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Meiosis: cell-cycle controls shuffle and deal

An Erratum to this article was published on 01 October 2005

Key Points

  • Meiosis is a specialized type of cell division in which two rounds of chromosome segregation follow a single round of DNA replication. In diploid organisms, meiosis generates gametes with a haploid number of chromosomes. Both general cell-cycle regulators and meiosis-specific proteins bring about this modified cell division.

  • Although pre-meiotic S phase uses the same replicative machinery as pre-mitotic S phase, its completion takes longer, probably because interactions between homologous chromosomes (homologues) — such as meiotic recombination, pairing of homologues and the formation of the synaptonemal complex — are being initiated during S phase.

  • Meiosis I is a unique chromosome-segregation event in which homologues segregate away from each other. Meiotic recombination during G2 generates chiasmata, which are important in holding homologues together, in preparation for their segregation during meiosis I.

  • Sister-chromatid cohesion is lost in a stepwise manner during meiosis. In yeast, the loss of the cohesin Rec8 on chromosome arms during meiosis I allows homologues to segregate away from each other. Rec8 at the centromere is retained, however, and holds sister chromatids together until meiosis II. MEI-S332/Sgo1 has an important role in protecting Rec8 from loss at the centromere during meiosis I.

  • In meiosis I, sister chromatids uniquely attach to microtubules from the same pole (monopolar attachment), whereas, in meiosis II, kinetochores attach to microtubules from opposite poles (bipolar attachment). In budding yeast, a complex known as monopolin was identified, which ensures the monopolar attachment of kinetochores during meiosis I.

  • The existence of two consecutive chromosome-segregation events during meiosis, without an intervening S phase, requires specialization of cell-cycle controls to execute the meiosis-I–meiosis-II transition. In some organisms this is achieved by a partial reduction in cyclin-dependent-kinase activity.

Abstract

Meiosis is the type of cell division that gives rise to eggs and sperm. Errors in the execution of this process can result in the generation of aneuploid gametes, which are associated with birth defects and infertility in humans. Here, we review recent findings on how cell-cycle controls ensure the coordination of meiotic events, with a particular focus on the segregation of chromosomes.

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Figure 1: The mitotic and meiotic cell cycles.
Figure 2: Cyclin-dependent-kinase activity in meiosis and mitosis.
Figure 3: The early crossover decision (ECD) model for meiotic recombination.
Figure 4: A model for meiotic chromosome segregation.
Figure 5: A model for the control of pericentromeric and centromeric cohesion in fission yeast.
Figure 6: Kinetochore orientation in mitosis and meiosis.

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Acknowledgements

We are grateful to T. Orr-Weaver and members of the Amon laboratory for their critical reading of this manuscript. We apologize to our colleagues whose work was not discussed in this review due to space limitations.

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DATABASES

Flybase

MEI-S332

Saccharomyces genome database

Cdc5

Cdc14

Cdc28

Chl4

CLB1

CLB3

CLB4

Clb5

Clb6

Csm1

Emi1

Esp1

IME1

IME2

Iml3

Ipl1

Mam1

MUM2

Ndt80

Pds5

Rec8

Scc1

Scc3

Sgo1

Sic1

Smc1

Smc3

Spo11

Spo13

Sum1

Swe1

S. pombe gene database

Bub1

Clr4

Cnp1

Mei2

Mei3

meiRNA

mes1 +

Pat1

Pcs1

Psc3

Rad21

Rec11

Rec12

Sgo2

Swi6

Glossary

HOMOLOGUE

One member of a chromosome pair (where each member of the pair is derived from one parent) in diploid organisms.

CYCLIN-DEPENDENT KINASE

(CDK). A protein kinase that requires an associated cyclin protein for activity. Various CDK–cyclin complexes regulate different stages of the cell cycle.

APC/C

(Anaphase-promoting complex/cyclosome). A ubiquitin ligase which, together with a ubiquitin-conjugating enzyme, attaches ubiquitin peptides to a substrate protein. Ubiquitylated proteins are recognized by the 26S proteasome and are subsequently degraded.

SYNAPTONEMAL COMPLEX

(SC). A proteinaceous structure that forms between two homologues during meiotic G2, which is defined by a state of low CDK activity (when chromosomes are condensed — cytologically speaking, this is prophase).

COHESIN

A protein complex that tethers sister chromatids together.

SISTER CHROMATIDS

Chromosomes that have been duplicated during S phase.

MITOTIC/MEIOTIC SPINDLE

A bipolar array of microtubules that forms during mitosis and meiosis to which chromosomes attach and by which chromosomes are segregated to daughter cells.

CHIASMA

(plural: chiasmata). Cytological manifestation of the point of exchange or crossing over between two homologues due to meiotic recombination.

COHESION

The sticking together of two sister chromatids.

SPINDLE POLE

The yeast equivalent of the centrosome that nucleates microtubules, including those that will form the spindle.

BIVALENT

A pair of homologues that are linked together following meiotic G2, which is defined by a state of low CDK activity (when chromosomes are condensed — cytologically speaking, this is prophase).

SEPARASE

An enzyme that cleaves the cohesin subunit Scc1 or Rec8 during mitosis and meiosis.

CENTROMERE

The region of the DNA on which the kinetochore assembles.

HOLOCENTRIC CHROMOSOME

A chromosome that has centromeres distributed along its length, which are known as diffuse centromeres.

MONOCENTRIC CHROMOSOME

A chromosome with a single centromere.

SECURIN

An inhibitor of separase that keeps the protease inactive until the onset of anaphase, at which point securin is destroyed, thereby liberating separase.

KINETOCHORE

A complex that is composed of a large number of proteins that mediate the attachment of chromosomes to microtubules.

AMPHITELIC

Connection of sister kinetochores to microtubules that emanate from opposite spindle pole bodies.

SYNTELIC

Connection of sister kinetochores to microtubules that emanate from the same spindle pole body.

MONOPOLIN COMPLEX

A protein complex that ensures the syntelic attachment of sister kinetochores during meiosis I.

MEROTELIC

Attachment of a single kinetochore to microtubules from both spindle-pole bodies.

CSF

(cytostatic factor). A cytoplasmic factor that is responsible for the arrest of oocytes at meiosis II.

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Marston, A., Amon, A. Meiosis: cell-cycle controls shuffle and deal. Nat Rev Mol Cell Biol 5, 983–997 (2004). https://doi.org/10.1038/nrm1526

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