Nucleolar Cdc14 Splitting Reflects Recombination Context and Meiotic Chromosome Dynamics

TL;DR

This study explores how chromosome movements during meiosis affect nucleolar structure, revealing that nucleolar splitting reflects chromosome dynamics independent of DNA breaks.

Contribution

The study introduces a novel framework linking nucleolar architecture to meiotic chromosome dynamics, independent of DNA recombination.

Findings

Nucleolar Cdc14 splitting increases when homolog engagement is disrupted, independent of DNA breaks.

Splitting correlates with chromosome-scale forces like telomere clustering and centromere pairing.

Population checkpoint readouts do not fully explain nucleolar splitting patterns.

Abstract

Chromosome dynamics, recombination, and nucleolar organization intersect during meiotic prophase I, yet how the recombination context influences nucleolar architecture remains unclear. We analyzed the nucleolar pool of Cdc14 in Saccharomyces cerevisiae under matched prophase I gating and a uniform, frame-based operational definition of transient two-focus episodes. In a prophase-arrest reference, Cdc14–mCherry formed a predominant single nucleolar focus with occasional, reversible two-focus episodes that Nop56–GFP placed within the nucleolar compartment (nucleolar splitting). Splitting rose sharply when interhomolog recombination was compromised and remained elevated when Spo11 catalytic activity was abolished, indicating that increased DSB formation is not required and pointing instead to the homolog engagement state as a key variable. Population checkpoint readouts did not map onto the phenotype: Hop1 phosphorylation differed strongly across genotypes, yet splitting remained high in recombination-defective and DSB-free contexts and low in the reference. Timing analyses showed that events concentrated early and declined in the reference, whereas recombination-defective and DSB-free backgrounds retained activity into later windows across thresholds. We propose that nucleolar splitting reflects a rheological response of the nucleolus to chromosome-scale forces that vary with homolog engagement, consistent with contributions from DSB-independent chromosome dynamics such as telomere clustering, telomere-led rapid prophase movements, and centromere coupling/pairing. Together, these data support the nucleolus as a mesoscale, mechanically sensitive readout of meiotic chromosome dynamics.

Figures