A two-pathway analysis of meiotic crossing over and gene conversion in Saccharomyces cerevisiae

Genetics

Volumn 186, Issue 2, 2010, Pages 515-536

  Stahl, Franklin W ^a   Foss, Henriette M ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEIN;

ARTICLE; CROSSING OVER; DNA REPLICATION; DNA STRAND BREAKAGE; EUKARYOTE; GENE CONVERSION; MEIOSIS; MISMATCH REPAIR; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

CHROMOSOME MAPPING; CHROMOSOME SEGREGATION; CHROMOSOMES, FUNGAL; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA MISMATCH REPAIR; DNA REPAIR; DNA, FUNGAL; GENE CONVERSION; GENETIC LINKAGE; MEIOSIS; MUTATION; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 78951486055     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.121194     Document Type: Article

References (71)

1. ABDULLAH, M. F. F., and R.H. Borts, 2001 Meiotic recombination frequencies are affected by nutritional states in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98: 14526-14529.
2. ABDULLAH, M. F. F., E.R. HOFFMANN, V.E. COTTON and R. H. BORTS, 2004 A role for the MutL homologue MLH2 in controlling heteroduplex formation and in regulating between two different crossover pathways in budding yeast. Cytogenet. Genome Res. 107: 180-190.
3. ACHARYA, S., P. L. FOSTER, P. BROOKS and R. FISHEL, 2003 The coordinated functions of the MutS and MutL proteins in mismatch repair. Mol. Cell 12: 233-246.
4. ALLERS, T., and M. LICHTEN, 2001a Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
5. ALLERS, T., and M. LICHTEN, 2001b Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8: 225-231.
6. ARGUESO, J. L., D. SMITH, J. YI, M. WAASE, S. SARIN et al., 2002 Analysis of conditional mutations in the Saccharomyces cerevisiae MLH1 gene in mismatch repair and in meiotic crossing over. Genetics 160: 909-921.
7. ARGUESO, J. L., J. WANAT, Z. GEMICI and E. ALANI, 2004 Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168: 1805-1816.
8. BELL, L. R., and B. BYERS, 1983 Homologous association of chromosomal DNA during yeast meiosis. Cold Spring Harbor Symp. Quant. Biol. 47: 829-840.
9. BERCHOWITZ, L. E., and G. P. COPENHAVER, 2010 Genetic interference: don't stand so close to me. Curr. Genomics 11: 91-102.
10. BISHOP, D. K., and D. ZICKLER, 2004 Early decision: meiotic cross-over interference prior to stable strand exchange and synapsis. Cell 117: 9-15.
11. BISHOP, D. K., M. S. WILLIAMSON, S. FOGEL and R. D. Kolodner, 1987 The role of heteroduplex correction in gene conversion in Saccharomyces cerevisiae. Nature 328: 362-364.
12. Börner, G. V., N. Kleckner and N. Hunter, 2004 Crossover/non- crossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
13. Burns, N.,B.Grimwade, P. B. Ross-MacDonald, E-Y. Choi, K. Finberg et al., 1994 Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes. Dev. 8: 1087-1105.
14. Chambers, S. R., N. Hunter, E. J. Louis and R. H. Borts, 1996 The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss. Mol. Cell. Biol. 16: 6110-6120.
15. CoÏc, E., L. Gluck and F. Fabre, 2000 Evidence for short-patch mismatch repair in Saccharomyces cerevisiae. EMBO J. 19: 3408-3417. (Pubitemid 30428218)
16. Cotton, V. E., E. R. Hoffmann, A. F. F. Abdullah and R. H. Borts, 2009 Interaction of genetic and environmental factors in Saccharomyces cerevisiae meiosis: the Devil is in the details. Methods Mol. Biol. 557: 3-20.
17. Cromie, G. A., and G. R. Smith, 2008 Meiotic recombination in Schizzosacharomyces pombe: a paradigm for genetic and molecular analysis. Genome Dyn. Stab. 3: 195-230.
18. Culligan, K. M., G. Meyer-Gauen, J. Lyons-Weiler and J. B. Hays, 2000 Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins. Nucleic Acids Res. 28: 463-471.
19. Detloff, P., M. A. White and T. D. Petes, 1992 Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae. Genetics 132: 113-123.
20. Ferguson, D. O., and W. K. Holloman, 1996 Recombinational repair of gaps in DNA is asymmetric in Ustilago maydis and can be explained by a migrating D-loop model. Proc. Natl. Acad. Sci. USA 93: 5419-5424.
21. Foss, E., R. Lande, F. W. Stahl and C.M. Steinberg, 1993 Chiasma interference as a function of genetic distance. Genetics 133: 681-691.
22. Foss, H. M., K. J. Hillers and F. W. Stahl, 1999 The conversion gradient at HIS4 in Saccharomyces cerevisiae. II. A role for mismatch repair directed by biased resolution of the recombinational intermediate. Genetics 153: 573-583.
23. Getz, T. J., S. A. Banse, L. S. Young, A. V. Banse, J. Swanson et al., 2008 Reduced mismatch repair of heteroduplexes reveals "non"- interfering crossing over in wild-type Saccharomyces cerevisiae. Genetics 178: 1251-1269.
24. Gilbertson, L. A., and F. W. Stahl, 1996 A test of the double strand break model for meiotic recombination in Saccharomyces cerevisiae. Genetics 144: 27-41.
25. Goldfarb, T., and E. Alani, 2005 Distinct roles for the Saccharomyces cerevisiae mismatch repair proteins in heteroduplex rejection, mismatch repair and nonhomologous tail removal. Genetics 169: 563-574.
26. Hillers, K. J., and F. W. Stahl, 1999 The conversion gradient at HIS4 of Saccharomyces cerevisiae. I. Heteroduplex rejection and restoration of Mendelian segregation. Genetics 153: 555-572.
27. Hoffmann, E. R., and R. H. Borts, 2004 Meiotic recombination intermediates and mismatch repair proteins. Cytogenet. Genome Res. 107: 232-248.
28. Hoffmann, E. R., and R. H. Borts, 2005 Trans events associated with crossovers are revealed in the absence of mismatch repair genes in Saccharomyces cerevisiae. Genetics 169: 1305-1310.
29. Hoffmann, E. R., E. Eriksson, B. J. Herbert and R. H. Borts, 2005 MLH1 and MSH2 promote the symmetry of double-strand break repair events at the HIS4 hotspot in Saccharomyces cerevisiae. Genetics 169: 1291-1303.
30. Hollingsworth, N. M., and S. J. Brill, 2004 The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev. 18: 117-125.
31. Hollingsworth, N. M., L. Ponte and C. Halsey, 1995 Msh5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev. 9: 1728-1739.
32. Hotchkiss, R. D., 1971 Toward a general theory of genetic recombination in DNA. Adv. Genet. 16: 325-348.
33. Hunter, N., 2007 Meiotic recombination, pp. 381-442 in Molecular Genetics of Recombination, edited by A. Aguilera and R. Rothstein. Springer, New York.
34. Hunter, N., and R. H. Borts, 1997 Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over duringmeiosis. Genes Dev. 11: 1573-1582.
35. Hunter, N., andN. Kleckner, 2004 The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic tecombination. Cell 106: 59-70.
36. Jessop, L., and M. Lichten, 2008 Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol. Cell 31: 313-323.
37. Kitani, Y., 1978 Absence of interference in association with gene conversion in Sordaria fimicola, and presence of interference in association with ordinary recombination. Genetics 89: 467-497.
38. Kitani, Y., and L. S. Olive, 1967 Genetics of Sordaria fimicola. VI. Gene conversion at the g locus in mutant x wild type crosses. Genetics 57: 767-782.
39. Lamb, B. C., and M. R. T. Wickramaratne, 1973 Correspondingsite interference, synaptinemal complex structure, and 8+:0m and 7+:1m octads from wild-type x mutant crosses of Ascobolus immersus. Genet. Res. 22: 113-124.
40. Maloisel, L., J. Bhargava and G. S. Roeder, 2004 A role for DNA polymerase in gene conversion and crossing over during meiosis in Saccharomyces cerevisiae. Genetics 167: 1133-1142.
41. Mancera, E,R. Bourgon, A. Brozzi, W.Huber and L.M. Steinmetz, 2008 High-resolution mapping of meiotic crossovers and noncrossovers in yeast. Nature 454: 479-485.
42. Merker, J.D.,M.Dominska and T. D. Petes, 2003 Patterns of heteroduplex formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 165: 47-63.
43. Modrich, P., 1991 Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25: 229-253.
44. Nag, D. K., M. A. White and T. D. Petes, 1989 Palindromic sequences in heteroduplex DNA inhibit mismatch repair in yeast. Nature 340: 318-320.
45. Nakagawa, T., A. Datta and R. D. Kolodner, 1999 Multiple functions of MutS- and MutL-related heterocomplexes. Proc. Natl. Acad. Sci. USA 96: 14186-14188.
46. Novak, J. E., P.B. Ross-MacDonald and G. S. Roeder, 2001 The budding yeastMsh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013-1025.
47. Oh, S. D., J. P. Lao, A. F. Taylor, G. R. Smith and N. Hunter, 2008 RecQ Helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol. Cell 31: 324-336.
48. Papazian,H. P., 1952 The analysis of tetrad data.Genetics 37: 175-188.
49. Paques, F., and J. E. Haber, 1999 Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
50. Perkins, D., 1949 Biochemical mutants of the smut fungus Ustilago maydis. Genetics 34: 607-626.
51. Pochart, P., D. Woltering and N. M. Hollingsworth, 1997 Conserved properties between functionally distinct MutS homologs in yeast. J. Biol. Chem. 272: 30345-30349.
52. Radford, S. J., S. McMahan, H. L. Blanton and J. Sekelsky, 2007 Heteroduplex DNA in meiotic recombination in Drosophila mei-9 mutants. Genetics 176: 63-72.
53. Ray, A., N. Machin and F.W. Stahl, 1989 A DNA double-chain break stimulates triparental recombination in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 86: 6225-6229.
54. Ross-MacDonald, P., and G. S. Roeder, 1994 Mutation of a meiosisspecific MutS homolog decreases crossing over but not mismatch correction. Cell 79: 1069-1080.
55. Schwacha, A., and N. Kleckner, 1995 Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
56. Shinohara, M., K. Sakai, A. Shinohara and D. K. Bishop, 2003 Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics 163: 1273-1286.
57. Snowden, T., S. Acharya, C. Butz, M. Berardini and R. Fishel, 2004 hMSH4-hMSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that links homologous chromosomes. Mol. Cell 15: 437-451. (Pubitemid 39092759)
58. Stahl, F. W., 2008 On the "NPD ratio" as a test for crossover interference. Genetics 179: 701-704.
59. Stahl, F. W., and H. M. Foss, 2008 But see Kitani (1978). Genetics 178: 1141-1145.
60. Stahl, F. W., and K. J. Hillers, 2000 Heteroduplex rejection in yeast? Genetics 154: 1913-1916.
61. Stahl, F.W., and E. A. Housworth, 2009 Methods for analysis of crossover interference in S. cerevisiae. Methods Mol. Biol. 557: 35-53.
62. Stahl, F. W., and R. Lande, 1995 Estimating interference and linkage map distance fromtwo-factor tetrad data. Genetics 139: 1449-1454.
63. Stahl, F.W., H. M. Foss, L. S. Young, R.H. Borts, M. F. F. Abdullah et al., 2004 Does crossover interference count in Saccharomyces cerevisiae? Genetics 168: 35-48.
64. Stone, J. E., and T. D. Petes, 2006 Analysis of the proteins involved in the in vivo repair of base-base mismatches and four-base loops formed during meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 173: 1223-1239.
65. Sun, H., D. Treco and J. W. Szostak, 1991 Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific doublestrand breaks at the ARG4 recombination initiation site. Cell 64: 1155-1161.
66. Surtees, J. A., J-L Argueso and E. Alani, 2004 Mismatch repair proteins: Key regulators of genetic recombination. Cytogenet. Genome Res. 107: 146-159.
67. Szostak, J., T. L. Orr-Weaver, R. J. Rothstein and F.W. Stahl, 1983 The double-strand-break repair model for recombination. Cell 33: 25-35.
68. Terasawa, M., H. Ogawa, Y. Tsukamoto, M. Shinohara, K. Shirahige et al., 2007 Meiotic recombination-related DNA synthesis and its implications for cross-over and non-crossover recombinant formation. Proc. Natl. Acad. Sci. USA 104: 5965-5970.
69. Wang, H., Y. Yang, M. J. Schofield, C. Du, Y. Fridman et al., 2003 DNA bending and unbending by MutS govern mismatch recognition and specificity. Proc. Natl. Acad. Sci. USA 100: 14822-14827.
70. Wang, T-F., N. Kleckner and N. Hunter, 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.
71. Zalevsky, J., A. J. MacQueen, J. B. Duffy, K. J. Kemphues and A. M. Villeneuve, 1999 Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271-1283.