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.
Highlights
The emerging collective behaviors during embryogenesis are key to understand the origin of the precise and reproducible morphogenesis [1,2,3]
We quantify the collective behaviors of the nuclear array from NC11 to NC14 in intact embryos with light-sheet microscopy and automatic image processing
We discover that during NC11-14 the collective motion of the nuclear array after the mitotic wave shows a damped standing wave, and the stabilized nuclear density after the collective motion is higher in the middle of the embryo
Summary
The emerging collective behaviors during embryogenesis are key to understand the origin of the precise and reproducible morphogenesis [1,2,3]. From NC10 to NC14, the nuclei distribute near the embryo periphery to form a two-dimensional (2D) nuclear array [10,11]. The density of the nuclear array doubles, and the internuclear distance decreases. The spatial and orientation orders increase from early to later nuclear cycles [12], but the radial distribution functions overlap if they are rescaled with the nuclear density [13]. A collective “yo-yo”-like nuclear motion follows the onset of anaphase, i.e., the nuclei move towards the two poles back nearly to the original position [3]
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