Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early development

Abstract

Proper positioning of cells is important for many aspects of embryonic development, tissue homeostasis, and regeneration. A simple mechanism by which cell positions can be specified is via orienting the cell division axis. This axis is specified at the onset of cytokinesis, but can be reoriented as cytokinesis proceeds.Rotatory actomyosin flows have been implied in specifying and reorienting the cell division axis in certain cases, but how general such reorientation events are, and how they are controlled, remains unclear. In this study, we set out to address these questions by investigating early Caenorhabditis elegans development.In particular, we determined which of the early embryonic cell divisions exhibit chiral counter-rotating actomyosin flows, and which do not. We follow the first nine divisions of the early embryo, and discover that chiral counter-rotating flows arise systematically in the early AB lineage, but not in early P/EMS lineage cell divisions. Combining our experiments with thin film active chiral fluid theory we identify specific properties of the actomyosin cortex in the symmetric AB lineage divisions that favor chiral counter-rotating actomyosin flows of the two halves of the dividing cell. Finally, we show that these counter-rotations are the driving force of both the AB lineage spindle skew and cell reorientation events. In conclusion, we here have shed light on the physical basis of lineage-specific actomyosin-based processes that drive chiral morphogenesis during development.Proper positioning of cells is instrumental for many aspects of early embryonic development [1][2][3]. One way to achieve proper cell positioning is via migration [4,5]. Another way by which cell positions can be specified is via the orientation of the cell division axis [6][7][8]. Since the orientation of the mitotic spindle dictates the cell division axis, the orientation of the mitotic spindle at cleavage is instrumental for determining daughter cell positions [9][10][11][12]. This axis can be set at the beginning of cytokinesis, by assembling the mitotic spindle in the correct orientation from the start, or during cytokinesis by reorientation of the mitotic spindle [13][14][15][16][17][18] While several studies highlight the mechanisms that determine the initial orientation of the mitotic spindle at the onset of cytokinesis [15-17, 19, 20] the mechanisms controlling reorientation remain not very well understood. We here set out to investigate cell repositioning during cytokinesis in the early development of the C. elegans nematode. The fully grown hermaphrodite worm consists of exactly 959 somatic cells that are essentially invariant both in terms of position and lineage [21][22][23][24]. Development is deterministic from the start: the one-cell embryo undergoes an asymmetric cell division that gives rise to the AB (somatic) lineage and the P lineage [22,25]. While the anterior daughter cell, AB, undergoes a symmetric cell division into ABa and ABp, the posterior daughter cell, P 1 , divides asymmetrically into...

Establishment of a morphological atlas of the Caenorhabditis elegans embryo using deep-learning-based 4D segmentation

“…Changes in cell shape over time reveal the dynamics of cellular mechanical properties, including, but not limited to, the passive force due to the surrounding environment, stiffness, and adhesion 16,18 . In addition, the changing shapes of cells during development may suggest ongoing cell signal transduction, division, or migration, which are processes specifically associated with cell identity and cell fate 45,54,56 . Our membrane segmentation allows accurate delineation of cell shape dynamics throughout development with a resolution of~1.5 min.…”

spheresDT/Mpacts-PiCS: cell tracking and shape retrieval in membrane-labeled embryos

“…It is unclear if the asymmetry has biological significance as the cells have equivalent lineage potential ( Wood, 1991 ), though it has been observed that ABpl and ABpr behave differently in the compressed embryo ( Jelier et al , 2016 ; Pohl and Bao, 2010 ). One possibility is that the volume difference is a consequence of geometric constraints, as the ABp spindle position is oriented by directed cortical flows ( Naganathan et al , 2014 ; Pimpale et al , 2020 ) that may be affected by the compression of the embryo for imaging, which is supported by our observation that this volume asymmetry disappeared in uncompressed embryos.…”