Attractive internuclear force drives the collective behavior of nuclear arrays in Drosophila embryos

PLoS Comput Biol. 2021 Nov 19;17(11):e1009605. doi: 10.1371/journal.pcbi.1009605. eCollection 2021 Nov.

Abstract

The collective behavior of the nuclear array in Drosophila embryos during nuclear cycle (NC) 11 to NC14 is crucial in controlling cell size, establishing developmental patterns, and coordinating morphogenesis. After live imaging on Drosophila embryos with light sheet microscopy, we extract the nuclear trajectory, speed, and internuclear distance with an automatic nuclear tracing method. We find that the nuclear speed shows a period of standing waves along the anterior-posterior (AP) axis after each metaphase as the nuclei collectively migrate towards the embryo poles and partially move back. And the maximum nuclear speed dampens by 28-45% in the second half of the standing wave. Moreover, the nuclear density is 22-42% lower in the pole region than the middle of the embryo during the interphase of NC12-14. To find mechanical rules controlling the collective motion and packing patterns of the nuclear array, we use a deep neural network (DNN) to learn the underlying force field from data. We apply the learned spatiotemporal attractive force field in the simulations with a particle-based model. And the simulations recapitulate nearly all the observed characteristic collective behaviors of nuclear arrays in Drosophila embryos.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Behavior, Animal
  • Drosophila / embryology*

Grants and funding

FL received the support from the National Natural Science Foundation of China (http://www.nsfc.gov.cn/) with the grant number 31670852. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.