Abstract
Sexually reproducing eukaryotes use recombination between homologous chromosomes to promote chromosome segregation during meiosis. Meiotic recombination is almost universally conserved in its broad strokes, but specific molecular details often differ considerably between taxa, and the proteins that constitute the recombination machinery show substantial sequence variability. The extent of this variation is becoming increasingly clear because of recent increases in genomic resources and advances in protein structure prediction. We discuss the tension between functional conservation and rapid evolutionary change with a focus on the proteins that are required for the formation and repair of meiotic DNA double-strand breaks. We highlight phylogenetic relationships on different time scales and propose that this remarkable evolutionary plasticity is a fundamental property of meiotic recombination that shapes our understanding of molecular mechanisms in reproductive biology.
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Acknowledgements
The authors apologize to authors whose work could not be cited owing to space limitations. They thank M. Marcet-Ortega for the micrograph of the mouse spermatocyte spread in Fig. 1b. M.A. was supported by an EMBO long-term fellowship (ALTF 905-2019) and a postdoctoral award from the SKI Basic Research Innovation Award Initiative and the Dewitt Wallace Basic Science Award Fund. Research in the Keeney lab is supported in part by National Cancer Institute Cancer Center support grant P30 CA08748, NIH grants R35 GM118092 (to S.K.) and R01 HD110120 (to S.K. and D. Patel) and the Howard Hughes Medical Institute.
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Glossary
- Aneuploidy
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Describes the occurrence of missing or extra chromosomes (or parts of chromosomes) in a cell. Meiotic errors that lead to aneuploidy in gametes can have detrimental consequences for an organism.
- Crossover
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One potential product of the homologous recombination DNA repair pathway. During a crossover event, the DNA flanking the break site is reciprocally exchanged.
- Crossover interference
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Describes the observation that crossovers show a non-random distribution along chromosomes in which presence of a crossover is accompanied by a reduced likelihood of finding another crossover nearby. As a consequence of interference, crossovers tend to be widely and evenly spaced.
- DNA double-strand breaks
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DNA lesions in which both DNA strands are cut. During meiosis, DNA double-strand breaks are essential to initiate homologous recombination.
- Haploidization
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The reduction of the genome complement by half. Haploidization is essential during meiosis to allow the restoration of the genome content at fertilization.
- Homologous chromosomes
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Homologous chromosomes (homologues) in diploid organisms are pairs of chromosomes that contain the same genes but are of different parental origin. During meiosis, homologous chromosomes are paired to achieve segregation.
- Meiotic drivers
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Genetic loci that gain a transmission advantage, not by conferring a fitness advantage, but instead by promoting their inheritance in more than 50% of gametes through manipulation of the meiotic process.
- Molecular evolution
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The study of evolutionary changes at the DNA level. The molecular evolution approaches discussed in this Review aim to distinguish whether protein-coding genes or gene domains experience purifying or positive selection.
- Non-crossover
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A product of homologous recombination in which no reciprocal exchange of chromosome arms happens, and exchange of genetic information (usually non-reciprocal) is limited.
- Positive selection
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Describes a process in which novel genetic variants confer a fitness advantage and thus become fixed in a population. This is in contrast to genetic variants that are neutral and become fixed owing to genetic drift.
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Arter, M., Keeney, S. Divergence and conservation of the meiotic recombination machinery. Nat Rev Genet 25, 309–325 (2024). https://doi.org/10.1038/s41576-023-00669-8
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DOI: https://doi.org/10.1038/s41576-023-00669-8
