Issue 5, 2014, Pages 609-617

  Balaresque, Patricia ^a,b   King, Turi E ^b   Parkin, Emma J ^b   Heyer, Evelyne ^c   Carvalho Silva, Denise ^d   Kraaijenbrink, Thirsa ^e   de Knijff, Peter ^e   Tyler Smith, Chris ^d   Jobling, Mark A ^b  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c Université Diderot Paris 7   (France)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

DYS385; Gene conversion; Microsatellite; Palindrome; Stepwise mutation model; Y chromosome

Indexed keywords

MICROSATELLITE DNA; PALINDROMIC DNA; REPETITIVE DNA;

ALLELE; ARTICLE; CAPILLARY ELECTROPHORESIS; CHROMOSOME DUPLICATION; CONTROLLED STUDY; GENE CONVERSION; GENE MUTATION; HAPLOTYPE; HUMAN; MALE; MUTATION RATE; PRIORITY JOURNAL; Y CHROMOSOME; BIOLOGICAL MODEL; GENETICS; INVERTED REPEAT; MUTATION;

CHROMOSOMES, HUMAN, Y; GENE CONVERSION; HUMANS; INVERTED REPEAT SEQUENCES; MICROSATELLITE REPEATS; MODELS, GENETIC; MUTATION;

EID: 84898824257     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22542     Document Type: Article

References (44)

1. Balaresque P. 2007. Microsatellites or the eukaryotic genome: life cycle concept and neutrality issues. Med Sci (Paris) 23:729-734.
2. Balaresque P, Bowden GR, Adams SM, Leung H-Y, King TE, Rosser ZH, Goodwin J, Moisan J-P, Richard C, Demaine AG, Wilson IJ, Tyler-Smith C, et al. 2010. A predominantly Neolithic origin for European paternal lineages. PLoS Biol 8:e1000285.
3. Balaresque P, Sibert A, Heyer E, Crouau-Roy B. 2007. Unbiased interpretation of haplotypes at duplicated microsatellites. Ann Hum Genet 71:209-219.
4. Balaresque P, Toupance B, Heyer E, Crouau-Roy B. 2003. Evolutionary dynamics of duplicated microsatellites shared by sex chromosomes. J Mol Evol 57(Suppl 1):S128-S137.
5. Ballantyne KN, Goedbloed M, Fang R, Schaap O, Lao O, Wollstein A, Choi Y, van Duijn K, Vermeulen M, Brauer S, Decorte R, Poetsch M, et al. 2010. Mutability of Y-chromosomal microsatellites: rates, characteristics, molecular bases, and forensic implications. Am J Hum Genet 87:341-353.
6. Ballantyne KN, Keerl V, Wollstein A, Choi Y, Zuniga SB, Ralf A, Vermeulen M, de Knijff P, Kayser M. 2012. A new future of forensic Y-chromosome analysis: rapidly mutating Y-STRs for differentiating male relatives and paternal lineages. Forensic Sci Int Genet 6:208-218.
7. Ballard DJ, Phillips C, Wright G, Thacker CR, Robson C, Revoir AP, Court DS. 2005. A study of mutation rates and the characterisation of intermediate, null and duplicated alleles for 13 Y chromosome STRs. Forensic Sci Int 155:65-70.
8. Bianchi NO, Catanesi CI, Bailliet G, Martinez-Marignac VL, Bravi CM, Vidal-Rioja LB, Herrera RJ, López-Camelo JS. 1998. Characterization of ancestral and derived Y-chromosome haplotypes of new world native populations. Am J Hum Genet 63:1862-1871.
9. Bosch E, Calafell F, González-Neira A, Flaiz C, Mateu E, Scheil H-G, Huckenbeck W, Efremovska L, Mikerezi I, Xirotiris N, Grasa C, Schmidt H, et al. 2006. Male and female lineages in the Balkans show a homogeneous landscape over linguistic barriers, except for the isolated Aromuns. Ann Hum Genet 70:459-487.
10. Budowle B, Adamowicz M, Aranda XG, Barna C, Chakraborty R, Cheswick D, Dafoe B, Eisenberg A, Frappier R, Gross AM, Ladd C, Lee HS, et al. 2005. Twelve short tandem repeat loci Y chromosome haplotypes: genetic analysis on populations residing in North America. Forensic Sci Int 150:1-15.
11. Buschiazzo E, Gemmell NJ. 2006. The rise, fall and renaissance of microsatellites in eukaryotic genomes. Bioessays 28:1040-1050.
12. Butler JM, Schoske R, Vallone PM, Kline MC, Redd AJ, Hammer MF. 2002. A novel multiplex for simultaneous amplification of 20 Y chromosome STR markers. Forensic Sci Int 129:10-24.
13. de Souza Goes AC, de Carvalho EF, Gomes I, da Silva DA, Gil EH, Amorim A, Gusmao L. 2005. Population and mutation analysis of 17 Y-STR loci from Rio de Janeiro (Brazil). Int J Legal Med 119:70-76.
14. Decker AE, Kline MC, Redman JW, Reid TM, Butler JM. 2008. Analysis of mutations in father-son pairs with 17 Y-STR loci. Forensic Sci Int Genet 2:e31-e35.
15. Domingues PM, Gusmao L, da Silva DA, Amorim A, Pereira RW, de Carvalho EF. 2007. Sub-Saharan Africa descendents in Rio de Janeiro (Brazil): population and mutational data for 12 Y-STR loci. Int J Legal Med 121:238-241.
16. Dupuy BM, Stenersen M, Egeland T, Olaisen B. 2004. Y-chromosomal microsatellite mutation rates: differences in mutation rate between and within loci. Hum Mutat 23:117-124.
17. Gusmão L, Butler JM, Carracedo A, Gill P, Kayser M, Mayr WR, Morling N, Prinz M, Roewer L, Tyler-Smith C, Schneider PM. 2006. DNA commission of the International Society of Forensic Genetics (ISFG): an update of the recommendations on the use of Y-STRs in forensic analysis. Forensic Sci Int 157:187-197.
18. Gusmão L, Sanchez-Diz P, Calafell F, Martin P, Alonso CA, Alvarez-Fernandez F, Alves C, Borjas-Fajardo L, Bozzo WR, Bravo ML, Builes JJ, Capilla J, et al. 2005. Mutation rates at Y chromosome specific microsatellites. Hum Mutat 26:520-528.
19. Hallast P, Balaresque P, Bowden GR, Ballereau SJ, Jobling MA. 2013. Recombination dynamics of a human Y-chromosomal palindrome: rapid GC-biased gene conversion, multi-kilobase conversion tracts, and rare inversions. PLoS Genet 9:e1003666.
20. Hohoff C, Dewa K, Sibbing U, Hoppe K, Forster P, Brinkmann B. 2007. Y-chromosomal microsatellite mutation rates in a population sample from northwestern Germany. Int J Legal Med 121:359-363.
21. Kayser M, Roewer L, Hedman M, Henke L, Henke J, Brauer S, Krüger C, Krawczak M, Nagy M, Dobosz T, Szibor R, de Knijff P, et al. 2000. Characteristics and frequency of germline mutations at microsatellite loci from the human Y chromosome, as revealed by direct observation in father/son pairs. Am J Hum Genet 66: 1580-1588.
22. King TE, Jobling MA. 2009a. Founders, drift and infidelity: the relationship between Y chromosome diversity and patrilineal surnames. Mol Biol Evol 26:1093-1102.
23. King TE, Jobling MA. 2009b. What's in a name? Y chromosomes, surnames and the genetic genealogy revolution. Trends Genet 25:351-360.
24. Kittler R, Erler A, Brauer S, Stoneking M, Kayser M. 2003. Apparent intrachromosomal exchange on the human Y chromosome explained by population history. Eur J Hum Genet 11:304-314.
25. Kraaijenbrink T, Parkin EJ, Carvalho-Silva DR, van Driem GL, Barbujani G, Tyler-Smith C, Jobling MA, de Knijff P. 2009. Genetic and linguistic borders in the Himalayan Region. In: d'Errico F, Hombert J-M, editors. Becoming eloquent: advances in the emergence of language, human cognition and modern cultures. Amsterdam, The Netherlands: John Benjamins Publishing Company. p 181-201.
26. Kurihara R, Yamamoto T, Uchihi R, Li SL, Yoshimoto T, Ohtaki H, Kamiyama K, Katsumata Y. 2004. Mutations in 14 Y-STR loci among Japanese father-son haplotypes. Int J Legal Med 118:125-131.
27. Lee HY, Park MJ, Chung U, Yang WI, Cho SH, Shin KJ. 2007. Haplotypes and mutation analysis of 22 Y-chromosomal STRs in Korean father-son pairs. Int J Legal Med 121:128-135.
28. Malyarchuk B, Derenko M, Denisova G, Wozniak M, Grzybowski T, Dambueva I, Zakharov I. 2010. Phylogeography of the Y-chromosome haplogroup C in northern Eurasia. Ann Hum Genet 74:539-546.
29. Messier W, Li SH, Stewart CB. 1996. The birth of microsatellites. Nature 381:483.
30. Ohta T, Kimura M. 1973. A model of mutation appropriate to estimate the number of electrophoretically detectable molecules in a finite population. Genet Res 22:201-204.
31. Paracchini S, Arredi B, Chalk R, Tyler-Smith C. 2002. Hierarchical high-throughput SNP genotyping of the human Y chromosome using MALDI-TOF mass spectrometry. Nucleic Acids Res 30:e27.
32. Parkin EJ, Kraayenbrink T, Opgenort JR, van Driem GL, Tuladhar NM, de Knijff P, Jobling MA. 2007. Diversity of 26-locus Y-STR haplotypes in a Nepalese population sample: isolation and drift in the Himalayas. Forensic Sci Int 166:176-181.
33. Parkin EJ, Kraayenbrink T, van Driem GL, Tshering K, de Knijff P, Jobling MA. 2006. 26-locus Y-STR typing in a Bhutanese population sample. Forensic Sci Int 161:1-7.
34. Rose O, Falush D. 1998. A threshold size for microsatellite expansion. Mol Biol Evol 15:613-615.
35. Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Page DC. 2003. Abundant gene conversion between arms of massive palindromes in human and ape Y chromosomes. Nature 423:873-876.
36. Schlotterer C. 2000. Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365-371.
37. Segurel L, Martinez-Cruz B, Quintana-Murci L, Balaresque P, Georges M, Hegay T, Aldashev A, Nasyrova F, Jobling MA, Heyer E, Vitalis R. 2008. Sex-specific genetic structure and social organization in Central Asia: insights from a multi-locus study. PLoS Genet 4:e1000200.
38. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova R, Ali J, Bieri T, Chinwalla A, Delehaunty A, et al. 2003. The male-specific region of the human Y chromosome: a mosaic of discrete sequence classes. Nature 423:825-837.
39. Sun C, Skaletsky H, Birren B, Devon K, Tang Z, Silber S, Oates R, Page DC. 1999. An azoospermic man with a de novo point mutation in the Y-chromosomal gene USP9Y. Nat Genet 23:429-432.
40. Sun JX, Helgason A, Masson G, Ebenesersdottir SS, Li H, Mallick S, Gnerre S, Patterson N, Kong A, Reich D, Stefansson K. 2012. A direct characterization of human mutation based on microsatellites. Nat Genet 44:1161-1165.
41. Taylor JS, Durkin JM, Breden F. 1999. The death of a microsatellite: a phylogenetic perspective on microsatellite interruptions. Mol Biol Evol 16:567-572.
42. Turrina S, Atzei R, De Leo D. 2006. Y-chromosomal STR haplotypes in a Northeast Italian population sample using 17plex loci PCR assay. Int J Legal Med 120:56-59.
43. Wilson IJ, Balding DJ. 1998. Genealogical inference from microsatellite data. Genetics 150:499-510.
44. Y Chromosome Consortium. 2002. A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res 12:339-348.