Short indels are subject to insertion-biased gene conversion

Evolution

Volumn 67, Issue 9, 2013, Pages 2604-2613

  Leushkin, Evgeny V ^a,b   Bazykin, Georgii A ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

Author keywords

Gene conversion; Indel polymorphisms; Insertions and deletions; Recombination

Indexed keywords

DIVERGENCE; DNA; FLY; GENE; MUTATION; POLYMORPHISM; RECOMBINATION; SUBSTITUTION;

DROSOPHILA MELANOGASTER; HOMO SAPIENS; SACCHAROMYCES CEREVISIAE;

ANIMAL; ARTICLE; DROSOPHILA MELANOGASTER; GENE CONVERSION; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETICS; HUMAN; INDEL MUTATION; INDEL POLYMORPHISMS; MUTATION RATE; POINT MUTATION; RECOMBINATION; SACCHAROMYCES CEREVISIAE; SPECIES DIFFERENCE;

GENE CONVERSION; INDEL POLYMORPHISMS; INSERTIONS AND DELETIONS; RECOMBINATION;

ANIMALS; DROSOPHILA MELANOGASTER; GENE CONVERSION; HUMANS; INDEL MUTATION; MUTAGENESIS, INSERTIONAL; MUTATION RATE; POINT MUTATION; POLYMORPHISM, GENETIC; SACCHAROMYCES CEREVISIAE; SPECIES SPECIFICITY;

EID: 84883557944     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12129     Document Type: Article

References (50)

1. Barton, N. H., and B. Charlesworth 1998. Why sex and recombination? Science 281:1986-1990.
2. Begun, D. J., and C. F. Aquadro 1992. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356:519-520.
3. Berglund, J., K. S. Pollard, and M. T. Webster 2009. Hotspots of biased nucleotide substitutions in human genes. PLoS Biol. 7:e26.
4. Bill, C. A., W. A. Duran, N. R. Miselis, and J. A. Nickoloff 1998. Efficient repair of all types of single-base mismatches in recombination intermediates in Chinese hamster ovary cells: competition between long-patch and G-T glycosylase-mediated repair of G-T mismatches. Genetics 149:1935-1943.
5. Birky, C. W., and J. B. Walsh 1988. Effects of linkage on rates of molecular evolution. PNAS 85:6414-6418.
6. Buhler, C., V. Borde, and M. Lichten 2007. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol. 5:e324.
7. Campos, J. L., B. Charlesworth, and P. R. Haddrill 2012. Molecular evolution in nonrecombining regions of the Drosophila melanogaster genome. Genome Biol. Evol. 4:278-288.
8. Carvalho, A. B., and A. G. Clark 1999. Intron size and natural selection. Nature 401:344.
9. Charlesworth, B. 2012. The effects of deleterious mutations on evolution at linked sites. Genetics 190:5-22.
10. Clemente, F., and C. Vogl 2012. Unconstrained evolution in short introns? An analysis of genome-wide polymorphism and divergence data from Drosophila. J. Evol. Biol. 25:1975-1990.
11. Comeron, J. M., and M. Kreitman 2000. The correlation between intron length and recombination in drosophila. Dynamic equilibrium between mutational and selective forces. Genetics 156:1175-1190.
12. Comeron, J. M., R. Ratnappan, and S. Bailin 2012. The many landscapes of recombination in Drosophila melanogaster. PLoS Genet. 8:e1002905.
13. Crosby, M. A., J. L. Goodman, V. B. Strelets, P. Zhang, W. M. Gelbart, and The FlyBase Consortium. 2007. FlyBase: genomes by the dozen. Nucleic Acids Res. 35:D486-D491.
14. Dreszer, T. R., G. D. Wall, D. Haussler, and K. S. Pollard 2007. Biased clustered substitutions in the human genome: the footprints of male-driven biased gene conversion. Genome Res. 17:1420-1430.
15. Duret, L., and N. Galtier 2009. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu. Rev. Genomics Hum. Genet. 10:285-311.
16. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
17. Fiston-Lavier, A.-S., N. D. Singh, M. Lipatov, and D. A. Petrov 2010. Drosophila melanogaster recombination rate calculator. Gene. 463:18-20.
18. Garcia-Diaz, M., and T. A. Kunkel 2006. Mechanism of a genetic glissando*: structural biology of indel mutations. Trends Biochem. Sci. 31:206-214.
19. Graur, D., Y. Shuali, and W. H. Li 1989. Deletions in processed pseudogenes accumulate faster in rodents than in humans. J. Mol. Evol. 28:279-285.
20. Gregory, T. R. 2004. Insertion-deletion biases and the evolution of genome size. Gene 324:15-34.
21. Haddrill, P. R., B. Charlesworth, D. L. Halligan, and P. Andolfatto 2005. Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biol. 6:R67.
22. Haddrill, P. R., D. L. Halligan, D. Tomaras, and B. Charlesworth 2007. Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol. 8:R18.
23. Heger, A., and C. P. Ponting 2007. Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes. Genome Res. 17:1837-1849.
24. Hicks, W. M., M. Kim, and J. E. Haber 2010. Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329:82-85.
25. Hildebrand, F., A. Meyer, and A. Eyre-Walker 2010. Evidence of selection upon genomic GC-content in bacteria. PLoS Genet. 6:e1001107.
26. Hilliker, A. J., G. Harauz, A. G. Reaume, M. Gray, S. H. Clark, and A. Chovnick 1994. Meiotic gene conversion tract length distribution within the Rosy locus of Drosophila melanogaster. Genetics 137:1019-1026.
27. Hsu, F., W. J. Kent, H. Clawson, R. M. Kuhn, M. Diekhans, and D. Haussler 2006. The UCSC known genes. Bioinformatics 22:1036-1046.
28. Hubbard, T., D. Barker, E. Birney, G. Cameron, Y. Chen, L. Clark, T. Cox, J. Cuff, V. Curwen, T. Down, R. Durbin, et al. 2002. The Ensembl genome database project. Nucleic Acids Res. 30:38-41.
29. Hudson, R. R. 1994. How can the low levels of DNA sequence variation in regions of the drosophila genome with low recombination rates be explained? PNAS 91:6815-6818.
30. Keightley, P. D., U. Trivedi, M. Thomson, F. Oliver, S. Kumar, and M. L. Blaxter 2009. Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res. 19:1195-1201.
31. Kong, A., D. F. Gudbjartsson, J. Sainz, G. M. Jonsdottir, S. A. Gudjonsson, B. Richardsson, S. Sigurdardottir, J. Barnard, B. Hallbeck, G. Masson, et al. 2002. A high-resolution recombination map of the human genome. Nat. Genet. 31:241-247.
32. Kulathinal, R. J., S. M. Bennett, C. L. Fitzpatrick, and M. A. F. Noor 2008. Fine-scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. PNAS 105:10051-10056.
33. Leushkin, E. V., G. A. Bazykin, and A. S. Kondrashov 2012. Insertions and deletions trigger adaptive walks in Drosophila proteins. Proc. Biol. Sci. 279:3075-3082.
34. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, and R. Durbin 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079.
35. Lindblad-Toh, K., M. Garber, O. Zuk, M. F. Lin, B. J. Parker, et al. 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:476-482.
36. Lynch, M. 2007. The Origins of genome architecture. 1st ed. Sinauer Associates, Sunderland, MA.
37. Mackay, T. F. C., S. Richards, E. A. Stone, A. Barbadilla, J. F. Ayroles, D. Zhu, S. Casillas, Y. Han, M. M. Magwire, J. M. Cridland, et al. 2012. The Drosophila melanogaster genetic reference panel. Nature 482:173-178.
38. Mancera, E., R. Bourgon, A. Brozzi, W. Huber, and L. M. Steinmetz 2008. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454:479-485.
39. McVean, G. A., and B. Charlesworth 2000. The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155:929-944.
40. Messer, P. W. 2009. Measuring the rates of spontaneous mutation from deep and large-scale polymorphism data. Genetics 182:1219-1232.
41. Ometto, L., W. Stephan, and D. De Lorenzo 2005. Insertion/deletion and nucleotide polymorphism data reveal constraints in Drosophila melanogaster introns and intergenic regions. Genetics 169:1521-1527.
42. Parsch, J., S. Novozhilov, S. S. Saminadin-Peter, K. M. Wong, and P. Andolfatto 2010. On the utility of short intron sequences as a reference for the detection of positive and negative selection in Drosophila. Mol. Biol. Evol. 27:1226-1234.
43. Petrov, D. A., and D. L. Hartl 1998. High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol. Biol. Evol. 15:293-302.
44. Petrov, D. A., and D. L. Hartl 1999. Patterns of nucleotide substitution in Drosophila and mammalian genomes. Proc. Natl. Acad. Sci. U.S.A. 96:1475-1479.
45. Petrov, D. A., E. R. Lozovskaya, and D. L. Hartl 1996. High intrinsic rate of DNA loss in Drosophila. Nature 384:346-349.
46. Presgraves, D. C. 2006. Intron length evolution in Drosophila. Mol. Biol. Evol. 23:2203-2213.
47. Sella, G., D. A. Petrov, M. Przeworski, and P. Andolfatto 2009. Pervasive natural selection in the Drosophila genome? PLoS Genet. 5:e1000495.
48. Siepel, A., and D. Haussler 2004. Combining phylogenetic and hidden Markov models in biosequence analysis. J. Comput. Biol. 11:413-428.
49. Webster, M. T., and N. G. C. Smith 2004. Fixation biases affecting human SNPs. Trends Genet. 20:122-126.
50. Yang, Y., J. Sterling, F. Storici, M. A. Resnick, and D. A. Gordenin 2008. Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS Genet. 4:e1000264.