DOI: 10.1093/genetics/151.4.1245. CYS3, a Hotspot of Meiotic Recombination in Saccharomyces cerevisiae: Effects of Heterozygosity and Mismatch Repair Functions on Gene Conversion and Recombination Intermediates

CYS3, a Hotspot of Meiotic Recombination in Saccharomyces cerevisiae: Effects of Heterozygosity and Mismatch Repair Functions on Gene Conversion and Recombination Intermediates

10.1093/genetics/151.4.1245

Crossref journal-article

Oxford University Press (OUP)

Genetics (286)

Abstract

Abstract We have examined meiotic recombination at the CYS3 locus. Genetic analysis indicates that CYS3 is a hotspot of meiotic gene conversion, with a putative 5′–3′ polarity gradient of conversion frequencies. This gradient is relieved in the presence of msh2 and pms1 mutations, indicating an involvement of mismatch repair functions in meiotic recombination. To investigate the role of mismatch repair proteins in meiotic recombination, we performed a physical analysis of meiotic DNA in wild-type and msh2 pms1 strains in the presence or absence of allelic differences at CYS3. Neither the mutations in CYS3 nor the absence of mismatch repair functions affects the frequency and distribution of nearby recombination-initiating DNA double-strand breaks (DSBs). Processing of DSBs is also similar in msh2 pms1 and wild-type strains. We conclude that mismatch repair functions do not control the distribution of meiotic gene conversion events at the initiating steps. In the MSH2 PMS1 background, strains heteroallelic for frameshift mutations in CYS3 exhibit a frequency of gene conversion greater than that observed for either marker alone. Physical analysis revealed no modification in the formation of DSBs, suggesting that this marker effect results from subsequent processing events that are not yet understood.

Bibliography

Vedel, M., & Nicolas, A. (1999). CYS3, a Hotspot of Meiotic Recombination in Saccharomyces cerevisiae: Effects of Heterozygosity and Mismatch Repair Functions on Gene Conversion and Recombination Intermediates. Genetics, 151(4), 1245â1259.

Authors 2

Michèle Vedel (first)
Alain Nicolas (additional)

References 61 Referenced 22

10.1128/MCB.16.10.5604 / Mol. Cell. Biol. / The Saccharomyces cerevisiae Msh2 and Msh6 proteins form a complex that binds specifically to duplex oligonucleotides containing mismatched DNA base pairs by Alani (1996)
10.1016/0092-8674(90)90524-I / Cell / Analysis of wild type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination by Alani (1990)
10.1093/genetics/137.1.19 / Genetics / Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae by Alani (1994)
10.1006/jmbi.1996.0743 / J. Mol. Biol. / Saccharomyces cerevisiae MSH2, a mispaired base recognition protein, also recognizes Holliday junctions in DNA by Alani (1997)
10.1002/yea.320090406 / Yeast / Physical localization of yeast CYS3, a gene whose product resembles the rat γ-cystathionase and Escherichia coli cystathionine γ-synthase enzymes by Barton (1993)
10.1073/pnas.94.10.5213 / Proc. Natl. Acad. Sci. USA / Clustering of meiotic double-strand breaks on yeast chromosome III by Baudat (1997)
10.1038/386414a0 / Nature / An atypical topoisomerase II from archaea with implications for meiotic recombination by Bergerat (1997)
10.1016/0092-8674(92)90446-J / Cell / DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression by Bishop (1992)
10.1007/BF00330984 / Mol. Gen. Genet. / A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoroacetic acid resistance by Boeke (1984)
10.1126/science.2820060 / Science / Meiotic recombination in yeast: alteration by multiple heterozygosities by Borts (1987)
10.1073/pnas.93.23.13054 / Proc. Natl. Acad. Sci. USA / Double strand breaks at the HIS2 recombination hotspot in Saccharomyces cerevisiae by Bullard (1996)
10.1016/0092-8674(90)90072-M / Cell / A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae by Cao (1990)
10.1093/genetics/130.1.51 / Genetics / Genetic analysis of a new mutation conferring cysteine auxotrophy in Saccharomyces cerevisiae: updating of the sulfur metabolism pathway by Cherest (1992)
10.1073/pnas.81.7.1991 / Proc. Natl. Acad. Sci. USA / Genomic sequencing by Church (1984)
10.1073/pnas.94.18.9757 / Proc. Natl. Acad. Sci. USA / Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast by Datta (1997)
10.1002/j.1460-2075.1993.tb05789.x / EMBO J. / The control in cis of the position and the amount of the ARG4 meiotic double-strand break of Saccharomyces cerevisiae by de Massy (1993)
10.1002/j.1460-2075.1995.tb00138.x / EMBO J. / The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae by de Massy (1995)
{'key': '2022010314113376800_R18', 'first-page': '1805', 'article-title': 'Measurements of excision repair tracts formed during meiotic recombination in Saccharomyces cerevisiae', 'volume': '12', 'author': 'Detloff', 'year': '1992', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Measurements of excision repair tracts formed during meiotic recombination in Saccharomyces cerevisiae by Detloff (1992)
10.1093/genetics/132.1.113 / Genetics / Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae by Detloff (1992)
10.1128/MCB.16.5.2037 / Mol. Cell. Biol. / Relationship between nuclease-hypersensitive sites and meiotic recombination hotspot activity at the HIS4 locus of Saccharomyces cerevisiae by Fan (1996)
10.1128/MCB.15.3.1679 / Mol. Cell. Biol. / Meiosis-specific double-strand DNA breaks at the HIS4 recombination hotspot in the yeast Saccharomyces cerevisiae: control in cis and trans by Fan (1995)
{'key': '2022010314113376800_R22', 'first-page': '89', 'article-title': 'Gene conversion in unselected tetrads from multipoint crosses', 'author': 'Fogel', 'year': '1971', 'journal-title': 'The Second Stadler Symposia'} / The Second Stadler Symposia / Gene conversion in unselected tetrads from multipoint crosses by Fogel (1971)
{'key': '2022010314113376800_R23', 'first-page': '289', 'article-title': 'Mechanism of meiotic gene conversion or “wandering on a foreign strand,”', 'volume-title': 'The Molecular Biology of Yeast Saccharomyces', 'author': 'Fogel', 'year': '1981'} / The Molecular Biology of Yeast Saccharomyces / Mechanism of meiotic gene conversion or “wandering on a foreign strand,” by Fogel (1981)
10.1093/genetics/133.2.159 / Genetics / A short chromosomal region with major roles in yeast chromosome III meiotic disjunction, recombination and double strand breaks by Goldway (1993)
10.1101/SQB.1984.049.01.008 / Cold Spring Harbor Symp. Quant. Biol. / Measurement of restoration and conversion: its meaning for the mismatch repair hypothesis of conversion by Hastings (1984)
10.1046/j.1365-2443.1996.d01-257.x / Genes Cells / Communication between homologous chromosomes: genetic alterations at a nuclease-hypersensitive site can alter mitotic chromatin structure at that site both in cis and in trans by Keeney (1996)
10.1016/S0092-8674(00)81876-0 / Cell / Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family by Keeney (1997)
10.1093/genetics/149.4.1693 / Genetics / Conversion-type and restoration-type repair of DNA mismatches formed during meiotic recombination in Saccharomyces cerevisiae by Kirkpatrick (1998)
10.1007/BF02524645 / Chromosoma / Patterns of meiotic double-strand breakage on native and artificial yeast chromosomes by Klein (1996)
10.1128/jb.171.10.5339-5346.1989 / J. Bacteriol. / Cloning and nucleotide sequence of DNA mismatch repair gene PMS1 from Saccharomyces cerevisiae: homology of PMS1 to procaryotic MutL and HexB by Kramer (1989)
10.1146/annurev.ge.29.120195.002231 / Annu. Rev. Genet. / Meiotic recombination hotspots by Lichten (1995)
10.1073/pnas.87.19.7653 / Proc. Natl. Acad. Sci. USA / Detection of heteroduplex DNA molecules among the products of Saccharomyces cerevisiae meiosis by Lichten (1990)
10.1038/359154a0 / Nature / A meiotic gene conversion gradient opposite to the direction of transcription by Malone (1992)
10.1093/genetics/137.1.5 / Genetics / Analysis of a recombination hotspot for gene conversion occurring at the HIS2 gene of Saccharomyces cerevisiae by Malone (1994)
10.1093/genetics/144.1.71 / Genetics / Analysis of meiotic recombination pathways in Saccharomyces cerevisiae by Mao-Draayer (1996)
10.1101/gad.10.4.407 / Genes Dev. / Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair by Marsischky (1996)
{'key': '2022010314113376800_R37', 'first-page': '2324', 'article-title': 'Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae', 'volume': '13', 'author': 'Nag', 'year': '1993', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae by Nag (1993)
10.1007/BF01924007 / Experientia / Polarity of meiotic gene conversion in fungi: contrasting views by Nicolas (1994)
10.1139/g89-101 / Genome / Intermediates in homologous recombination revealed by marker effects in Ascobolus by Nicolas (1989)
10.1038/338035a0 / Nature / An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae by Nicolas (1989)
10.1002/j.1460-2075.1994.tb06913.x / EMBO J. / Changes in chromatin structure at recombination initiation sites during yeast meiosis by Ohta (1994)
10.1128/jb.174.10.3339-3347.1992 / J. Bacteriol. / Cloning and characterization of the CYS3 (CYI1) gene of Saccharomyces cerevisiae by Ono (1992)
10.1139/g93-005 / Genome / Sequencing of chromosome I from Saccharomyces cerevisiae: analysis of a 32 kb region between the LTE1 and SPO7 genes by Ouellette (1993)
{'key': '2022010314113376800_R44', 'first-page': '407', 'article-title': 'Recombination in yeast', 'volume-title': 'The Molecular and Cellular Biology of the Yeast Saccharomyces', 'author': 'Petes', 'year': '1991'} / The Molecular and Cellular Biology of the Yeast Saccharomyces / Recombination in yeast by Petes (1991)
10.1126/science.8066446 / Science / MLH1, PMS1, and MSH2 interactions during the initiation of DNA mismatch repair in yeast by Prolla (1994)
10.1093/genetics/132.4.963 / Genetics / Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins by Reenan (1992)
10.1093/genetics/132.4.975 / Genetics / Characterization of insertion mutation in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions by Reenan (1992)
10.1046/j.1365-2443.1996.00256.x / Genes Cells / Sensing of nonhomology lowers the initiation of meiotic recombination in yeast by Rocco (1996)
10.1073/pnas.76.10.4951 / Proc. Natl. Acad. Sci. USA / Replacement of chromosome segments with altered DNA sequences constructed in vitro by Scherer (1979)
10.1093/genetics/126.4.813 / Genetics / Decreasing gradients of gene conversion on both sides of the initiation site for meiotic recombination at the ARG4 locus in yeast by Schultes (1990)
10.1016/0092-8674(95)90191-4 / Cell / Identification of double Holliday junctions as intermediates in meiotic recombination by Schwacha (1995)
10.1016/S0092-8674(00)81791-2 / Cell / Meiotic recombination in yeast: coronation of the double-strand break repair model by Stahl (1996)
10.1038/338087a0 / Nature / Doublestrand breaks at an initiation site for meiotic gene conversion by Sun (1989)
10.1016/0092-8674(91)90270-9 / Cell / Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site by Sun (1991)
10.1016/0092-8674(83)90331-8 / Cell / The double-strand break repair model for conversion and crossing-over by Szostak (1983)
{'key': '2022010314113376800_R56', 'volume-title': 'Genetic Recombination, Understanding the Mechanisms.', 'author': 'Whitehouse', 'year': '1982'} / Genetic Recombination, Understanding the Mechanisms. by Whitehouse (1982)
10.1016/S0092-8674(00)80978-2 / Cell / RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling by Wilson (1996)
10.1126/science.8290959 / Science / Meiosis-induced double-strand break sites determined by yeast chromatin structure by Wu (1994)
10.1093/genetics/143.3.1115 / Genetics / Fine-structure mapping of meiosis-specific double-strand DNA breaks at a recombination hotspot associated with an insertion of telomeric sequence upstream of the HIS4 locus in yeast by Xu (1996)
10.1007/BF02426957 / Curr. Genet. / The distance dependence of the fission yeast ade6-M26 marker effect in two-factor crosses by Zahn-Zabal (1996)
10.1002/j.1460-2075.1992.tb05423.x / EMBO J. / Multiple sites for double-strand breaks in whole meiotic chromosomes of Saccharomyces cerevisiae by Zenvirth (1992)

Dates

Type	When
Created	4 years, 4 months ago (April 27, 2021, 11:05 p.m.)
Deposited	3 years, 7 months ago (Jan. 3, 2022, 12:47 p.m.)
Indexed	4 days, 8 hours ago (Aug. 23, 2025, 9:54 p.m.)
Issued	26 years, 4 months ago (April 1, 1999)
Published	26 years, 4 months ago (April 1, 1999)
Published Online	26 years, 4 months ago (April 1, 1999)
Published Print	26 years, 4 months ago (April 1, 1999)

Funders 0

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BibTeX

@article{Vedel_1999, title={CYS3, a Hotspot of Meiotic Recombination in Saccharomyces cerevisiae: Effects of Heterozygosity and Mismatch Repair Functions on Gene Conversion and Recombination Intermediates}, volume={151}, ISSN={1943-2631}, url={http://dx.doi.org/10.1093/genetics/151.4.1245}, DOI={10.1093/genetics/151.4.1245}, number={4}, journal={Genetics}, publisher={Oxford University Press (OUP)}, author={Vedel, Michèle and Nicolas, Alain}, year={1999}, month=apr, pages={1245–1259} }

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      "volume": "16",
      "author": "Alani",
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      "journal-title": "Mol. Cell. Biol."
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      "first-page": "419",
      "DOI": "10.1016/0092-8674(90)90524-I",
      "article-title": "Analysis of wild type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination",
      "volume": "61",
      "author": "Alani",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2022010314113376800_R3",
      "doi-asserted-by": "crossref",
      "first-page": "19",
      "DOI": "10.1093/genetics/137.1.19",
      "article-title": "Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae",
      "volume": "137",
      "author": "Alani",
      "year": "1994",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R4",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1006/jmbi.1996.0743",
      "article-title": "Saccharomyces cerevisiae MSH2, a mispaired base recognition protein, also recognizes Holliday junctions in DNA",
      "volume": "265",
      "author": "Alani",
      "year": "1997",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2022010314113376800_R5",
      "doi-asserted-by": "crossref",
      "first-page": "363",
      "DOI": "10.1002/yea.320090406",
      "article-title": "Physical localization of yeast CYS3, a gene whose product resembles the rat \u03b3-cystathionase and Escherichia coli cystathionine \u03b3-synthase enzymes",
      "volume": "9",
      "author": "Barton",
      "year": "1993",
      "journal-title": "Yeast"
    },
    {
      "key": "2022010314113376800_R6",
      "doi-asserted-by": "crossref",
      "first-page": "5213",
      "DOI": "10.1073/pnas.94.10.5213",
      "article-title": "Clustering of meiotic double-strand breaks on yeast chromosome III",
      "volume": "94",
      "author": "Baudat",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022010314113376800_R7",
      "doi-asserted-by": "crossref",
      "first-page": "414",
      "DOI": "10.1038/386414a0",
      "article-title": "An atypical topoisomerase II from archaea with implications for meiotic recombination",
      "volume": "386",
      "author": "Bergerat",
      "year": "1997",
      "journal-title": "Nature"
    },
    {
      "key": "2022010314113376800_R8",
      "doi-asserted-by": "crossref",
      "first-page": "439",
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      "volume": "69",
      "author": "Bishop",
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      "journal-title": "Cell"
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      "doi-asserted-by": "crossref",
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      "volume": "197",
      "author": "Boeke",
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      "first-page": "51",
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      "volume": "81",
      "author": "Church",
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      "author": "Detloff",
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    },
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      "first-page": "113",
      "DOI": "10.1093/genetics/132.1.113",
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      "volume": "132",
      "author": "Detloff",
      "year": "1992",
      "journal-title": "Genetics"
    },
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      "first-page": "2037",
      "DOI": "10.1128/MCB.16.5.2037",
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      "volume": "16",
      "author": "Fan",
      "year": "1996",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022010314113376800_R21",
      "doi-asserted-by": "crossref",
      "first-page": "1679",
      "DOI": "10.1128/MCB.15.3.1679",
      "article-title": "Meiosis-specific double-strand DNA breaks at the HIS4 recombination hotspot in the yeast Saccharomyces cerevisiae: control in cis and trans",
      "volume": "15",
      "author": "Fan",
      "year": "1995",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022010314113376800_R22",
      "first-page": "89",
      "article-title": "Gene conversion in unselected tetrads from multipoint crosses",
      "author": "Fogel",
      "year": "1971",
      "journal-title": "The Second Stadler Symposia"
    },
    {
      "key": "2022010314113376800_R23",
      "first-page": "289",
      "article-title": "Mechanism of meiotic gene conversion or \u201cwandering on a foreign strand,\u201d",
      "volume-title": "The Molecular Biology of Yeast Saccharomyces",
      "author": "Fogel",
      "year": "1981"
    },
    {
      "key": "2022010314113376800_R24",
      "doi-asserted-by": "crossref",
      "first-page": "159",
      "DOI": "10.1093/genetics/133.2.159",
      "article-title": "A short chromosomal region with major roles in yeast chromosome III meiotic disjunction, recombination and double strand breaks",
      "volume": "133",
      "author": "Goldway",
      "year": "1993",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R25",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1101/SQB.1984.049.01.008",
      "article-title": "Measurement of restoration and conversion: its meaning for the mismatch repair hypothesis of conversion",
      "volume": "49",
      "author": "Hastings",
      "year": "1984",
      "journal-title": "Cold Spring Harbor Symp. Quant. Biol."
    },
    {
      "key": "2022010314113376800_R26",
      "doi-asserted-by": "crossref",
      "first-page": "475",
      "DOI": "10.1046/j.1365-2443.1996.d01-257.x",
      "article-title": "Communication between homologous chromosomes: genetic alterations at a nuclease-hypersensitive site can alter mitotic chromatin structure at that site both in cis and in trans",
      "volume": "1",
      "author": "Keeney",
      "year": "1996",
      "journal-title": "Genes Cells"
    },
    {
      "key": "2022010314113376800_R27",
      "doi-asserted-by": "crossref",
      "first-page": "375",
      "DOI": "10.1016/S0092-8674(00)81876-0",
      "article-title": "Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family",
      "volume": "88",
      "author": "Keeney",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2022010314113376800_R28",
      "doi-asserted-by": "crossref",
      "first-page": "1693",
      "DOI": "10.1093/genetics/149.4.1693",
      "article-title": "Conversion-type and restoration-type repair of DNA mismatches formed during meiotic recombination in Saccharomyces cerevisiae",
      "volume": "149",
      "author": "Kirkpatrick",
      "year": "1998",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R29",
      "doi-asserted-by": "crossref",
      "first-page": "205",
      "DOI": "10.1007/BF02524645",
      "article-title": "Patterns of meiotic double-strand breakage on native and artificial yeast chromosomes",
      "volume": "105",
      "author": "Klein",
      "year": "1996",
      "journal-title": "Chromosoma"
    },
    {
      "key": "2022010314113376800_R30",
      "doi-asserted-by": "crossref",
      "first-page": "5339",
      "DOI": "10.1128/jb.171.10.5339-5346.1989",
      "article-title": "Cloning and nucleotide sequence of DNA mismatch repair gene PMS1 from Saccharomyces cerevisiae: homology of PMS1 to procaryotic MutL and HexB",
      "volume": "171",
      "author": "Kramer",
      "year": "1989",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2022010314113376800_R31",
      "doi-asserted-by": "crossref",
      "first-page": "423",
      "DOI": "10.1146/annurev.ge.29.120195.002231",
      "article-title": "Meiotic recombination hotspots",
      "volume": "29",
      "author": "Lichten",
      "year": "1995",
      "journal-title": "Annu. Rev. Genet."
    },
    {
      "key": "2022010314113376800_R32",
      "doi-asserted-by": "crossref",
      "first-page": "7653",
      "DOI": "10.1073/pnas.87.19.7653",
      "article-title": "Detection of heteroduplex DNA molecules among the products of Saccharomyces cerevisiae meiosis",
      "volume": "87",
      "author": "Lichten",
      "year": "1990",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022010314113376800_R33",
      "doi-asserted-by": "crossref",
      "first-page": "154",
      "DOI": "10.1038/359154a0",
      "article-title": "A meiotic gene conversion gradient opposite to the direction of transcription",
      "volume": "359",
      "author": "Malone",
      "year": "1992",
      "journal-title": "Nature"
    },
    {
      "key": "2022010314113376800_R34",
      "doi-asserted-by": "crossref",
      "first-page": "5",
      "DOI": "10.1093/genetics/137.1.5",
      "article-title": "Analysis of a recombination hotspot for gene conversion occurring at the HIS2 gene of Saccharomyces cerevisiae",
      "volume": "137",
      "author": "Malone",
      "year": "1994",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R35",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1093/genetics/144.1.71",
      "article-title": "Analysis of meiotic recombination pathways in Saccharomyces cerevisiae",
      "volume": "144",
      "author": "Mao-Draayer",
      "year": "1996",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R36",
      "doi-asserted-by": "crossref",
      "first-page": "407",
      "DOI": "10.1101/gad.10.4.407",
      "article-title": "Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair",
      "volume": "10",
      "author": "Marsischky",
      "year": "1996",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022010314113376800_R37",
      "first-page": "2324",
      "article-title": "Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae",
      "volume": "13",
      "author": "Nag",
      "year": "1993",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022010314113376800_R38",
      "doi-asserted-by": "crossref",
      "first-page": "242",
      "DOI": "10.1007/BF01924007",
      "article-title": "Polarity of meiotic gene conversion in fungi: contrasting views",
      "volume": "50",
      "author": "Nicolas",
      "year": "1994",
      "journal-title": "Experientia"
    },
    {
      "key": "2022010314113376800_R39",
      "doi-asserted-by": "crossref",
      "first-page": "528",
      "DOI": "10.1139/g89-101",
      "article-title": "Intermediates in homologous recombination revealed by marker effects in Ascobolus",
      "volume": "31",
      "author": "Nicolas",
      "year": "1989",
      "journal-title": "Genome"
    },
    {
      "key": "2022010314113376800_R40",
      "doi-asserted-by": "crossref",
      "first-page": "35",
      "DOI": "10.1038/338035a0",
      "article-title": "An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae",
      "volume": "338",
      "author": "Nicolas",
      "year": "1989",
      "journal-title": "Nature"
    },
    {
      "key": "2022010314113376800_R41",
      "doi-asserted-by": "crossref",
      "first-page": "5754",
      "DOI": "10.1002/j.1460-2075.1994.tb06913.x",
      "article-title": "Changes in chromatin structure at recombination initiation sites during yeast meiosis",
      "volume": "13",
      "author": "Ohta",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022010314113376800_R42",
      "doi-asserted-by": "crossref",
      "first-page": "3339",
      "DOI": "10.1128/jb.174.10.3339-3347.1992",
      "article-title": "Cloning and characterization of the CYS3 (CYI1) gene of Saccharomyces cerevisiae",
      "volume": "174",
      "author": "Ono",
      "year": "1992",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2022010314113376800_R43",
      "doi-asserted-by": "crossref",
      "first-page": "32",
      "DOI": "10.1139/g93-005",
      "article-title": "Sequencing of chromosome I from Saccharomyces cerevisiae: analysis of a 32 kb region between the LTE1 and SPO7 genes",
      "volume": "36",
      "author": "Ouellette",
      "year": "1993",
      "journal-title": "Genome"
    },
    {
      "key": "2022010314113376800_R44",
      "first-page": "407",
      "article-title": "Recombination in yeast",
      "volume-title": "The Molecular and Cellular Biology of the Yeast Saccharomyces",
      "author": "Petes",
      "year": "1991"
    },
    {
      "key": "2022010314113376800_R45",
      "doi-asserted-by": "crossref",
      "first-page": "1091",
      "DOI": "10.1126/science.8066446",
      "article-title": "MLH1, PMS1, and MSH2 interactions during the initiation of DNA mismatch repair in yeast",
      "volume": "265",
      "author": "Prolla",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "2022010314113376800_R46",
      "doi-asserted-by": "crossref",
      "first-page": "963",
      "DOI": "10.1093/genetics/132.4.963",
      "article-title": "Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins",
      "volume": "132",
      "author": "Reenan",
      "year": "1992",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R47",
      "doi-asserted-by": "crossref",
      "first-page": "975",
      "DOI": "10.1093/genetics/132.4.975",
      "article-title": "Characterization of insertion mutation in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions",
      "volume": "132",
      "author": "Reenan",
      "year": "1992",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R48",
      "doi-asserted-by": "crossref",
      "first-page": "645",
      "DOI": "10.1046/j.1365-2443.1996.00256.x",
      "article-title": "Sensing of nonhomology lowers the initiation of meiotic recombination in yeast",
      "volume": "1",
      "author": "Rocco",
      "year": "1996",
      "journal-title": "Genes Cells"
    },
    {
      "key": "2022010314113376800_R49",
      "doi-asserted-by": "crossref",
      "first-page": "4951",
      "DOI": "10.1073/pnas.76.10.4951",
      "article-title": "Replacement of chromosome segments with altered DNA sequences constructed in vitro",
      "volume": "76",
      "author": "Scherer",
      "year": "1979",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022010314113376800_R50",
      "doi-asserted-by": "crossref",
      "first-page": "813",
      "DOI": "10.1093/genetics/126.4.813",
      "article-title": "Decreasing gradients of gene conversion on both sides of the initiation site for meiotic recombination at the ARG4 locus in yeast",
      "volume": "126",
      "author": "Schultes",
      "year": "1990",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R51",
      "doi-asserted-by": "crossref",
      "first-page": "783",
      "DOI": "10.1016/0092-8674(95)90191-4",
      "article-title": "Identification of double Holliday junctions as intermediates in meiotic recombination",
      "volume": "83",
      "author": "Schwacha",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "2022010314113376800_R52",
      "doi-asserted-by": "crossref",
      "first-page": "965",
      "DOI": "10.1016/S0092-8674(00)81791-2",
      "article-title": "Meiotic recombination in yeast: coronation of the double-strand break repair model",
      "volume": "87",
      "author": "Stahl",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2022010314113376800_R53",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.1038/338087a0",
      "article-title": "Doublestrand breaks at an initiation site for meiotic gene conversion",
      "volume": "338",
      "author": "Sun",
      "year": "1989",
      "journal-title": "Nature"
    },
    {
      "key": "2022010314113376800_R54",
      "doi-asserted-by": "crossref",
      "first-page": "1155",
      "DOI": "10.1016/0092-8674(91)90270-9",
      "article-title": "Extensive 3\u2032-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site",
      "volume": "64",
      "author": "Sun",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2022010314113376800_R55",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1016/0092-8674(83)90331-8",
      "article-title": "The double-strand break repair model for conversion and crossing-over",
      "volume": "33",
      "author": "Szostak",
      "year": "1983",
      "journal-title": "Cell"
    },
    {
      "key": "2022010314113376800_R56",
      "volume-title": "Genetic Recombination, Understanding the Mechanisms.",
      "author": "Whitehouse",
      "year": "1982"
    },
    {
      "key": "2022010314113376800_R57",
      "doi-asserted-by": "crossref",
      "first-page": "235",
      "DOI": "10.1016/S0092-8674(00)80978-2",
      "article-title": "RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling",
      "volume": "88",
      "author": "Wilson",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2022010314113376800_R58",
      "doi-asserted-by": "crossref",
      "first-page": "515",
      "DOI": "10.1126/science.8290959",
      "article-title": "Meiosis-induced double-strand break sites determined by yeast chromatin structure",
      "volume": "263",
      "author": "Wu",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "2022010314113376800_R59",
      "doi-asserted-by": "crossref",
      "first-page": "1115",
      "DOI": "10.1093/genetics/143.3.1115",
      "article-title": "Fine-structure mapping of meiosis-specific double-strand DNA breaks at a recombination hotspot associated with an insertion of telomeric sequence upstream of the HIS4 locus in yeast",
      "volume": "143",
      "author": "Xu",
      "year": "1996",
      "journal-title": "Genetics"
    },
    {
      "key": "2022010314113376800_R60",
      "doi-asserted-by": "crossref",
      "first-page": "530",
      "DOI": "10.1007/BF02426957",
      "article-title": "The distance dependence of the fission yeast ade6-M26 marker effect in two-factor crosses",
      "volume": "29",
      "author": "Zahn-Zabal",
      "year": "1996",
      "journal-title": "Curr. Genet."
    },
    {
      "key": "2022010314113376800_R61",
      "doi-asserted-by": "crossref",
      "first-page": "3441",
      "DOI": "10.1002/j.1460-2075.1992.tb05423.x",
      "article-title": "Multiple sites for double-strand breaks in whole meiotic chromosomes of Saccharomyces cerevisiae",
      "volume": "11",
      "author": "Zenvirth",
      "year": "1992",
      "journal-title": "EMBO J."
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