Regulation Mechanisms of Meiotic Recombination Revealed from the Analysis of a Fission Yeast Recombination Hotspot

Overview

Journal Biomolecules

Publisher MDPI

Specialties Biochemistry
Molecular Biology

Date 2022 Dec 23

PMID 36551189

Authors

Kouji Hirota

Affiliations

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Abstract

Meiotic recombination is a pivotal event that ensures faithful chromosome segregation and creates genetic diversity in gametes. Meiotic recombination is initiated by programmed double-strand breaks (DSBs), which are catalyzed by the conserved Spo11 protein. Spo11 is an enzyme with structural similarity to topoisomerase II and induces DSBs through the nucleophilic attack of the phosphodiester bond by the hydroxy group of its tyrosine (Tyr) catalytic residue. DSBs caused by Spo11 are repaired by homologous recombination using homologous chromosomes as donors, resulting in crossovers/chiasmata, which ensure physical contact between homologous chromosomes. Thus, the site of meiotic recombination is determined by the site of the induced DSB on the chromosome. Meiotic recombination is not uniformly induced, and sites showing high recombination rates are referred to as recombination hotspots. In fission yeast, , a nonsense point mutation of is a well-characterized meiotic recombination hotspot caused by the heptanucleotide sequence 5'-ATGACGT-3' at the mutation point. In this review, we summarize the meiotic recombination mechanisms revealed by the analysis of the fission gene as a model system.

Citing Articles

Metabolic stress-induced long ncRNA transcription governs the formation of meiotic DNA breaks in the fission yeast fbp1 gene.

Tsuruta Y, Senmatsu S, Oe H, Hoffman C, Hirota K PLoS One. 2024; 19(1):e0294191.

PMID: 38252660 PMC: 10802949. DOI: 10.1371/journal.pone.0294191.

References

Szostak J, Rothstein R, Stahl F . The double-strand-break repair model for recombination. Cell. 1983; 33(1):25-35. DOI: 10.1016/0092-8674(83)90331-8. View

Szankasi P, Heyer W, Schuchert P, Kohli J . DNA sequence analysis of the ade6 gene of Schizosaccharomyces pombe. Wild-type and mutant alleles including the recombination host spot allele ade6-M26. J Mol Biol. 1988; 204(4):917-25. DOI: 10.1016/0022-2836(88)90051-4. View

Hirota K, Miyoshi T, Kugou K, Hoffman C, Shibata T, Ohta K . Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs. Nature. 2008; 456(7218):130-4. DOI: 10.1038/nature07348. View

Vassarotti A, Friesen J . Isolation of the fructose-1,6-bisphosphatase gene of the yeast Schizosaccharomyces pombe. Evidence for transcriptional regulation. J Biol Chem. 1985; 260(10):6348-53. View

Janoo R, Neely L, Braun B, Whitehall S, Hoffman C . Transcriptional regulators of the Schizosaccharomyces pombe fbp1 gene include two redundant Tup1p-like corepressors and the CCAAT binding factor activation complex. Genetics. 2001; 157(3):1205-15. PMC: 1461578. DOI: 10.1093/genetics/157.3.1205. View

Carthew R, Sontheimer E . Origins and Mechanisms of miRNAs and siRNAs. Cell. 2009; 136(4):642-55. PMC: 2675692. DOI: 10.1016/j.cell.2009.01.035. View

Ranjha L, Howard S, Cejka P . Main steps in DNA double-strand break repair: an introduction to homologous recombination and related processes. Chromosoma. 2018; 127(2):187-214. DOI: 10.1007/s00412-017-0658-1. View

Hirota K, Steiner W, Shibata T, Ohta K . Multiple modes of chromatin configuration at natural meiotic recombination hot spots in fission yeast. Eukaryot Cell. 2007; 6(11):2072-80. PMC: 2168419. DOI: 10.1128/EC.00246-07. View

Ponticelli A, Smith G . Chromosomal context dependence of a eukaryotic recombinational hot spot. Proc Natl Acad Sci U S A. 1992; 89(1):227-31. PMC: 48209. DOI: 10.1073/pnas.89.1.227. View

10.

Zhou X, Wu X, Lai K, Zhou R, Chen Z, Yang Z . Discovery of the hidden coding information in cancers: Mechanisms and biological functions. Int J Cancer. 2022; 153(1):20-32. DOI: 10.1002/ijc.34360. View

11.

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

12.

Mieczkowski P, Dominska M, Buck M, Gerton J, Lieb J, Petes T . Global analysis of the relationship between the binding of the Bas1p transcription factor and meiosis-specific double-strand DNA breaks in Saccharomyces cerevisiae. Mol Cell Biol. 2006; 26(3):1014-27. PMC: 1347019. DOI: 10.1128/MCB.26.3.1014-1027.2006. View

13.

Panizza S, Mendoza M, Berlinger M, Huang L, Nicolas A, Shirahige K . Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell. 2011; 146(3):372-83. DOI: 10.1016/j.cell.2011.07.003. View

14.

Meselson M, Radding C . A general model for genetic recombination. Proc Natl Acad Sci U S A. 1975; 72(1):358-61. PMC: 432304. DOI: 10.1073/pnas.72.1.358. View

15.

Cromie G, Hyppa R, Taylor A, Zakharyevich K, Hunter N, Smith G . Single Holliday junctions are intermediates of meiotic recombination. Cell. 2006; 127(6):1167-78. PMC: 2803030. DOI: 10.1016/j.cell.2006.09.050. View

16.

Gutz H . Site Specific Induction of Gene Conversion in SCHIZOSACCHAROMYCES POMBE. Genetics. 1971; 69(3):317-37. PMC: 1212708. DOI: 10.1093/genetics/69.3.317. View

17.

Fisher C . Enzymology of the pigmented adenine-requiring mutants of Saccharomyces and Schizosaccharomyces. Biochem Biophys Res Commun. 1969; 34(3):306-10. DOI: 10.1016/0006-291x(69)90832-8. View

18.

Zickler D, Kleckner N . Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 2000; 33:603-754. DOI: 10.1146/annurev.genet.33.1.603. View

19.

Lascarez-Lagunas L, Martinez-Garcia M, Colaiacovo M . SnapShot: Meiosis - Prophase I. Cell. 2020; 181(6):1442-1442.e1. DOI: 10.1016/j.cell.2020.04.038. View

20.

PLOUGH H . The Effect of Temperature on Linkage in the Second Chromosome of Drosophila. Proc Natl Acad Sci U S A. 1917; 3(9):553-5. PMC: 1091318. DOI: 10.1073/pnas.3.9.553. View