A compartmentalized signaling network mediates crossover control in meiosis

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Abstract

During meiosis, each pair of homologous chromosomes typically undergoes at least one crossover (crossover assurance), but these exchanges are strictly limited in number and widely spaced along chromosomes (crossover interference). The molecular basis for this chromosome-wide regulation remains mysterious. A family of meiotic RING finger proteins has been implicated in crossover regulation across eukaryotes. Caenorhabditis elegans expresses four such proteins, of which one (ZHP-3) is known to be required for crossovers. Here we investigate the functions of ZHP-1, ZHP-2, and ZHP-4. We find that all four ZHP proteins, like their homologs in other species, localize to the synaptonemal complex, an unusual, liquid crystalline compartment that assembles between paired homologs. Together they promote accumulation of pro-crossover factors, including ZHP-3 and ZHP-4, at a single recombination intermediate, thereby patterning exchanges along each chromosome. These proteins also act at the top of a hierarchical, symmetry-breaking process that enables crossovers to direct accurate chromosome segregation.

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Liangyu Zhang

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Simone Köhler

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Regina Rillo-Bohn

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Abby F Dernburg

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

For correspondence
afdernburg@lbl.gov

Competing interests
Abby F Dernburg, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0001-8037-1079

Funding

National Institute of General Medical Sciences (GM065591)

Abby F Dernburg

Howard Hughes Medical Institute

Liangyu Zhang
Regina Rillo-Bohn
Abby F Dernburg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.