Control of Meiotic Recombination and Gene Expression in Yeast by a Simple Repetitive DNA Sequence That Excludes Nucleosomes

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 1999 Oct 19

PMID 10523654

Citations 33

Authors

D T Kirkpatrick

Y H Wang

M Dominska

J D Griffith

T D Petes

Affiliations

Soon will be listed here.

Abstract

Tandem repeats of the pentanucleotide 5'-CCGNN (where N indicates any base) were previously shown to exclude nucleosomes in vitro (Y. -H. Wang and J. D. Griffith, Proc. Natl. Acad. Sci. USA 93:8863-8867, 1996). To determine the in vivo effects of these sequences, we replaced the upstream regulatory sequences of the HIS4 gene of Saccharomyces cerevisiae with either 12 or 48 tandem copies of CCGNN. Both tracts activated HIS4 transcription. We found that (CCGNN)(12) tracts elevated meiotic recombination (hot spot activity), whereas the (CCGNN)(48) tract repressed recombination (cold spot activity). In addition, a "pure" tract of (CCGAT)(12) activated both transcription and meiotic recombination. We suggest that the cold spot activity of the (CCGNN)(48) tract is related to the phenomenon of the suppressive interactions of adjacent hot spots previously described in yeast (Q.-Q. Fan, F. Xu, and T. D. Petes, Mol. Cell. Biol. 15:1679-1688, 1995; Q.-Q. Fan, F. Xu, M. A. White, and T. D. Petes, Genetics 145:661-670, 1997; T.-C. Wu and M. Lichten, Genetics 140:55-66, 1995; L. Xu and N. Kleckner, EMBO J. 16:5115-5128, 1995).

Citing Articles

The impact of poly-A microsatellite heterologies in meiotic recombination.

Heissl A, Betancourt A, Hermann P, Povysil G, Arbeithuber B, Futschik A Life Sci Alliance. 2019; 2(2).

PMID: 31023833 PMC: 6485458. DOI: 10.26508/lsa.201900364.

The effects of transcription and recombination on mutational dynamics of short tandem repeats.

Zavodna M, Bagshaw A, Brauning R, Gemmell N Nucleic Acids Res. 2018; 46(3):1321-1330.

PMID: 29300948 PMC: 5814968. DOI: 10.1093/nar/gkx1253.

Functional Mechanisms of Microsatellite DNA in Eukaryotic Genomes.

Bagshaw A Genome Biol Evol. 2017; 9(9):2428-2443.

PMID: 28957459 PMC: 5622345. DOI: 10.1093/gbe/evx164.

Crossing-over in a hypervariable species preferentially occurs in regions of high local similarity.

Seplyarskiy V, Logacheva M, Penin A, Baranova M, Leushkin E, Demidenko N Mol Biol Evol. 2014; 31(11):3016-25.

PMID: 25135947 PMC: 4209137. DOI: 10.1093/molbev/msu242.

The Drosophila early ovarian transcriptome provides insight to the molecular causes of recombination rate variation across genomes.

Adrian A, Comeron J BMC Genomics. 2013; 14:794.

PMID: 24228734 PMC: 3840681. DOI: 10.1186/1471-2164-14-794.

References

Kornberg R . Structure of chromatin. Annu Rev Biochem. 1977; 46:931-54. DOI: 10.1146/annurev.bi.46.070177.004435. View

Wang Y, Griffith J . The [(G/C)3NN]n motif: a common DNA repeat that excludes nucleosomes. Proc Natl Acad Sci U S A. 1996; 93(17):8863-7. PMC: 38559. DOI: 10.1073/pnas.93.17.8863. View

Lichten M, Goldman A . Meiotic recombination hotspots. Annu Rev Genet. 1995; 29:423-44. DOI: 10.1146/annurev.ge.29.120195.002231. View

Lambie E, Roeder G . Repression of meiotic crossing over by a centromere (CEN3) in Saccharomyces cerevisiae. Genetics. 1986; 114(3):769-89. PMC: 1203013. DOI: 10.1093/genetics/114.3.769. View

Tsukiyama T, Wu C . Chromatin remodeling and transcription. Curr Opin Genet Dev. 1997; 7(2):182-91. DOI: 10.1016/s0959-437x(97)80127-x. View

Ekwall K, Ruusala T . Mutations in rik1, clr2, clr3 and clr4 genes asymmetrically derepress the silent mating-type loci in fission yeast. Genetics. 1994; 136(1):53-64. PMC: 1205792. DOI: 10.1093/genetics/136.1.53. View

Fan Q, Xu F, Petes T . Meiosis-specific double-strand DNA breaks at the HIS4 recombination hot spot in the yeast Saccharomyces cerevisiae: control in cis and trans. Mol Cell Biol. 1995; 15(3):1679-88. PMC: 230392. DOI: 10.1128/MCB.15.3.1679. View

Shimada T, Inokuchi K, Nienhuis A . Chromatin structure of the human dihydrofolate reductase gene promoter. Multiple protein-binding sites. J Biol Chem. 1986; 261(3):1445-52. View

Griffith J . Chromatin structure: deduced from a minichromosome. Science. 1975; 187(4182):1202-3. DOI: 10.1126/science.187.4182.1202. View

10.

Ohta K, Shibata T, Nicolas A . Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO J. 1994; 13(23):5754-63. PMC: 395541. DOI: 10.1002/j.1460-2075.1994.tb06913.x. View

11.

Arndt K, Styles C, Fink G . Multiple global regulators control HIS4 transcription in yeast. Science. 1987; 237(4817):874-80. DOI: 10.1126/science.3303332. View

12.

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

13.

White M, Dominska M, Petes T . Transcription factors are required for the meiotic recombination hotspot at the HIS4 locus in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1993; 90(14):6621-5. PMC: 46984. DOI: 10.1073/pnas.90.14.6621. View

14.

Detloff P, White M, Petes T . Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae. Genetics. 1992; 132(1):113-23. PMC: 1205110. DOI: 10.1093/genetics/132.1.113. View

15.

Hartzog G, Winston F . Nucleosomes and transcription: recent lessons from genetics. Curr Opin Genet Dev. 1997; 7(2):192-8. DOI: 10.1016/s0959-437x(97)80128-1. View

16.

Symington L, Petes T . Meiotic recombination within the centromere of a yeast chromosome. Cell. 1988; 52(2):237-40. DOI: 10.1016/0092-8674(88)90512-0. View

17.

Wijgerde M, Grosveld F, Fraser P . Transcription complex stability and chromatin dynamics in vivo. Nature. 1995; 377(6546):209-13. DOI: 10.1038/377209a0. View

18.

Kornberg R, Lorch Y . Chromatin structure and transcription. Annu Rev Cell Biol. 1992; 8:563-87. DOI: 10.1146/annurev.cb.08.110192.003023. View

19.

Fan Q, Xu F, White M, Petes T . Competition between adjacent meiotic recombination hotspots in the yeast Saccharomyces cerevisiae. Genetics. 1997; 145(3):661-70. PMC: 1207851. DOI: 10.1093/genetics/145.3.661. View

20.

Devlin C, Shore D, Arndt K . RAP1 is required for BAS1/BAS2- and GCN4-dependent transcription of the yeast HIS4 gene. Mol Cell Biol. 1991; 11(7):3642-51. PMC: 361116. DOI: 10.1128/mcb.11.7.3642-3651.1991. View