The Emergent Yo-yo Movement of Nuclei Driven by Cytoskeletal Remodeling in Pseudo-synchronous Mitotic Cycles

Abstract

Many aspects in tissue morphogenesis are attributed to the collective behavior of the participating cells. Yet, the mechanism for emergence of dynamic tissue behavior is not understood completely. Here we report the "yoyo"-like nuclear drift movement in Drosophila syncytial embryo displays typical emergent feature of collective behavior, which is associated with pseudosynchronous nuclear division cycle. We uncover the direct correlation between the degree of asynchrony of mitosis and the nuclear collective movement. Based on experimental manipulations and numerical simulations, we find the ensemble of spindle elongation, rather than a nucleus' own spindle, is the main driving force for its drift movement. The cortical F-actin acts as viscoelastic medium to dampen the movements and plays a critical role in restoring the nuclear positions after a mitosis cycle. Our study provides insights into how the interactions between cytoskeleton as individual elements leads to collective movement of the nuclear array on a macroscopic scale.

Attractive internuclear force drives the collective behavior of nuclear arrays inDrosophilaembryos

“…S14A&B). Consistent with the previous experimental result (Lv et al, 2020), the simulation shows that faster mitotic waves associate with smaller maximum displacement (Fig. S14C).…”

“…S6). This phenomenon is consistent with the recently reported "yo-yo"-like movement (Lv et al, 2020). Interestingly, for each collective motion following with the mitosis wave, the nuclear speed projected to the AP axis shows one period of a 3-node standing wave (Movie S2).…”

“…The emerging collective behaviors during embryogenesis are key to understand the origin of the precise and reproducible morphogenesis (Streichan et al, 2018, Deneke et al, 2019, Lv et al, 2020. In general, complex collective behaviors (such as cytoskeleton filament arrangement, morphogenesis, and bird flocks) arise from interactions between many similar units (such as cytoskeleton macromolecules, cells, and birds) (Vicsek and Zafeiris, 2012).…”

“…At the end of each nuclear cycle, a persuade-synchronized mitotic wave usually starts from the two embryo poles, moves towards the equator of the embryo along the anterior-posterior (AP) axis. A collective "yo-yo"-like nuclear movement follows spindle splitting, i.e., the nuclei move towards the two poles then back nearly to the original position (Lv et al, 2020).…”

“…Several particle-based models have been proposed with different formulas of the pair-wise force between nuclei (Kaiser et al, 2018, Dutta et al, 2019, Lv et al, 2020.…”