Abstract
In the yeast, Saccharomyces cerevisiae, several genes appear to act early in meiotic recombination. HOP1 and RED1 have been classified as such early genes. The data in this paper demonstrate that neither a red1 nor a hop1 mutation can rescue the inviable spores produced by a rad52 spo13 strain; this phenotype helps to distinguish these two genes from other early meiotic recombination genes such as SPO11, REC104, or MEI4. In contrast, either a red1 or a hop1 mutation can rescue a rad50S spo13 strain; this phenotype is similar to that conferred by mutations in the other early recombination genes (e.g., REC104). These two different results can be explained because the data presented here indicate that a rad50S mutation does not diminish meiotic intrachromosomal recombination, similar to the mutant phenotypes conferred by red1 or hop1. Of course, RED1 and HOP1 do act in the normal meiotic interchromosomal recombination pathway; they reduce interchromosomal recombination to ~10% of normal levels. We demonstrate that a mutation in a gene (REC104) required for initiation of exchange is completely epistatic to a mutation in RED1. Finally, mutations in either HOP1 or RED1 reduce the number of double-strand breaks observed at the HIS2 meiotic recombination hotspot.
Full Text
The Full Text of this article is available as a PDF (2.4 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ajimura M., Leem S. H., Ogawa H. Identification of new genes required for meiotic recombination in Saccharomyces cerevisiae. Genetics. 1993 Jan;133(1):51–66. doi: 10.1093/genetics/133.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bishop D. K., Park D., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992 May 1;69(3):439–456. doi: 10.1016/0092-8674(92)90446-j. [DOI] [PubMed] [Google Scholar]
- Borts R. H., Lichten M., Haber J. E. Analysis of meiosis-defective mutations in yeast by physical monitoring of recombination. Genetics. 1986 Jul;113(3):551–567. doi: 10.1093/genetics/113.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cao L., Alani E., Kleckner N. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell. 1990 Jun 15;61(6):1089–1101. doi: 10.1016/0092-8674(90)90072-m. [DOI] [PubMed] [Google Scholar]
- Cool M., Malone R. E. Molecular and genetic analysis of the yeast early meiotic recombination genes REC102 and REC107/MER2. Mol Cell Biol. 1992 Mar;12(3):1248–1256. doi: 10.1128/mcb.12.3.1248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Massy B., Baudat F., Nicolas A. Initiation of recombination in Saccharomyces cerevisiae haploid meiosis. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11929–11933. doi: 10.1073/pnas.91.25.11929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donahue T. F., Farabaugh P. J., Fink G. R. The nucleotide sequence of the HIS4 region of yeast. Gene. 1982 Apr;18(1):47–59. doi: 10.1016/0378-1119(82)90055-5. [DOI] [PubMed] [Google Scholar]
- Engebrecht J. A., Voelkel-Meiman K., Roeder G. S. Meiosis-specific RNA splicing in yeast. Cell. 1991 Sep 20;66(6):1257–1268. doi: 10.1016/0092-8674(91)90047-3. [DOI] [PubMed] [Google Scholar]
- Engebrecht J., Roeder G. S. MER1, a yeast gene required for chromosome pairing and genetic recombination, is induced in meiosis. Mol Cell Biol. 1990 May;10(5):2379–2389. doi: 10.1128/mcb.10.5.2379. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engebrecht J., Roeder G. S. Yeast mer1 mutants display reduced levels of meiotic recombination. Genetics. 1989 Feb;121(2):237–247. doi: 10.1093/genetics/121.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedman D. B., Hollingsworth N. M., Byers B. Insertional mutations in the yeast HOP1 gene: evidence for multimeric assembly in meiosis. Genetics. 1994 Feb;136(2):449–464. doi: 10.1093/genetics/136.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Galbraith A. M., Malone R. E. Characterization of REC104, a gene required for early meiotic recombination in the yeast Saccharomyces cerevisiae. Dev Genet. 1992;13(6):392–402. doi: 10.1002/dvg.1020130603. [DOI] [PubMed] [Google Scholar]
- Game J. C., Zamb T. J., Braun R. J., Resnick M., Roth R. M. The Role of Radiation (rad) Genes in Meiotic Recombination in Yeast. Genetics. 1980 Jan;94(1):51–68. doi: 10.1093/genetics/94.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gietz R. D., Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988 Dec 30;74(2):527–534. doi: 10.1016/0378-1119(88)90185-0. [DOI] [PubMed] [Google Scholar]
- Gilbertson L. A., Stahl F. W. Initiation of meiotic recombination is independent of interhomologue interactions. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11934–11937. doi: 10.1073/pnas.91.25.11934. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hinnen A., Hicks J. B., Fink G. R. Transformation of yeast. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1929–1933. doi: 10.1073/pnas.75.4.1929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hollingsworth N. M., Byers B. HOP1: a yeast meiotic pairing gene. Genetics. 1989 Mar;121(3):445–462. doi: 10.1093/genetics/121.3.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hollingsworth N. M., Goetsch L., Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990 Apr 6;61(1):73–84. doi: 10.1016/0092-8674(90)90216-2. [DOI] [PubMed] [Google Scholar]
- Hollingsworth N. M., Johnson A. D. A conditional allele of the Saccharomyces cerevisiae HOP1 gene is suppressed by overexpression of two other meiosis-specific genes: RED1 and REC104. Genetics. 1993 Apr;133(4):785–797. doi: 10.1093/genetics/133.4.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hugerat Y., Simchen G. Mixed segregation and recombination of chromosomes and YACs during single-division meiosis in spo13 strains of Saccharomyces cerevisiae. Genetics. 1993 Oct;135(2):297–308. doi: 10.1093/genetics/135.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ivanov E. L., Korolev V. G., Fabre F. XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics. 1992 Nov;132(3):651–664. doi: 10.1093/genetics/132.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaytor M. D., Livingston D. M. Saccharomyces cerevisiae RAD52 alleles temperature-sensitive for the repair of DNA double-strand breaks. Genetics. 1994 Aug;137(4):933–944. doi: 10.1093/genetics/137.4.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klapholz S., Esposito R. E. Recombination and chromosome segregation during the single division meiosis in SPO12-1 and SPO13-1 diploids. Genetics. 1980 Nov;96(3):589–611. doi: 10.1093/genetics/96.3.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu J., Wu T. C., Lichten M. The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate. EMBO J. 1995 Sep 15;14(18):4599–4608. doi: 10.1002/j.1460-2075.1995.tb00139.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Malone R. E., Bullard S., Hermiston M., Rieger R., Cool M., Galbraith A. Isolation of mutants defective in early steps of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics. 1991 May;128(1):79–88. doi: 10.1093/genetics/128.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Malone R. E., Esposito R. E. Recombinationless meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1981 Oct;1(10):891–901. doi: 10.1128/mcb.1.10.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Malone R. E., Kim S., Bullard S. A., Lundquist S., Hutchings-Crow L., Cramton S., Lutfiyya L., Lee J. Analysis of a recombination hotspot for gene conversion occurring at the HIS2 gene of Saccharomyces cerevisiae. Genetics. 1994 May;137(1):5–18. doi: 10.1093/genetics/137.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Menees T. M., Roeder G. S. MEI4, a yeast gene required for meiotic recombination. Genetics. 1989 Dec;123(4):675–682. doi: 10.1093/genetics/123.4.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nag D. K., Petes T. D. Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1993 Apr;13(4):2324–2331. doi: 10.1128/mcb.13.4.2324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nag D. K., Scherthan H., Rockmill B., Bhargava J., Roeder G. S. Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics. 1995 Sep;141(1):75–86. doi: 10.1093/genetics/141.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991 Sep 20;66(6):1239–1256. doi: 10.1016/0092-8674(91)90046-2. [DOI] [PubMed] [Google Scholar]
- ROMAN H. Studies of gene mutation in Saccharomyces. Cold Spring Harb Symp Quant Biol. 1956;21:175–185. doi: 10.1101/sqb.1956.021.01.015. [DOI] [PubMed] [Google Scholar]
- Rockmill B., Engebrecht J. A., Scherthan H., Loidl J., Roeder G. S. The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics. 1995 Sep;141(1):49–59. doi: 10.1093/genetics/141.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rockmill B., Roeder G. S. A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination. Genes Dev. 1991 Dec;5(12B):2392–2404. doi: 10.1101/gad.5.12b.2392. [DOI] [PubMed] [Google Scholar]
- Rockmill B., Roeder G. S. Meiosis in asynaptic yeast. Genetics. 1990 Nov;126(3):563–574. doi: 10.1093/genetics/126.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rockmill B., Roeder G. S. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6057–6061. doi: 10.1073/pnas.85.16.6057. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rockmill B., Roeder G. S. The yeast med1 mutant undergoes both meiotic homolog nondisjunction and precocious separation of sister chromatids. Genetics. 1994 Jan;136(1):65–74. doi: 10.1093/genetics/136.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roth R., Fogel S. A system selective for yeast mutants deficient in meiotic recombination. Mol Gen Genet. 1971;112(4):295–305. doi: 10.1007/BF00334431. [DOI] [PubMed] [Google Scholar]
- SHERMAN F., ROMAN H. Evidence for two types of allelic recombination in yeast. Genetics. 1963 Feb;48:255–261. doi: 10.1093/genetics/48.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwacha A., Kleckner N. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell. 1994 Jan 14;76(1):51–63. doi: 10.1016/0092-8674(94)90172-4. [DOI] [PubMed] [Google Scholar]
- Sym M., Roeder G. S. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell. 1994 Oct 21;79(2):283–292. doi: 10.1016/0092-8674(94)90197-x. [DOI] [PubMed] [Google Scholar]
- Sym M., Roeder G. S. Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol. 1995 Feb;128(4):455–466. doi: 10.1083/jcb.128.4.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wagstaff J. E., Klapholz S., Waddell C. S., Jensen L., Esposito R. E. Meiotic exchange within and between chromosomes requires a common Rec function in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Dec;5(12):3532–3544. doi: 10.1128/mcb.5.12.3532. [DOI] [PMC free article] [PubMed] [Google Scholar]