Does crossover interference count in Saccharomyces cerevisiae?

Genetics

Volumn 168, Issue 1, 2004, Pages 35-48

  Stahl, Franklin W ^a   Foss, Henriette M ^a   Young, Lisa S ^a   Borts, Rhona H ^b   Abdullah, M F F ^c   Copenhaver, Gregory P ^d  

^a UNIVERSITY OF OREGON   (United States)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITI TEKNOLOGI MARA   (Malaysia)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN;

ARTICLE; CHROMOSOME BREAKAGE; CHROMOSOME PAIRING; CROSSING OVER; FUNGAL STRAIN; GENE CLUSTER; GENE MAPPING; GENETIC LINKAGE; GENOTYPE; HOLLIDAY JUNCTION; MATHEMATICAL MODEL; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SOMATIC CROSSING OVER; SYNAPSE;

CELL CYCLE PROTEINS; CROSSING OVER, GENETIC; DNA REPAIR; DNA, CRUCIFORM; MEIOSIS; MODELS, GENETIC; OLIGONUCLEOTIDES; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 4143092113     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.027789     Document Type: Article

References (100)

1. 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 length and in regulation between two different crossover pathways in budding yeast. Cytogenet. Genome Res.: Repair Proteins in Meiosis 107 (in press).
2. ATCHESON, C. L., B. DIDOMENICO, S. FRACKMAN, R. E. ESPOSITO and R. T. ELDER, 1987 Isolation, DNA sequence, and regulation of a meiosis-specific eukaryotic recombination gene. Proc. Natl. Acad. Sci. USA 84: 8035-8039.
3. BAILEY, N. T. J., 1961 Introduction to the Mathematical Theory of Genetic Linkage. Clarendon, Oxford.
4. BAKER, M. D., and E. C. BIRMINGHAM, 2001 Evidence for biased Holliday junction cleavage and mismatch repair directed by junction cuts during double-strand-break repair in mammalian cells. Mol. Cell. Biol. 21: 3425-3435.
5. BELL, L. R., and B. BYERS, 1983 Homologous association of chromosomal DNA during yeast meiosis. Cold Spring Harbor Symp. Quant. Biol. 47: 829-840.
6. BIRKENBIHL, R. P., and B. KEMPER, 2002 High affinity of endonuclease VII for the Holliday structure containing one nick ensures productive resolution. J. Mol. Biol. 321: 21-28.
7. BORKOVICH, K. A., L. A ALEX, O. YARDEN, M. FREITAG, G. E. TURNER et al., 2004 Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 68: 1-108.
8. BROMAN, K. W., and J. L. WEBER, 2000 Characterization of human crossover interference. Am. J. Hum. Genet. 66: 1911-1926.
9. BURGESS, S. M., N. KLECKNER and B. M. WEINER, 1999 Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev. 13: 1627-1641.
10. BYERS, B., and L. GOETSCH, 1982 Reversible pachytene arrest of Saccharomyces cerevisiae at elevated temperature. Mol. Gen. Genet. 187: 47-53.
11. CHU, S., J. DERISI, M. EISEN, J. MULHOLLAND, D. BOTSTEIN et al., 1998 The transcriptional program of sporulation in budding yeast. Science 282: 699-705.
12. COBBS, G., 1978 Renewal process approach to the theory of genetic linkage: case of no chromatid interference. Genetics 89: 563-581.
13. COLAIÁCOVO, M. P., A. J. MACQUEEN, E. MARTINEZ-PEREZ, K. MCDONALD, A. ADAMO et al., 2003 Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell 5: 463-474.
14. COPENHAVER, G. P., E. A. HOUSWORTH and F. W. STAHL, 2002 Crossover interference in Arabidopsis. Genetics 160: 1631-1639.
15. DAVIDOW, L. S., and B. BYERS, 1984 Enhanced gene conversion and postmeiotic segregation in pachytene-arrested Saccharomyces cerevisiae. Genetics 106: 165-183.
16. DE LOS SANTOS, T., N. HUNTER, C. LEE, B. LARKIN, J. LOIDL et al., 2003 The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164: 81-94.
17. DERNBURG, A. F., K. MCDONALD, G. MOULDER, R. BARSTEAD, M. DRESSER et al., 1998 Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.
18. FOGG, J. M., and D. M. J. LILLEY, 2000 Ensuring productive resolution by the junction-resolving enzyme RuvC: large enhancement of the second-strand cleavage rate. Biochemistry 39: 16125-16134.
19. FOSS, E. J., and F. W. STAHL, 1995 A test of a counting model for chiasma interference. Genetics 139: 1201-1209.
20. FOSS, E., R. LANDE, F. W. STAHL and C. M. STEINBERG, 1993 Chiasma interference as a function of genetic distance. Genetics 133: 681-691.
21. FOSS, H. M., K. J. HILLERS and F. W. STAHL, 1999 The conversion gradient at HIS4 of Saccharomyces cerevisiae. II. A role for mismatch repair directed by biased resolution of the recombinational intermediate. Genetics 153: 573-583.
22. FUNG, J. C., B. ROCKMILL, M. ODELL and G. S. ROEDER, 2004 Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795-802.
23. GAILLARD, P. H., E. NOGUCHI, P. SHANAHAN and P. RUSSELL, 2003 The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism. Mol. Cell 12: 747-759.
24. GERTON, J. L., and J. L. DERISI, 2002 Mnd1p: an evolutionarily conserved protein required for meiotic recombination. Proc. Natl. Acad. Sci. USA 99: 6895-6900.
25. GILBERTSON, L. A., and F. W. STAHL, 1996 A test of the double-strand break repair model for meiotic recombination in Saccharomyces cerevisiae. Genetics 144: 27-41.
26. GOLDMAN, A. S. H., and M. LICHTEN, 2000 Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc. Natl. Acad. Sci. USA 97: 9537-9542.
27. GÜLDENER, U., S. HECK, T. FIEDLER, J. BEINHAUER and J. H. HEGEMANN, 1996 A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24: 2519-2524.
28. HALDANE, J. B. S., 1919 The combination of linkage values, and the calculation of distances between the loci of linked factors. J. Genet. 8: 299-309.
29. HENDERSON, K. A., and S. KEENEY, 2004 Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 101: 4519-4524.
30. HILLIKER, A. J., and A. CHOVNICK, 1981 Further observations on intragenic recombination in Drosophila melanogaster. Genet. Res. 38: 281-296.
31. HILLIKER, A. J., S. H. CLARK and A. CHOVNICK, 1991 The effect of DNA sequence polymorphisms on intragenic recombination in the rosy locus of Drosophila melanogaster. Genetics 129: 779-781.
32. HILLERS, K. J., and F. W. STAHL, 1999 The conversion gradient at HIS4 of Saccharomyces cerevisiae. I. Rejection and restoration of Mendelian segregation. Genetics 153: 555-572.
33. HOFFMANN, E. R., 2002 Functional analysis of MLH1. Ph.D. Thesis, Oxford University, Oxford.
34. HOFFMANN, E. R., and R. H. BORTS, 2004 Meiotic recombination intermediates and mismatch repair proteins. Cytogenet. Genome Res.: Repair Proteins in Meiosis 107 (in press).
35. HOTTA, Y., and H. STERN, 1971 Analysis of DNA synthesis during meiotic prophase in Lilium. J. Mol. Biol. 55: 337-355.
36. HOUSWORTH, E. A., and F. W. STAHL, 2003 Crossover interference in humans. Am. J. Hum. Genet. 73: 188-197.
37. HUNTER, N., and N. KLECKNER, 2001 The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106: 59-70.
38. IKEYA, T., A. SHINOHARA, S. SATO, S. TABATA and T. OGAWA, 1996 Localization of mouse Rad51 and Lim15 proteins on meiotic chromosomes at late stages of prophase 1. Genes Cells 1: 379-389.
39. IRA, G., A. MALKOVA, G. LIBERI, M. FOIANI and J. HABER, 2003 Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115: 401-411.
40. JANG, J. K., D. E. SHERIZEN, R. BHAGAT, E. A. MANHEIM and K. S. MCKIM, 2003 Relationship of DNA double-strand breaks to synapsis in Drosophila. J. Cell Sci. 116: 3069-3077.
41. JONES, J. S., and L. PRAKASH, 1990 Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast 6: 363-366.
42. KABACK, D. B., V. GUACCI, D. BARBER and J. W. MAHON, 1992 Chromosome size-dependent control of meiotic recombination. Science 256: 228-232.
43. KABACK, D. B., D. BARBER, J. MAHON, J. LAMB and J. YOU, 1999 Chromosome size-dependent control of meiotic reciprocal recombination in Saccharomyces cerevisiae: the role of crossover interference. Genetics 152: 1475-1486.
44. KELLY, K. O., A. F. DERNBURG, G. M. STANFIELD and A. M. VILLENEUVE, 2000 Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156: 617-630.
45. KING, J. S., and R. K. MORTIMER, 1991 A mathematical model of interference for use in constructing linkage maps from tetrad data. Genetics 129: 597-602.
46. KLECKNER, N., 1996 Meiosis: How could it work? Proc. Natl. Acad. Sci. USA 93: 8167-8174.
47. LANDE, R., and F. W. STAHL, 1993 Chiasma interference and the distribution of exchanges in Drosophila melanogaster. Cold Spring Harbor Symp. Quant. Biol. 58: 543-552.
48. LIU, H., J. K. JANG, N. KATO and K. S. MCKIM, 2002 mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster. Genetics 162: 245-258.
49. MALKOVA, A., J. SWANSON, M. GERMAN, E. HOUSWORTH, F. W. STAHL et al., 2004 Gene conversion and crossing-over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49-63.
50. MCCUSKER, J. H., and J. E. HABER, 1988 Cycloheximide-resistant temperature-sensitive lethal mutations of Saccharomyces cerevisiae. Genetics 119: 303-315.
51. MCKIM, K. S., B. L. GREEN-MARROQUIN, J. J. SEKELSKY, G. CHIN, C. STEINBERG et al., 1998 Meiotic synapsis in the absence of recombination. Science 279: 876-878.
52. MCPEEK, M. S., and T. P. SPEED, 1995 Modeling interference in genetic recombination. Genetics 139: 1031-1044.
53. MENEELY, P. M., A. F. FARAGO and T. M. KAUFFMAN, 2002 Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics 162: 1169-1177.
54. 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.
55. MOENS, P. B., N. K. KOLAS, M. TARSOUNAS, E. MARCON, P. E. COHEN et al., 2002 The time course and chromosomal location of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J. Cell Sci. 115: 1611-1622.
56. MORTIMER, R. K., and S. FOGEL, 1974 Genetical interference and gene conversion, pp. 263-275 in Mechanisms in Recombination, edited by R. F. GRELL. Plenum, New York.
57. MULLER, H. J., 1916 The mechanism of crossing-over. Am. Nat. 50: 193-221 and ff.
58. NOVAK, J. E., P. B. ROSS-MACDONALD and G. S. ROEDER, 2001 The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013-1025.
59. PAGE, S. L., and R. S. HAWLEY, 2001 c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev. 15: 3130-3143.
60. PAPAZIAN, H. P., 1952 The analysis of tetrad data. Genetics 37: 175-188.
61. 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.
62. PERKINS, D. D., R. LANDE and F. W. STAHL, 1993 Estimates of the proportion of recombination intermediates that are resolved with crossing over in Neurospora crassa. Appendix 2, to Foss et al. (1993). Genetics 133: 681-691.
63. PIGOZZI, M. I., and A. J. SOLARI, 1998 First demonstration of the substructure of recombination nodules. Biocell 22: 177-186.
64. RINALDO, C., P. BAZZICALUPO, S. EDERLE, M. HILLIARD and A. LA VOLPE, 2002 Roles for Caenorhabditis elegans rad-51 in meiosis and in resistance to ionizing radiation during development. Genetics 160: 471-479.
65. ROCKMILL, B., M. SYM, H. SCHERTHAN and G. S. ROEDER, 1995 Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 9: 2684-2695.
66. ROCKMILL, B., J. C. FUNG, S. BRANDA and G. S. ROEDER, 2003 The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr. Biol. 13: 1954-1962.
67. ROEDER, G. S., 1997 Meiotic chromosomes: it takes two to tango. Genes Dev. 11: 2600-2621.
68. ROMANIENKO, P. J., and R. D. CAMERINI-OTERO, 2000 The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol. Cell 6: 975-987.
69. ROSSIGNOL, J. L., and N. PAQUETTE, 1979 Disparity of gene conversion in frameshift mutants located in locus b2 of Ascobolus immersus. Proc. Natl. Acad. Sci. USA 76: 2871-2875.
70. ROSS-MACDONALD, P., and G. S. ROEDER, 1994 Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79: 1069-1080.
71. SANTUCCI-DARMANIN, S., D. WALPITA, F. LESPINASSE, C. DESNUELLE, T. ASHLEY et al., 2000 MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB J. 14: 1539-1547.
72. SCHWACHA, A., and N. KLECKNER, 1995 Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
73. SCHWACHA, A., and N. KLECKNER, 1997 Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123-1135.
74. SHANNON, M., L. RICHARDSON, A. CHRISTIAN, M. A. HANDEL and M. P. THELEN, 1999 Differential gene expression of mammalian SPO11/TOP6A homologs during meiosis. FEBS Lett. 462: 329-334.
75. 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.
76. 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.
77. STADLER, D. R., 1959 The relationship of gene conversion to crossing over in Neurospora. Proc. Natl. Acad. Sci. USA 45: 1625-1629.
78. STADLER, D. R., and A. M. TOWE, 1963 Recombination of allelic cysteine mutants in Neurospora. Genetics 48: 1323-1344.
79. STAHL, F. W., 1993 Genetic recombination: thinking about it in phage and fungi, pp. 1-9 in The Chromosome, edited by J. S. HESLOP-HARRISON and R. B. FLAVELL. Bios, Oxford.
80. STAHL, F. W., and R. LANDE, 1995 Estimating interference and linkage map distance from two-factor tetrad data. Genetics 139: 1449-1454.
81. STAM, P., 1979 Interference in genetic crossing over and chromosome mapping. Genetics 92: 573-594.
82. STORLAZZI, A., L. XU, A. SCHWACHA and N. KLECKNER, 1996 Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc. Natl. Acad. Sci. USA 93: 9043-9048.
83. STURTEVANT, A. H., 1913 The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of association. J. Exp. Zool. 14: 43-59.
84. STURTEVANT, A. H., 1915 The behavior of chromosomes as studied through linkage. Z. Abstam. Vererbung. 13: 234-287.
85. SUN, H., D. TRECO, N. P. SCHULTES and J. W. SZOSTAK, 1989 Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338: 87-90.
86. SUN, H., D. TRECO and J. W. SZOSTAK, 1991 Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64: 1155-1161.
87. SYM, M., and G. S. ROEDER, 1994 Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79: 283-292.
88. SZOSTAK, J. W., T. L. ORR-WEAVER, R. J. ROTHSTEIN and F. W. STAHL, 1983 The double-strand-break repair model for recombination. Cell 33: 25-35.
89. TAKANAMI, T., A. MORI, H. TAKAHASHI and A. HIGASHITANI, 2000 Hyper-resistance of meiotic cells to radiation due to a strong expression of a single recA-like gene in Caenorhabditis elegans. Nucleic Acids Res. 28: 4232-4236.
90. TERASAWA, M., A. SHINOHARA, Y. HOTTA, H. OGAWA and T. OGAWA, 1995 Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev. 9: 925-934.
91. TSUBOUCHI, H., and G. S. ROEDER, 2002 The Mnd1 protein forms a complex with Hop2 to promote homologous chromosome pairing and meiotic double-strand break repair. Mol. Cell. Biol. 22: 3078-3088.
92. TSUBOUCHI, H., and G. S. ROEDER, 2003 The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev. Cell 5: 915-925.
93. VIERA, A., J. L. SANTOS, J. PAGE, M. T. PARRA, A. CALVENTE et al., 2004 DNA double-strand breaks, recombination and synapsis: the timing of meiosis differs in grasshoppers and flies. EMBO Rep. 5: 385-391.
94. VILLENEUVE, A. M., 1994 A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887-902.
95. WALKER, M. Y., and R. S. HAWLEY, 2000 Hanging on to your homolog: the roles of pairing, synapsis and recombination in the maintenance of homolog adhesion. Chromosoma 109: 3-9.
96. WEST, S. C., 1992 Enzymes and molecular mechanisms of genetic recombination. Annu. Rev. Biochem. 61: 603-640.
97. XU, L., B. M. WEINER and N. KLECKNER, 1997 Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 11: 106-118.
98. 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.
99. ZHAO, H., T. P. SPEED and M. S. MCPEEK, 1995 Statistical analysis of crossover interference using the chi-square model. Genetics 139: 1045-1056.
100. ZICKLER, D, and N. KLECKNER, 1998 The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32: 619-697.