Spatial heterogeneity accelerates phase-to-trigger wave transitions in frog egg extracts

Owen Puls, Daniel Ruiz-Reynés, Franco Tavella, Minjun Jin, Yeonghoon Kim, Lendert Gelens () and Qiong Yang ()
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Owen Puls: University of Michigan
Daniel Ruiz-Reynés: Department of Cellular and Molecular Medicine, University of Leuven
Franco Tavella: University of Michigan
Minjun Jin: University of Michigan
Yeonghoon Kim: University of Michigan
Lendert Gelens: Department of Cellular and Molecular Medicine, University of Leuven
Qiong Yang: University of Michigan

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Cyclin-dependent kinase 1 (Cdk1) activity rises and falls throughout the cell cycle: a cell-autonomous process called mitotic oscillations. Mitotic oscillators can synchronize when spatially coupled, facilitating rapid, synchronous divisions in large early embryos of Drosophila (~0.5 mm) and Xenopus (~1.2 mm). Diffusion alone cannot achieve such long-range coordination. Instead, studies proposed mitotic waves—phase and trigger waves—as mechanisms of the coordination. How waves establish over time remains unclear. Using Xenopus laevis egg extracts and a Cdk1 Förster resonance energy transfer sensor, we observe a transition from phase to trigger wave dynamics in initially homogeneous cytosol. Spatial heterogeneity promotes this transition. Adding nuclei accelerates entrainment. The system transitions almost immediately when driven by metaphase-arrested extracts. Numerical simulations suggest phase waves appear transiently as trigger waves take time to entrain the system. Therefore, we show that both waves belong to a single biological process capable of coordinating the cell cycle over long distances.

Date: 2024
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DOI: 10.1038/s41467-024-54752-7

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