Heterozygosity and mutation rate: Evidence for an interaction and its implications - The potential for meiotic gene conversions to influence both mutation rate and distribution

BioEssays

Volumn 32, Issue 1, 2010, Pages 82-90

  Amos, William ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Evolution; Heterozygosity; Microsatellite; Mutation rate; Population genetics

Indexed keywords

ISOENZYME; MICROSATELLITE DNA;

CROSSING OVER; DNA REPLICATION; GENE CONVERSION; GENE LINKAGE DISEQUILIBRIUM; HETEROZYGOSITY; HUMAN; MICROSATELLITE INSTABILITY; MUTATION RATE; NATURAL SELECTION; NONHUMAN; POINT MUTATION; POPULATION GENETICS; POPULATION SIZE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; EVOLUTION; GENE CONVERSION; GENETICS, POPULATION; GENOMIC INSTABILITY; HETEROZYGOTE; HUMANS; ISOENZYMES; MEIOSIS; MICROSATELLITE REPEATS; MODELS, GENETIC; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

EID: 74949098361     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.200900108     Document Type: Review

References (99)

1. Kimura M, Ohta T. 1978. Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75: 2868-72.
2. Schug MD, Mackay TFC, Aquadro CF. 1997. Low mutation rates of microsatellites in Drosophila melanogaster. Nat Genet 15: 99-102.
3. Beaumont MA. 2004. Recent developments in genetic data analysis: What can they tell us about human demographic history? Heredity 92: 365-79.
4. Zhivotovsky LA, Feldman MW, Grishechkin SA. 1997. Biased mutation and microsatellite variation. Mol Biol Evol 14: 926-33.
5. Hammer MF, Karafet T, Rasanayagam A, et al. 1998. Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol Biol Evol 15: 427-41.
6. Roewer L, Croucher PJP, Willuweit S, et al. 2005. Signature of recent historical events in the European Y-chromosomal STR haplotype distribution. Hum Genet 116: 279-91.
7. He Q, Cederberg H, Rannug U. 2002. The influence of sequence divergence between alleles of the human MS205 minisatellite incorporated into the yeast genome on length mutation rates and lethal recombination events during meiosis. J Mol Biol 319: 315-27.
8. Jauert PA, Kirkpatrick DT. 2005. Length and sequence heterozygosity differentially affect HRAS1 minisatellite stability during meiosis in yeast. Genetics 170: 601-12.
9. Collins I, Newlon CS. 1994. Meiosis-specific formation of joint DNA molecules containing sequences from homologous chromosomes. Cell 76: 65-75.
10. Nag DK, Scherthan H, Rockmill B, et al. 1995. Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 141: 75-86.
11. Lichten M, Goyon C, Schultes NP, et al. 1990. Detection of heteroduplex DNA molecules among the products of Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci USA 87: 7653-7.
12. Merker JD, Dominska M, Petes TD. 2003. Patterns of heteroduplex DNA formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 165: 47-63.
13. Borts RH, Haber JE. 1989. Length and distribution of meiotic gene conversion tracts and crossovers in Saccharomyces cerevisiae. Genetics 123: 69-80.
14. Borts RH, Leung W-Y, Kramer W, et al. 1990. Mismatch repair-induced meiotic recombination requires the PMS1 gene product. Genetics 124: 573-84.
15. Bishop AJR, Louis EJ, Borts RH. 2000. Minisatellite variants generated in yeast meiosis involve DNA removal during gene conversion. Genetics 156: 7-20.
16. Baker SM, Bronner CE, Zhang L, et al. 1995. Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 82: 309-19.
17. Manivasakam P, Rosenberg SM, Hastings PJ. 1996. Poorly repaired mismatches in heteroduplex DNA are hyper-recombinagenic in Saccharomyces cerevisiae. Genetics 142: 407-16.
18. Baker SM, Plug AW, Prolla TA, et al. 1996. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13: 336-42.
19. Koboldt DC, Miller RD, Kwok P-Y. 2006. Distribution of human SNPs and its effect on high throughput genotyping. Hum Mut 27: 249-54.
20. Wilding CS, Weetman D, Steen K, et al. 2009. High, clustered, nucleotide diversity in the genome of Anopheles gambiae revealed through pooled-template sequencing: implications for high-throughput genotyping protocols. BMC Genomics 10: 320.
21. Kolodner R. 1996. Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev 10: 1433-42.
22. Quintana JE, Neuwirth EAH, Grosovsky AJ. 2001. Interchromosomal gene conversion at an endogenous human cell locus. Genetics 158: 757-67.
23. Kibota TT, Lynch M. 1996. Estimates of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381: 694-6.
24. Barton NH, Halliday RB, Hewitt GM. 1983. Rare electrophoretic variants in a hybrid zone. Heredity 50: 139-46.
25. Bradley RD, Bull JJ, Johnson AD, et al. 1993. Origin of a novel allele in a mammalian hybrid zone. Proc Natl Acad Sci USA 90: 8939-41.
26. Woodruff RC. 1989. Genetic anomalies associated with Cerion hybrid zones: the origin and maintenance of new electrophoretic variants called hybrizymes. Biol J Linn Soc 36: 281-94.
27. Romanovsky MG, Ryabokon SM. 1992. Individual heterozygosity as a mutagenic factor. Genetika 28: 88-97.
28. Rubinsztein DC, Amos W, Leggo J, et al. 1995. Microsatellites are generally longer in humans compared to their homologues in non-human primates: evidence for directional evolution at microsatellite loci. Nat Genet 10: 337-43.
29. Crawford A, Knappes SM, Paterson KA, et al. 1998. Microsatellite evolution: testing the ascertainment bias hypothesis. J Mol Evol 46: 256-60.
30. Amos W, Hutter CM, Schug MD, et al. 2003. Directional evolution of size coupled with ascertainment bias for variation in Drosophila microsatellites. Mol Biol Evol 20: 660-2.
31. Primmer CR, Ellegren H. 1998. Patterns of molecular evolution in avian microsatellites. Mol Biol Evol 15: 997-1008.
32. Vigouroux Y, Matsuoka Y, Doebley J. 2003. Directional evolution for microsatellite size in maize. Mol Biol Evol 20: 1480-3.
33. Ellegren H, Primmer CR, Sheldon BC. 1995. Microsatellite evolution: directionality or bias in locus selection. Nat Genet 11: 360-2.
34. Cooper G, Rubinsztein DC, Amos W. 1998. Ascertainment bias does not entirely account for human microsatellites being longer than their chimpanzee homologues. Hum Mol Genet 7: 1425-9.
35. Vowles EJ, Amos W. 2006. Quantifying ascertainment bias and species-specific length differences in human and chimpanzee microsatellites using genome sequences. Mol Biol Evol 23: 598-607.
36. Primmer CR, Saino N, Møller AP, et al. 1998. Unravelling the process of microsatellite evolution through analysis of germ line mutations in barn swallows Hirundo rustica. Mol Biol Evol 15: 1047-54.
37. Amos W, Sawcer SJ, Feakes R, et al. 1996. Microsatellites show mutational bias and heterozygote instability. Nat Genet 13: 390-1.
38. Xu X, Peng M, Fang Z, et al. 2000. The direction of microsatellite mutations is dependent upon allele length. Nat Genet 24: 396-9.
39. Huang J, Papadopoulos N, McKinley AJ, et al. 1998. APC mutations in colorectal tumors with mismatch repair deficiency. Proc Natl Acad Sci USA 93: 9049-54.
40. Cooper G, Burroughs NJ, Rand DA, et al. 1999. Markov Chain Monte Carlo analysis of human Y-chromosome microsatellites provides evidence of biased mutation. Proc Natl Acad Sci USA 96: 11916-21.
41. Ellegren H. 2000. Heterogeneous mutation processes in human microsatellites. Nat Genet 24: 400-2.
42. Yamada NA, Smith GA, Castro A, et al. 2002. Relative rates of insertion and deletion mutations in dinucleotide repeats of various lengths in mismatch repair proficient mouse and mismatch deficient human cells. Mut Res 499: 213-25.
43. Huang Q-Y, Xu F-H, Shen H, et al. 2002. Mutations patterns at dinucleotide microsatellite loci in humans. Am J Hum Genet 70: 625-34.
44. Brinkmann B, Klintschar M, Neuhuber F, et al. 1998. Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. Am J Hum Genet 62: 1408-15.
45. Kayser M, Vowles EJ, Kappei D, et al. 2006. Microsatellite length differences between humans and chimpanzees at autosomal but not Y-chromosomal loci. Genetics 173: 2179-86.
46. Jeffreys AJ, Wilson V, Thein SL. 1985. Hypervariable 'minisatellite' regions in human DNA. Nature 314: 67-73.
47. Jeffreys AJ, MacLeod A, Tamaki K, et al. 1991. Minisatellite repeat coding as a digital approach to DNA typing. Nature 354: 204-9.
48. Vergnaud G, Mariat D, Apion F, et al. 1991. The use of synthetic tandem repeats to isolate new VNTR loci - cloning of a human hypermutable sequence. Genomics 11: 135-44.
49. Buard J, Bourdet A, Yardley J, et al. 1998. Influences of array size and homogeneity on minisatellite mutation. EMBO J 17: 3495-502.
50. Jeffreys AJ, Tamaki K, MacLeod A, et al. 1994. Complex gene conversion events in germline mutation at human minisatellites. Nat Genet 6: 136-45.
51. Jeffreys AJ, Neil DL, Neumann R. 1998. Repeat instability at human minisatellites arising from meiotic recombination. EMBO J 17: 4147-57.
52. Duret L, Arndt PF. 2008. The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 4: e10000071.
53. Lercher MJ, Hurst LD. 2002. Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet 18: 337-40.
54. Giver CR, Grosovsky AJ. 1997. Single and coincident intragenic mutations attributable to gene conversion in a human cell line. Genetics 146: 1429-39.
55. Ng SH, Parvanov E, Petkov PM, et al. 2008. A quantitative assay for crossover and noncrossover molecular events at individual recombination hotspots in both male and female gametes. Genomics 92: 204-9.
56. Jeffreys AJ, May CA. 2004. Intense and highly localized gene conversion activity in human meiotic crossover hotspots. Nat Genet 36: 151-6.
57. Kayser M, Roewer L, Hedman M, 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: 1580-8.
58. Weber JL, Wong C. 1993. Mutation of human short tandem repeats. Hum Mol Genet 2: 1123-8.
59. Amos W, Rubinsztein DC. 1996. Microsatellites are subject to directional evolution. Nat Genet 12: 13-4.
60. Ellegren H. 2000. Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet 16: 551-8.
61. Prugnolle F, Manica A, Balloux F. 2005. Geography predicts neutral genetic diversity of human populations. Curr Biol 15: R159-60.
62. Ramachandran S, Deshpande O, Roseman CC, et al. 2005. Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102: 15942-7.
63. Li JZ, Absher DM, Tang H, et al. 2008. Worldwide human relationships inferred from genomewide patterns of variation. Science 319: 1100-4.
64. Manica A, Amos W, Balloux F. 2007. The effect of ancient population bottlenecks on human phenotypes. Nature 448: 346-8.
65. Linz B, Balloux F, Moodley Y, et al. 2007. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445: 915-8.
66. Amos W, Flint J, Xu X. 2008. Heterozygosity increases microsatellite mutation rate, linking it to demographic history. BMC Genet 9: 72.
67. Kimmel M, Chakraborty R, Stivers DN, et al. 1996. Dynamics of repeat polymorphisms under a forward-backward mutation model: within- and between-population variability at microsatellite loci. Genetics 143: 549-55.
68. Garza JC, Slatkin M, Freimer NB. 1995. Microsatellite allele frequencies in humans and chimpanzees with implications for constraints on allele size. Mol Biol Evol 12: 594-604.
69. Schlö tterer C, Ritter R, Harr B, et al. 1998. High mutation rate of a long microsatellite allele in Drosophila melanogaster provides evidence for allele-specific mutation rates. Mol Biol Evol 15: 1269-74.
70. Tian D, Wang Q, Zhang P, et al. 2008. Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes. Nature 455: 105-9.
71. Hellmann I, Prüfer K, Ji H, et al. 2005. Why do human diversity levels vary at a megabase scale? Genome Res 15: 1222-31.
72. Gorlov IP, Gorlova OY, Amos CI. 2008. Relative effects of mutability and selection on single nucleotide polymorphisms in transcribed regions of the human genome. BMC Genomics 9: 292.
73. Bubb KL, Bovee D, Buckley D, et al. 2006. Scan of human genome reveals no new loci under ancient balancing selection. Genetics 173: 2165-77.
74. Hudson RR, Kaplan NL. 1995. The coalescent process and background selection. Phil Trans R Soc B 349: 19-23.
75. Myers S, Freeman C, Auton A, et al. 2008. A common sequence motif associated with recombination hot spots and genome instability in humans. Nat Genet 40: 1124-9.
76. Yeadon PJ, WBowring FJ, Catcheside DEA. 2004. Sequence heterology and gene conversion at his-3 of Neurospora crassa. Curr Genet 45: 289-301.
77. Winckler W, Myers SR, Richter DJ, et al. 2005. Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308: 107-11.
78. Ptak S, Hinds DA, Koehler K, et al. 2005. Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet 37: 429-34.
79. Lynch M, Gabriel W. 1990. Mutation load and the survival of small populations. Evolution 44: 1725-37.
80. Messier W, Li S-H, Stewart C-B. 1996. The birth of microsatellites. Nature 381: 483.
81. Weber JL. 1990. Informativeness of human (dC-dA)n. (dG-dT)n polymorphisms. Genomics 7: 524-30.
82. Lai Y, Sun F. 2003. The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol Biol Evol 20: 2123-31.
83. Kelkar YD, YTyekucheva S, Chlaromonte F, et al. 2008. The genomewide determinants of human and chimpanzee microsatellite evolution. Genome Res 18: 30-8.
84. Taylor JS, Durkin MH, Breden F. 1999. The death of a microsatellite: a phylogenetic perspective on microsatellite interruptions. Mol Biol Evol 16: 567-72.
85. Amos W. 1999. Two problems with the measurement of genetic diversity, distance. In Landweber LF, Dobson AP, ed; Genetics, the Extinction of Species. Princeton: Princeton University Press.
86. Amos W, Clarke A. 2008. Body temperature predicts maximum microsatellite length in mammals. Biol Lett 4: 399-401.
87. Valsecchi E, Palsbøll P, Hale P, et al. 1997. Microsatellite genetic distances between oceanic populations of the humpback whale (Megaptera novaeangliae). Mol Biol Evol 14: 355-62.
88. Przeworski M, Hudson RR, Di Rienzo A. 2000. Adjusting the focus on human variation. Trends Genet 16: 296-302.
89. Spencer CCA, Deloukas P, Hunt S, et al. 2006. The influence of recombination on human genetic diversity. PLoS Genet 2: e148.
90. Radford SJ, McMahan S, Blanton H, et al. 2007. Heteroduplex DNA in meiotic recombination in Drosophila mei-9 mutants. Genetics 176: 63-72.
91. Tenaillon MI, Austerlitz F, Tenaillon O. 2008. Apparent mutational hotspots and long distance linkage disequilibrium resulting from a bottleneck. J Evol Biol 21: 541-50.
92. Hinds DA, Stuve LL, Nilsen GB, et al. 2005. Whole-genome patterns of common DNA variation in three human populations. Science 307: 1072-9.
93. Voight BF, Kudaravalli S, Wen X, et al. 2006. A map of recent positive selection in the human genome. PLoS Biol 4: e72.
94. Johansson Á , Gyllensten U. 2008. Identification of local selective sweeps in human populations since the exodus from Africa. Hereditas 145: 126-37.
95. Wang E, Kodama G, Balbi P, et al. 2006. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc Natl Acad Sci USA 103: 135-40.
96. Prugnolle F, Manica A, Charpentier M, et al. 2005. Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol 15: 1022-7.
97. Lyons EJ, Amos W, Berkley JA, et al. 2009. Homozygosity and risk of childhood death due to invasive bacterial disease. BMC Med Genet 10: 55.
98. Rosenberg NA, Pritchard JK, Weber JL, et al. 2002. Genetic structure of human populations. Science 298: 2381-5.
99. Rosenberg NA, Maghajan S, Ramachandran S, et al. 2005. Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genet 1: 660-71.