The Saccharomyces Cerevisiae ARG4 Initiator of Meiotic Gene Conversion and Its Associated Double-strand DNA Breaks Can Be Inhibited by Transcriptional Interference

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1992 Dec 15

PMID 1465441

Citations 32

Authors

V Rocco

B de Massy

A Nicolas

Affiliations

Soon will be listed here.

Abstract

In the yeast Saccharomyces cerevisiae, as in other eukaryotes, some regions of the genome have a much higher level of meiotic gene conversion than others. Previous deletion analysis indicated that the sequence necessary for the high level of gene conversion within the ARG4 region defined an initiation site located between positions -316 and -37 [relative to the first base pair (+1) of the ARG4 coding sequence] of the ARG4 promoter. To test whether this sequence is sufficient to promote gene conversion in a novel chromosomal context, we inverted on the chromosome various DNA fragments including the implicated region and the ARG4 coding sequence. Surprisingly, these inversions resulted in the loss of the normal recombination properties and double-strand-break formation associated with this process. By Northern analysis, we found that a transcript traverses the ARG4 initiation site in these inversion mutants but not in the wild type. When transcription through this region was prevented by a transcription terminator, the activity of the initiation site and the formation of double-strand breaks were restored. From these results and from complementary deletion analysis in the normal ARG4 orientation, we conclude that the activity of the ARG4 initiation site requires protection from transcriptional interference.

Citing Articles

Extensive Recombination of a Yeast Diploid Hybrid through Meiotic Reversion.

Laureau R, Loeillet S, Salinas F, Bergstrom A, Legoix-Ne P, Liti G PLoS Genet. 2016; 12(2):e1005781.

PMID: 26828862 PMC: 4734685. DOI: 10.1371/journal.pgen.1005781.

Initiation of meiotic homologous recombination: flexibility, impact of histone modifications, and chromatin remodeling.

Szekvolgyi L, Ohta K, Nicolas A Cold Spring Harb Perspect Biol. 2015; 7(5).

PMID: 25934010 PMC: 4448624. DOI: 10.1101/cshperspect.a016527.

Complex minisatellite rearrangements generated in the total or partial absence of Rad27/hFEN1 activity occur in a single generation and are Rad51 and Rad52 dependent.

Lopes J, Ribeyre C, Nicolas A Mol Cell Biol. 2006; 26(17):6675-89.

PMID: 16914748 PMC: 1592832. DOI: 10.1128/MCB.00649-06.

Systematic mutagenesis of the Saccharomyces cerevisiae MLH1 gene reveals distinct roles for Mlh1p in meiotic crossing over and in vegetative and meiotic mismatch repair.

Argueso J, Kijas A, Sarin S, Heck J, Waase M, Alani E Mol Cell Biol. 2003; 23(3):873-86.

PMID: 12529393 PMC: 140715. DOI: 10.1128/MCB.23.3.873-886.2003.

Transcriptional collision between convergent genes in budding yeast.

Prescott E, Proudfoot N Proc Natl Acad Sci U S A. 2002; 99(13):8796-801.

PMID: 12077310 PMC: 124378. DOI: 10.1073/pnas.132270899.

References

Southern E . Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975; 98(3):503-17. DOI: 10.1016/s0022-2836(75)80083-0. View

Beacham I, Schweitzer B, Warrick H, Carbon J . The nucleotide sequence of the yeast ARG4 gene. Gene. 1984; 29(3):271-9. DOI: 10.1016/0378-1119(84)90056-8. View

Schultes N, Szostak J . A poly(dA.dT) tract is a component of the recombination initiation site at the ARG4 locus in Saccharomyces cerevisiae. Mol Cell Biol. 1991; 11(1):322-8. PMC: 359622. DOI: 10.1128/mcb.11.1.322-328.1991. View

Cao L, Alani E, Kleckner N . A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell. 1990; 61(6):1089-101. DOI: 10.1016/0092-8674(90)90072-m. View

Thomas B, Rothstein R . Elevated recombination rates in transcriptionally active DNA. Cell. 1989; 56(4):619-30. DOI: 10.1016/0092-8674(89)90584-9. View

Ciaramella M, Rocco V, PULITZER J . Foreign transcriptional enhancers in yeast. II. Interplay of the polyomavirus transcriptional enhancer and Saccharomyces cerevisiae promoter elements. Nucleic Acids Res. 1988; 16(18):8869-86. PMC: 338640. DOI: 10.1093/nar/16.18.8869. View

Snyder M, Sapolsky R, Davis R . Transcription interferes with elements important for chromosome maintenance in Saccharomyces cerevisiae. Mol Cell Biol. 1988; 8(5):2184-94. PMC: 363400. DOI: 10.1128/mcb.8.5.2184-2194.1988. View

Keil R, Roeder G . Recombination-stimulating sequences in yeast ribosomal DNA correspond to sequences regulating transcription by RNA polymerase I. Cell. 1987; 48(6):1071-9. DOI: 10.1016/0092-8674(87)90714-8. View

Mellor J, Dobson M, Roberts N, Kingsman A, Kingsman S . Factors affecting heterologous gene expression in Saccharomyces cerevisiae. Gene. 1985; 33(2):215-26. DOI: 10.1016/0378-1119(85)90096-4. View

10.

Adhya S, Gottesman M . Promoter occlusion: transcription through a promoter may inhibit its activity. Cell. 1982; 29(3):939-44. DOI: 10.1016/0092-8674(82)90456-1. View

11.

Rothstein R . One-step gene disruption in yeast. Methods Enzymol. 1983; 101:202-11. DOI: 10.1016/0076-6879(83)01015-0. View

12.

Resnick M, Stasiewicz S, Game J . Meiotic DNA metabolism in wild-type and excision-deficient yeast following UV exposure. Genetics. 1983; 104(4):583-601. PMC: 1202128. DOI: 10.1093/genetics/104.4.583. View

13.

ROSS L, Treco D, Nicolas A, Szostak J, Dawson D . Meiotic recombination on artificial chromosomes in yeast. Genetics. 1992; 131(3):541-50. PMC: 1205028. DOI: 10.1093/genetics/131.3.541. View

14.

White M, Detloff P, Strand M, Petes T . A promoter deletion reduces the rate of mitotic, but not meiotic, recombination at the HIS4 locus in yeast. Curr Genet. 1992; 21(2):109-16. DOI: 10.1007/BF00318468. View

15.

Schultes N, Szostak J . Decreasing gradients of gene conversion on both sides of the initiation site for meiotic recombination at the ARG4 locus in yeast. Genetics. 1990; 126(4):813-22. PMC: 1204280. DOI: 10.1093/genetics/126.4.813. View

16.

Sun H, Treco D, Szostak J . Extensive 3'-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell. 1991; 64(6):1155-61. DOI: 10.1016/0092-8674(91)90270-9. View

17.

Alani E, Padmore R, Kleckner N . Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990; 61(3):419-36. DOI: 10.1016/0092-8674(90)90524-i. View

18.

Nicolas A, Treco D, Schultes N, Szostak J . An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature. 1989; 338(6210):35-9. DOI: 10.1038/338035a0. View

19.

Sun H, Treco D, Schultes N, Szostak J . Double-strand breaks at an initiation site for meiotic gene conversion. Nature. 1989; 338(6210):87-90. DOI: 10.1038/338087a0. View

20.

Hirschman J, Durbin K, Winston F . Genetic evidence for promoter competition in Saccharomyces cerevisiae. Mol Cell Biol. 1988; 8(11):4608-15. PMC: 365549. DOI: 10.1128/mcb.8.11.4608-4615.1988. View