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Homologous chromosome interactions in meiosis: diversity amidst conservation

Key Points

  • One of the unique aspects of meiosis is the pairing and exchange of information between homologous chromosomes.

  • Recombination is one of the main methods for recognition and pairing of homologous chromosomes.

  • Other methods for recognition and pairing of homologous chromosomes involve cis elements, such as heterochromatin, centromeres and pairing centres, and the nuclear organization of chromosomes that involves chromosome territories and telomeres.

  • In some organisms, such as worms and flies, recombination is dispensable for homologue matching and synapsis, whereas in other organisms, such as yeast and mice, recombination is essential for correct synapsis of homologues.

  • In the face of the high levels of recombination that occur during meiosis, some organisms use other proteins to ensure that recombination occurs appropriately, such as the Dmc1–Mei5–Sae3 and Mnd1–Hop2 complexes. Other organisms require only Rad51.

  • Because different organisms rely to varying extents on different methods for matching and genetic exchange between homologous chromosomes, specific model organisms are better-suited to the elucidation of particular mechanisms.

Abstract

Proper chromosome segregation is crucial for preventing fertility problems, birth defects and cancer. During mitotic cell divisions, sister chromatids separate from each other to opposite poles, resulting in two daughter cells that each have a complete copy of the genome. Meiosis poses a special problem in which homologous chromosomes must first pair and then separate at the first meiotic division before sister chromatids separate at the second meiotic division. So, chromosome interactions between homologues are a unique feature of meiosis and are essential for proper chromosome segregation. Pairing and locking together of homologous chromosomes involves recombination interactions in some cases, but not in others. Although all organisms must match and lock homologous chromosomes to maintain genome integrity throughout meiosis, recent results indicate that the underlying mechanisms vary in different organisms.

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Figure 1: Homologue interactions during meiosis.
Figure 2: Telomere clusters during meiosis in budding yeast.
Figure 3: Visualization of chromosomal bridges in Allium fistulosum and Allium cepa (plant) meiocytes.
Figure 4: The molecular mechanism of meiotic crossover recombination.
Figure 5: A model for Rad51, Dmc1–Mei5–Sae3 and Mnd1–Hop2 function in meiosis.
Figure 6

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Acknowledgements

We thank S. Burgess for helpful comments and for sharing data prior to publication.

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Correspondence to Jennifer L. Gerton.

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DATABASES

Entrez

HIM-17

rec12

Spo11

OMIM

Down syndrome

Klinefelter syndrome

Turner syndrome

FURTHER INFORMATION

Stowers Institute Research Team web site

Glossary

HOLLIDAY JUNCTION

A point at which the strands of two dsDNA molecules exchange partners, which occurs as an intermediate during genetic recombination.

COHESIN

A multi-protein complex that maintains tight association of sister chromatids.

CHROMOSOME TERRITORY

A domain of the nucleus occupied by a pair of homologous chromosomes.

CHIASMA

(Pl. chiasmata.) A cytologically visible physical connection between homologous chromosomes that corresponds to the position of a meiotic cross-over.

HETEROSOMES

Homologous chromosomes that are not identical in appearance; for example, the sex chromosomes.

ASTRAL MICROTUBULES

Microtubules that extend from each pole of the mitotic spindle without attaching to any other visible structure.

CHROMOSOME PAINTING

Fluorescence in situ hybridization (FISH) to chromosomes using a probe that represents a whole chromosome or part of a chromosome.

HETERODUPLEX DNA

DNA that contains a strand from each homologue.

FLUORESCENCE IN SITU HYBRIDIZATION

(FISH). A technique in which a fluorescently labelled DNA probe is used to hybridize with and therefore detect a particular chromosome or gene with the help of fluorescence microscopy.

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Gerton, J., Hawley, R. Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6, 477–487 (2005). https://doi.org/10.1038/nrg1614

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