The rate and tract length of gene conversion between duplicated genes

Genes

Volumn 2, Issue 2, 2011, Pages 313-331

  Mansai, Sayaka P ^a   Kado, Tomoyuki ^a   Innan, Hideki ^a,b  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Gene conversion rate; Interlocus gene conversion; Tract length

Indexed keywords

ARTICLE; DNA RECOMBINATION; DNA REPAIR; DNA SEQUENCE; DNA STRUCTURE; DUPLICATE GENE; GENE CONVERSION; GENOTYPE; HOMOLOGOUS RECOMBINATION; HUMAN; MAXIMUM LIKELIHOOD METHOD; MISSENSE MUTATION; MOLECULAR EVOLUTION; NONHUMAN; NONSENSE MUTATION; POINT MUTATION; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL ANALYSIS; TRACT LENGTH;

EID: 79959768175     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes2020313     Document Type: Article

References (100)

1. Mitchell, M.B. Aberrant recombination of pyridoxine mutants of Neurospora. Proc. Natl. Acad. Sci. USA 1955, 41, 215-220.
2. Ernst, J.F.; Stewart, J.W.; Sherman, F. The cyc1-11 mutation in yeast reverts by recombination with a nonallelic gene: Composite genes determining the iso-cytochromes c. Proc. Natl. Acad. Sci. USA 1981, 78, 6334-6338.
3. Chen, J.M.; Cooper, D.N.; Chuzhanova, N.; Férec, C.; Patrinos, G.P. Gene conversion: Mechanisms, evolution and human disease. Nat. Rev. Genet. 2007, 8, 762-775.
4. Hastings, P.J. Mechanisms of ectopic gene conversion. Genes 2010, 1, 427-439.
5. Ling, F.; Mikawa, T.; Shibata, T. Enlightenment of yeast mitochondrial homoplasmy: Diversified roles of gene conversion. Genes 2011, 2, 169-190.
6. Esposito, M.S. Evidence that spontaneous mitotic recombination occurs at the two-strand stage. Proc. Natl. Acad. Sci. USA 1978, 75, 4436-4440.
7. Mieczkowski, P.A.; Lemoine, F.J.; Petes, T.D. Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair 2006, 5, 1010-1020.
8. Mikus, M.D.; Petes, T.D. Recombination between genes located on nonhomologous chromosomes in Saccharomyces cerevisiae. Genetics 1982, 101, 369-404.
9. Sugawara, N.; Szostak, J.W. Recombination between sequences in nonhomologous positions. Proc. Natl. Acad. Sci. USA 1983, 80, 5675-5679.
10. Jinks-Robertson, S.; Petes, T.D. High-frequency meiotic gene conversion between repeated genes on nonhomologous chromosomes in yeast Proc. Natl. Acad. Sci. USA 1985, 82, 3350-3354.
11. Haber, J.E.; Leung, W.Y.; Borts, R.H.; Lichten, M. The frequency of meiotic recombination in yeast is independent of the number and position of homologous donor sequences: Implications for chromosome pairing. Proc. Natl. Acad. Sci. USA 1991, 88, 1120-1124.
12. Jinks-Robertson, S.; Petes, T.D. Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes. Genetics 1986, 114, 731-752.
13. Lichten, M.; Borts, R.H.; Haber, J.E. Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics 1987, 115, 233-246.
14. Jinks-Robertson, S.; Michelitch, M.; Ramcharan, S. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Mol. Cell Biol. 1993, 13, 3937-3950.
15. Lichten, M.; Haber, J.E. Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. Genetics 1989, 123, 261-268.
16. Kupiec, M.; Petes, T.D. Allelic and ectopic recombination between Ty elements in yeast. Genetics 1988, 119, 549-559.
17. Steele, D.F.; Morris, M.E.; Jinks-Robertson, S. Allelic and ectopic interactions in recombination-defective yeast strains. Genetics 1991, 127, 53-60.
18. Jackson, J.A.; Fink, G.R. Meiotic recombination between duplicated genetic elements in Saccharomyces cerevisiae. Genetics 1985, 109, 303-332.
19. Bailis, A.M.; Rothstein, R. A defect in mismatch repair in Saccharomyces cerevisiae stimulates ectopic recombination between homeologous genes by an excision repair dependent process. Genetics 1990, 126, 535-547.
20. Harris, S.; Rudnicki, K.S.; Haber, J.E. Gene conversions and crossing over during homologous and homeologous ectopic recombination in Saccharomyces cerevisiae. Genetics 1993, 135, 5-16.
21. Mézard, C.; Pompon, D.; Nicolas, A. Recombination between similar but not identical DNA sequences during yeast transformation occurs within short stretches of identity. Cell 1992, 70, 659-670.
22. Datta, A.; Adjiri, A.; New, L.; Crouse, G.F.; Jinks-Robertson, S. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccharomyces cerevisiae. Mol. Cell Biol. 1996, 16, 1085-1093.
23. Datta, A.; Hendrix, M.; Lipsitch, M.; Jinks-Robertson, S. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc. Natl. Acad. Sci. USA 1997, 94, 9757-9762.
24. Chen, W.; Jinks-Robertson, S. Mismatch repair proteins regulate heteroduplex formation during mitotic recombination in yeast. Mol. Cell Biol. 1998, 18, 6525-6537.
25. Chen, W.; Jinks-Robertson, S. The role of the mismatch repair machinery in regulating mitotic and meiotic recombination between diverged sequences in yeast. Genetics 1999, 151, 1299-1313.
26. Ahn, B.Y.; Dornfeld, K.J.; Fagrelius, T.J.; Livingston, D.M. Effect of limited homology on gene conversion in a Saccharomyces cerevisiae plasmid recombination system. Mol. Cell Biol. 1988, 8, 2442-2448.
27. Shen, P.; Huang, H.V. Homologous recombination in Escherichia coli: Dependence on substrate length and homology. Genetics 1986, 112, 441-457.
28. Waldman, A.S. Ensuring the fidelity of recombination in mammalian chromosomes. Bioessays 2008, 30, 1163-1171.
29. Sugawara, N.; Ira, G.; Haber, J.E. DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol. Cell Biol. 2000, 20, 5300-5309.
30. Kijima, T.E.; Innan, H. On the estimation of the insertion time of LTR retrotransposable elements. Mol. Biol Evol. 2010, 27, 896-904.
31. Murti, J.R.; Bumbulis, M.; Schimenti, J.C. High-frequency germ line gene conversion in transgenic mice. Mol. Cell Biol. 1992, 12, 2545-2552.
32. Schildkraut, E.; Miller, C.A.; Nickoloff, J.A. Gene conversion and deletion frequencies during double-strand break repair in human cells are controlled by the distance between direct repeats. Nucleic Acids Res. 2005, 33, 1574-1580.
33. Perez, C.; Guyot, V.; Cabaniols, J.P.; Gouble, A.; Micheaux, B.; Smith, J.; Leduc, S.; Pâques, F.; Duchateau, P. Factors affecting double-strand break-induced homologous recombination in mammalian cells. Biotechniques 2005, 39, 109-115.
34. Waldman, A.S.; Liskay, R.M. Differential effects of base-pair mismatch on intrachromosomal versus extrachromosomal recombination in mouse cells. Proc. Natl. Acad. Sci. USA 1987, 84, 5340-5344.
35. Waldman, A.S.; Liskay, R.M. Dependence of intrachromosomal recombination in mammalian cells on uninterrupted homology. Mol. Cell Biol. 1988, 8, 5350-5357.
36. Elliott, B.; Richardson, C.; Winderbaum, J.; Nickoloff, J.A.; Jasin, M. Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell Biol. 1998, 18, 93-101.
37. Lukacsovich, T.; Waldman, A.S. Suppression of intrachromosomal gene conversion in mammalian cells by small degrees of sequence divergence. Genetics 1999, 151, 1559-1568.
38. Yang, D.; Goldsmith, E.B.; Lin, Y.; Waldman, B.C.; Kaza, V.; Waldman, A.S. Genetic exchange between homeologous sequences in mammalian chromosomes is averted by local homology requirements for initiation and resolution of recombination. Genetics 2006, 174, 135-144.
39. Nickoloff, J.A.; Chen, E.Y.; Heffron, F. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc. Natl. Acad. Sci. USA 1986, 83, 7831-7835.
40. Plessis, A.; Perrin, A.; Haber, J.E.; Dujon, B. Site-specific recombination determined by I-SceI, a mitochondrial group I intron-encoded endonuclease expressed in the yeast nucleus. Genetics 1992, 130, 451-460.
41. Chen, J.M.; Férec, C.; Cooper, D.N. Gene conversion in human genetic disease. Genes 2010, 1, 550-563.
42. Chuzhanova, N.; Chen, J.M.; Bacolla, A.; Patrinos, G.P.; Férec, C.; Wells, R.D.; Cooper, D.N. Gene conversion causing human inherited disease: Evidence for involvement of non-B-DNA-forming sequences and recombination-promoting motifs in DNA breakage and repair. Hum. Mutat. 2009, 30, 1189-1198.
43. Harfe, B.D.; Jinks-Robertson, S. DNA mismatch repair and genetic instability. Annu. Rev. Genet. 2000, 34, 359-399.
44. Wiuf, C.; Hein, J. The coalescent with gene conversion. Genetics 2000, 155, 451-462.
45. Innan, H. A method for estimating the mutation, gene conversion and recombination parameters in small multigene families. Genetics 2002, 161, 865-872.
46. Innan, H. The coalescent and infinite-site model of a small multigene family. Genetics 2003, 163, 803-810.
47. Ohta, T. Allelic and nonallelic homology of a supergene family. Proc. Natl. Acad. Sci. USA 1982, 79, 3251-3254.
48. Takuno, S.; Innan, H. Selection to maintain paralogous amino acid differences under the pressure of gene conversion in the heat-shock protein genes in yeast. Mol. Biol. Evol. 2009, 26, 2655-2659.
49. Thornton, K.; Long, M. Excess of amino acid substitutions relative to polymorphism between X-linked duplications in Drosophila melanogaster. Mol. Biol. Evol. 2005, 22, 273-284.
50. Arguello, J.R.; Chen, Y.; Yang, S.; Wang, W.; Long, M. Origination of an X-linked testes chimeric gene by illegitimate recombination in Drosophila. PLoS Genet. 2006, 2, e77.
51. Nielsen, K.M.; Kasper, J.; Choi, M.; Bedford, T.; Kristiansen, K.; Wirth, D.F.; Volkman, S.K.; Lozovsky, E.R.; Hartl, D.L. Gene conversion as a source of nucleotide diversity in Plasmodium falciparum. Mol. Biol. Evol. 2003, 20, 726-734.
52. Takuno, S.; Nishio, T.; Satta, Y.; Innan, H. Preservation of a pseudogene by gene conversion and diversifying selection. Genetics 2008, 180, 517-531.
53. Eda, M.; Kuro-o, M.; Higuchi, H.; Hasegawa, H.; Koike, H. Mosaic gene conversion after a tandem duplication of mtDNA sequence in Diomedeidae (albatrosses). Genes Genet. Syst. 2010, 85, 129-139.
54. Innan, H. A two-locus gene conversion model with selection and its application to the human RHCE and RHD genes. Proc. Natl. Acad. Sci. USA 2003, 100, 8793-8798.
55. Rozen, S.; Skaletsky, H.; Marszalek, J.D.; Minx, P.J.; Cordum, H.S.; Waterston, R.H.; Wilson, R.K.; Page, D.C. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 2003, 423, 873-876.
56. Ogorelkova, M.; Navarro, A.; Vivarelli, F.; Ramirez-Soriano, A.; Estivill, X. Positive selection and gene conversion drive the evolution of a brain-expressed snoRNAs cluster. Mol. Biol. Evol. 2009, 26, 2563-2571.
57. Fogel, S.; Mortimer, R.; Lusnak, K. Mechanisms of Meiotic Gene Conversion, or Wanderings on a Foreign Strand; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 1981.
58. Golin, J.E.; Esposito, M.S. Coincident gene conversion during mitosis in Saccharomyces. Genetics 1984, 107, 355-365.
59. Ahn, B.Y.; Livingston, D.M. Mitotic gene conversion lengths, coconversion patterns, and the incidence of reciprocal recombination in a Saccharomyces cerevisiae plasmid system. Mol. Cell Biol. 1986, 6, 3685-3693.
60. Sweetser, D.B.; Hough, H.; Whelden, J.F.; Arbuckle, M.; Nickoloff, J.A. Fine-resolution mapping of spontaneous and double-strand break-induced gene conversion tracts in Saccharomyces cerevisiae reveals reversible mitotic conversion polarity. Mol. Cell Biol. 1994, 14, 3863-3875.
61. Cho, J.W.; Khalsa, G.J.; Nickoloff, J.A. Gene-conversion tract directionality is influenced by the chromosome environment. Curr. Genet. 1998, 34, 269-279.
62. Weng, Y.; Barton, S.L.; Cho, J.W.; Nickoloff, J.A. Marker structure and recombination substrate environment influence conversion preference of broken and unbroken alleles in Saccharomyces cerevisiae. Mol. Genet. Genomics. 2001, 265, 461-468.
63. Taghian, D.G.; Nickoloff, J.A. Chromosomal double-strand breaks induce gene conversion at high frequency in mammalian cells. Mol. Cell Biol. 1997, 17, 6386-6393.
64. Kim, P.M.; Allen, C.; Wagener, B.M.; Shen, Z.; Nickoloff, J.A. Over expression of human RAD51 and RAD52 reduces double-strand break-induced homologous recombination in mammalian cells. Nucleic Acids Res. 2001, 29, 4352-4360.
65. Gloor, G.B.; Nassif, N.A.; Johnson-Schlitz, D.M.; Preston, C.R.; Engels, W.R. Targeted gene replacement in Drosophila via P element-induced gap repair. Science 1991, 253, 1110-1117.
66. Hilliker, A.J.; Harauz, G.; Reaume, A.G.; Gray, M.; Clark, S.H.; Chovnick, A. Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics 1994, 137, 1019-1026.
67. Johnson-Schlitz, D.M.; Engels, W.R. P-element-induced interallelic gene conversion of insertions and deletions in Drosophila melanogaster. Mol. Cell Biol. 1993, 13, 7006-7018.
68. Preston, C.R.; Engels, W.R. P-element-induced male recombination and gene conversion in Drosophila. Genetics 1996, 144, 1611-1622.
69. de Massy, B. Distribution of meiotic recombination sites. Trends Genet. 2003, 19, 514-522.
70. Palmer, S.; Schildkraut, E.; Lazarin, R.; Nguyen, J.; Nickoloff, J.A. Gene conversion tracts in Saccharomyces cerevisiae can be extremely short and highly directional. Nucleic Acids Res. 2003, 31, 1164-1173.
71. Yang, D.; Waldman, A.S. Fine-resolution analysis of products of intrachromosomal homeologous recombination in mammalian cells. Mol. Cell Biol. 1997, 17, 3614-3628.
72. Rukść, A.; Bell-Rogers, P.; Smith, J.D.; Baker, M.D. Analysis of spontaneous gene conversion tracts within and between mammalian chromosomes. J. Mol. Biol. 2008, 377, 337-351.
73. Mancera, E.; Bourgon, R.; Brozzi, A.; Huber, W.; Steinmetz, L.M. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 2008, 454, 479-485.
74. Sawyer, S. Statistical tests for detecting gene conversion. Mol. Biol. Evol. 1989, 6, 526-538.
75. Mansai, S.P.; Innan, H. The power of the methods for detecting interlocus gene conversion. Genetics. 2010, 184, 517-527.
76. Benovoy, D.; Drouin, G. Ectopic gene conversions in the human genome. Genomics 2009, 93, 27-32.
77. Stephens, J.C. Statistical methods of DNA sequence analysis: Detection of intragenic recombination or gene conversion. Mol. Biol. Evol. 1985, 2, 539-556.
78. Takahata, N. Comments on the detection of reciprocal recombination or gene conversion. Immunogenetics. 1994, 39, 146-149.
79. Betrán, E.; Rozas, J.; Navarro, A.; Barbadilla, A. The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics 1997, 146, 89-99.
80. Jakobsen, I.B.; Wilson, S.R.; Easteal, S. The partition matrix: Exploring variable phylogenetic signals along nucleotide sequence alignments. Mol. Biol. Evol. 1997, 14, 474-484.
81. Ezawa, K.; Oota, S.; Saitou, N.; Investigators, S.T.N.Y. Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Genome-wide search of gene conversions in duplicated genes of mouse and rat. Mol. Biol. Evol. 2006, 23, 927-940.
82. Adams, J.G. II; Morrison, W.T.; Steinberg, M.H. Hemoglobin Parchman: Double crossover within a single human gene. Science 1982, 218, 291-293.
83. Eikenboom, J.C.; Vink, T.; Briët, E.; Sixma, J.J.; Reitsma, P.H. Multiple substitutions in the von Willebrand factor gene that mimic the pseudogene sequence. Proc. Natl. Acad. Sci. USA 1994, 91, 2221-2224.
84. Watnick, T.J.; Gandolph, M.A.; Weber, H.; Neumann, H.P.; Germino, G.G. Gene conversion is a likely cause of mutation in PKD1. Hum. Mol. Genet. 1998, 7, 1239-1243.
85. De Marco, P.; Moroni, A.; Merello, E.; de Franchis, R.; Andreussi, L.; Finnell, R.H.; Barber, R.C.; Cama, A.; Capra, V. Folate pathway gene alterations in patients with neural tube defects. Am J. Med. Genet. 2000, 95, 216-223.
86. Hatton, C.; Cooper, A.; Whitehouse, C.; Wraith, J. Mutation analysis in 46 British and Irish patients with Gaucher's disease. Arc. Dis. Child. 1997, 77, 17-22.
87. Vázquez, N.; Lehrnbecher, T.; Chen, R.; Christensen, B.L.; Gallin, J.I.; Malech, H.; Holland, S.; Zhu, S.; Chanock, S.J. Mutational analysis of patients with p47-phox-deficient chronic granulomatous disease: The significance of recombination events between the p47-phox gene (NCF1) and its highly homologous pseudogenes. Exp. Hematol. 2001, 29, 234-243.
88. Boocock, G.R.; Morrison, J.A.; Popovic, M.; Richards, N.; Ellis, L.; Durie, P.R.; Rommens, J.M. Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat. Genet. 2003, 33, 97-101.
89. Gupta, P.K.; Adamtziki, E.; Budde, U.; Jaiprakash, M.; Kumar, H.; Harbeck-Seu, A.; Kannan, M.; Oyen, F.; Obser, T.; Wedekind, I.; Saxena, R.; Schneppenheim, R. Gene conversions are a common cause of von Willebrand disease. Br. J. Haematol. 2005, 130, 752-758.
90. Gupta, P.K.; Saxena, R.; Adamtziki, E.; Budde, U.; Oyen, F.; Obser, T.; Schneppenheim, R. Genetic defects in von Willebrand disease type 3 in Indian and Greek patients. Blood Cells Mol. Dis. 2008, 41, 219-222.
91. Friães, A.; Rêgo, A.T.; Aragüés, J.M.; Moura, L.F.; Mirante, A.; Mascarenhas, M.R.; Kay, T.T.; Lopes, L.A.; Rodrigues, J.C.; Guerra, S.; Dias, T.; Teles, A.G.; Gonçalves, J. CYP21A2 mutations in Portuguese patients with congenital adrenal hyperplasia: Identification of two novel mutations and characterization of four different partial gene conversions. Mol. Genet. Metab. 2006, 88, 58-65.
92. Tayebi, N.; Stubblefield, B.K.; Park, J.K.; Orvisky, E.; Walker, J.M.; LaMarca, M.E.; Sidransky, E. Reciprocal and nonreciprocal recombination at the glucocerebrosidase gene region: implications for complexity in Gaucher disease. Am J. Hum. Genet. 2003, 72, 519-534.
93. Nicolis, E.; Bonizzato, A.; Assael, B.M.; Cipolli, M. Identification of novel mutations in patients with Shwachman-Diamond syndrome. Hum. Mutat. 2005, 25, 410.
94. Petes, T.D. Meiotic recombination hot spots and cold spots. Nat. Rev. Genet. 2001, 2, 360-369.
95. Myers, S.; Bottolo, L.; Freeman, C.; McVean, G.; Donnelly, P. A fine-scale map of recombination rates and hotspots across the human genome. Science 2005, 310, 321-324.
96. Jeffreys, A.J.; Neumann, R.; Panayi, M.; Myers, S.; Donnelly, P. Human recombination hot spots hidden in regions of strong marker association. Nat. Genet. 2005, 37, 601-606.
97. Paigen, K.; Petkov, P. Mammalian recombination hot spots: properties, control and evolution. Nat. Rev. Genet. 2010, 11, 221-233.
98. Han, L.L.; Keller, M.P.; Navidi, W.; Chance, P.F.; Arnheim, N. Unequal exchange at the Charcot-Marie-Tooth disease type 1A recombination hot-spot is not elevated above the genome average rate. Hum. Mol. Genet. 2000, 9, 1881-1889.
99. Bosch, E.; Hurles, M.E.; Navarro, A.; Jobling, M.A. Dynamics of a human interparalog gene conversion hotspot. Genome Res. 2004, 14, 835-844.
100. Turner, D.J.; Miretti, M.; Rajan, D.; Fiegler, H.; Carter, N.P.; Blayney, M.L.; Beck, S.; Hurles, M.E. Germline rates of de novo meiotic deletions and duplications causing several genomic disorders. Nat. Genet. 2008, 40, 90-95.