Abstract
Cell division orientation is thought to result from a competition between cell geometry and polarity domains controlling the position of the mitotic spindle during mitosis. Depending on the level of cell shape anisotropy or the strength of the polarity domain, one dominates the other and determines the orientation of the spindle. Whether and how such competition is also at work to determine unequal cell division (UCD), producing daughter cells of different size, remains unclear. Here, we show that cell geometry and polarity domains cooperate, rather than compete, in positioning the cleavage plane during UCDs in early ascidian embryos. We found that the UCDs and their orientation at the ascidian third cleavage rely on the spindle tilting in an anisotropic cell shape, and cortical polarity domains exerting different effects on spindle astral microtubules. By systematically varying mitotic cell shape, we could modulate the effect of attractive and repulsive polarity domains and consequently generate predicted daughter cell size asymmetries and position. We therefore propose that the spindle position during UCD is set by the combined activities of cell geometry and polarity domains, where cell geometry modulates the effect of cortical polarity domain(s).
Highlights
The century old observation of cells dividing orthogonal to their long axis applies to somatic cells (Wyatt et al, 2015) or embryos (Minc and Piel, 2012) and is the result of spindle alignment with the longest axis of the cell
Before these three canonical unequal cell divisions (UCDs), the orientation of the third cleavage is thought to be determined by the CAB attracting one mitotic spindle pole thereby conferring the slanted shape of the 8-cell stage embryo with the CAB located in the pair of vegetal-posterior blastomeres B4.1 (Figure 1B) (Negishi et al, 2007)
Our findings reveal spindle tilting in an anisotropic cell shape as a yet unknown mechanism determining UCD
Summary
The century old observation of cells dividing orthogonal to their long axis applies to somatic cells (Wyatt et al, 2015) or embryos (Minc and Piel, 2012) and is the result of spindle alignment with the longest axis of the cell. These deviations from the length-dependent spindle positioning mechanism are usually due to local alteration of microtubule-associated forces by polarity domains Such polarity domains can be cortical enrichment of molecular motors such as Dynein (Grill et al, 2001; Kotak and Gönczy, 2013), polarity proteins such as Ezrin in epithelial cells (Hebert et al, 2012; Korotkevich et al, 2017), or organelles like yolk granules (Pierre et al, 2016) as well as local actomyosin driven tension (Scarpa et al, 2018). This has led to the notion that cell geometry and polarity domains are in direct competition to orient the spindle (Niwayama et al, 2019; Pierre et al, 2016). Whether and how cell geometry and polarity domains compete with each other to determine the orientation and the centering of the mitotic spindle leading to equal or unequal cell divisions (UCDs) remains unclear
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