A role for the mismatch repair system during incipient speciation in Saccharomyces

Journal of Evolutionary Biology

Volumn 16, Issue 3, 2003, Pages 429-437

  Greig, D ^a,b   Travisano, M ^b   Louis, E J ^c   Borts, Rhona H ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b University of Houston   (United States)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Evolution; Meiosis; Mismatch repair; Speciation; Yeast

Indexed keywords

REPRODUCTIVE ISOLATION; SPECIATION (BIOLOGY); YEAST;

BASE PAIR MISMATCH; CROSSES, GENETIC; DNA REPAIR ENZYMES; EVOLUTION, MOLECULAR; HYBRIDIZATION, GENETIC; REPRODUCTION; SACCHAROMYCES CEREVISIAE; SPECIES SPECIFICITY;

SACCHAROMYCES;

EID: 0037546919     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1420-9101.2003.00546.x     Document Type: Article

References (63)

1. Abdullah, M.F.F. & Borts, R.H. 2001. Meiotic recombination frequencies are affected by nutritional states in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98: 14524-14529.
2. Adams, A., Gottschling, C.A., Kaiser, T. & Stearns, T. 1997. Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Plainveiw.
3. Alani, A., Reenan, R.A. & Kolodner, R.D. 1994. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics 137: 19-39.
4. Argueso, J.L., Sarin, S., Kijas, A. & Alani, E. 2002. Analysis of conditional mutations in the Saccharomyces cerevisiae MLHI gene in mismatch repair and crossing over. Genetics 160: 909-921.
5. Borts, R.H. & Haber, J.E. 1987. Meiotic recombination in yeast: alteration by multiple heterozygosities. Science 237: 1459-1463.
6. Borts, R.H., Leung, W.-Y., Kramer, K., Kramer, B., Williamson, M.S., Fogel, S. & Haber, J.E. 1990. Mismatch repair-induced meiotic recombination requires the PMS1 gene product. Genetics 124: 573-584.
7. Borts, R.H., Chambers, S.R. & Abdullah, M.F.F. 2000. The many faces of mismatch repair in meiosis. Mut. Res. 451: 129-150.
8. Chambers, S.R., Hunter, N., Louis, E.J. & Borts, R.H. 1996. The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss. Mol. Cell. Biol. 16: 6110-6120.
9. Chen, W. & Jinks-Robertson, S. 1998. Mismatch repair protein regulate heteroduplex formation during mitotic recombination in yeast. Mol. Cell. Biol. 18: 6525-6537.
10. Chen, W. & Jinks-Robertson, S. 1999. The role of the mismatch repair machinery in regulating mitotic and meiotic recombination between diverged sequences in yeast. Genetics 151: 1299-1313.
11. Coyne, J.A. 1992. Genetics and speciation. Nature 355: 511-515.
12. Datta, A., Hendrix, M., Lipsitch, M. & Jinks-Robertson, S. 1997. 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 94: 9757-9762.
13. Dover, G.A. 1982. Molecular drive: a cohesive mode of species evolution. Nature 299: 111-117.
14. Drake, J.W., Charlesworth, B., Charlesworth, D. & Crow, J.F. 1998. Rates of spontaneous mutation. Genetics 148: 1667-1686.
15. Efron, B. 1982. The Jackknife, the Bootstrap, and Other Resampling Plans. SIAM/CBMS, Philadelphia.
16. Elliott, B. & Jasin, M. 2001. Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells. Mol. Cell. Biol. 21: 2671-2682.
17. Elliott, B., Richardson, C., Winderbaum, J., Nickoloff, J.A. & Jasin, M. 1998. Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell. Biol. 18: 93-101.
18. Fischer, G., James, S.A., Roberts, I.N., Oliver, S.G. & Louis, E.J. 2000. Chromosomal evolution in Saccharomyces. Nature 405: 451-454.
19. Gendrel, C.G. & Dutreix, M. 2001. (CA/TG) microsatellite sequences escape the inhibition of recombination by mismatch repair in Saccharomyces cerevisiae. Genetics 159: 1539-1545.
20. Greig, D., Borts, R.H., Louis, E.J. & Travisano, M. 2002. Epistasis and hybrid sterility in Saccharomyces. Proc. R. Soc. Lond. B. Biol. Sci. 269: 1167-1171.
21. Harfe, B.D. & Jinks-Robertson, S. 2000. DNA mismatch repair and genetic instability. Ann. Rev. Genet. 34: 359-399.
22. Hawthorne, D. & Philippsen, P. 1994. Genetic and molecular analysis of hybrids in the genus Saccharomyces involving S. cerevisiae, S. uvarum and a new species, S. douglasii. Yeast 10: 1285-1296.
23. Holbeck, S.L. & Strathern, J.N. 1997. A role for REV3 in mutagenesis during double-strand break repair in Saccharomyces cerevisiae. Genetics 147: 1017-1024.
24. Hunter, N. & Borts, R.H. 1997. Mlh1p is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev. 11: 1573-1582.
25. Hunter, N., Chambers, S.R., Louis, E.J. & Borts, R.H. 1996. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 15: 1726-1733.
26. Kramer, W., Kramer, B., Williamson, M.S. & Fogel, S. 1989. Cloning and nucleotide sequence of DNA mismatch repair gene PMS1 from Saccharomyces cerevisiae: homology to prokaryotic MutL and HexB. J. Bacteriol. 171: 5339-5346.
27. Louis, E.J. 1994. Corrected sequence for the right telomere of Saccharomyces cerevisiae chromosome III. Yeast 10: 271-274.
28. Louis, E.J. & Haber, J.E. 1989. Non-recombinant meiosis I non-disjunction in Saccharomyces cerevisiae is induced by tRNA ochre suppressors. Genetics 123: 81-95.
29. Lukacsovich, T. & Waldman, A.S. 1999. Suppression of intrachromosomal gene conversion in mammalian cells by small degrees of sequence divergence. Genetics 151: 1559-1568.
30. Mayr, E. 1963. Animal Species and Evolution. Belknap Press, Harvard University Press, Cambridge.
31. McCusker, J.H. & Haber, J.E. 1988a. Cycloheximide-resistant temperature sensitive lethal mutations of Saccharomyces cerevisiae. Genetics 119: 303-315.
32. McCusker, J.H. & Haber, J.E. 1988b. CRL mutants of Saccharomyces cerevisiae resemble both mutants affecting general control of amino acid biosynthesis and omnipotent translational suppressor mutants. Genetics 119: 317-327.
33. McMillan, W.O., Jiggins, C.D. & Mallet, J. 1997. What initiates speciation in passion-vine butterflies? Proc. Natl. Acad. Sci. USA 94: 8628-8633.
34. Mortimer, R.K. & Johnston, J.R. 1986. Genealogy of principal strains of the yeast genetic stock center. Genetics 113: 35-43.
35. Myung, K., Chen, C. & Kolodner, R.D. 2001. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411: 1073-1076.
36. Naumov, G.I. 1987. Genetic basis for classification and identification of the ascomycetous yeasts. Stud. Mycol. 30: 469-475.
37. Naumov, G.I., Naumova, E.S., Azbukina, Z.M., Korhola, M. & Gaillardin, C. 1993. Genetic and karyotypic identification of Saccharomyces yeasts from Far East Asia. Cryptogamie, Mycol. 14: 85-93.
38. Naumov, G.I., Naumova, E.S. & Sniegowski, P.D. 1997. Differentiation of European and Far East Asian populations of Saccharomyces paradoxus by allozyme analysis. Int. J. Syst. Bacteriol. 47: 341-344.
39. Naumov, G.I, & Nikomenko, T. 1988. New isolates of S. paradoxus from oak tree exudates. Biol. Nanki 7: 84-87.
40. Nelson, S.F., McCusker, J.H., Sander, M.A., Kee, Y., Modrich, P. & Brown, P.O. 1993. Genomic mismatch scanning: a new approach to genetic linkage mapping. Nat. Genet. 4: 11-18.
41. Novak, J.E., Ross-Macdonald, P.B. & Roeder, G.S. 2001. The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013-1025.
42. Orr, H.A. & Presgraves, D.C. 2000. Speciation by postzygotic isolation: forces, genes and molecules. Bioessays 22: 1085-1094.
43. Parker, G.A. & Partridge, L. 1998. Sexual conflict and speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353: 261-274.
44. Radman, M. 1989. Mismatch repair and fidelity of genetic recombination. Genome 31: 68-73.
45. Rayssiguier, C., Thaler, D.S. & Radman, M. 1989. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342: 396-400.
46. Reenan, R.A. & Kolodner, R.D. 1992. Characterisation of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics 132: 975-985.
47. Reiseberg, L.H. & Burke, J.M. 2001. A genic view of species integration. J. Evol. Biol. 14: 883-886.
48. Roeder, G.S. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11: 2600-2621.
49. Rose, M.R. & Doolittle, W.F. 1983. Molecular biological mechanisms of speciation. Science 220: 157-162.
50. Ross-Macdonald, P. & Roeder, G.S. 1994. Mutation of a meiosis-specific MutS homolog decreases crossing-over but not mismatch correction. Cell 79: 1069-1080.
51. Selva, E.M., New, L., Crouse, G.F. & Lahue, R.S. 1995. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae. Genetics 139: 1175-1188.
52. Sniegowski, P. 1998. Mismatch repair: origin of species? Curr. Biol. 8: R59-R61.
53. Sokal, R.R. & Rohlf, F.J. 1969. Biometry. W.H. Freeman, San Francisco.
54. Templeton, A.R. 1981. Mechanisms of speciation - a population genetic approach. Ann. Rev. Ecol. Syst. 12: 23-48.
55. Travisano, M. & Rainey, P.B. 2000. Studies of adaptive radiation using model microbial systems. Am. Nat. 156: S35-S44.
56. Vulic, M., Dionisio, F., Taddei, F. & Radman, M. 1997. Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. Proc. Natl. Acad. Sci. USA 94: 9763-9767.
57. Vulic, M., Lenski, R.E. & Radman, M. 1999. Mutation, recombination, and incipient speciation of bacteria in the laboratory. Proc. Natl. Acad. Sci. USA 96: 7348-7351.
58. Waldman, A.S. & Liskay, R.M. 1988. Dependence of intrachromosomal recombination in mammalian cells on uninterrupted homology. Mol. Cell. Biol. 8: 5350-5357.
59. Wang, T.-F., Kleckner, N. & Hunter, N. 1999. Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc. Natl. Acad. Sci. USA 96: 13914-13919.
60. Williamson, M.S., Game, J.C. & Fogel, S. 1985. Meiotic gene conversion mutants in Saccharomyces cerevisiae. I. Isolation and characterization of pms1-1 and pms1-2. Genetics 110: 609-646.
61. de Wind, N., Dekker, M., Berns, A., Radman, M. & te Riele, H. 1995. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 82: 321-330.
62. Wu, C.-L 2001a. The genic view of the process of speciation. J. Evol. Biol. 14: 851-865.
63. Wu, C.-I. 2001b. Genes and speciation. J. Evol. Biol. 14: 889-891.