Abstract
Asymmetric divisions that yield daughter cells of different sizes are frequent during early embryogenesis, but the importance of such a physical difference for successful development remains poorly understood. Here, we investigated this question using the first division of Caenorhabditis elegans embryos, which yields a large AB cell and a small P1 cell. We equalized AB and P1 sizes using acute genetic inactivation or optogenetic manipulation of the spindle positioning protein LIN-5. We uncovered that only some embryos tolerated equalization, and that there was a size asymmetry threshold for viability. Cell lineage analysis of equalized embryos revealed an array of defects, including faster cell cycle progression in P1 descendants, as well as defects in cell positioning, division orientation, and cell fate. Moreover, equalized embryos were more susceptible to external compression. Overall, we conclude that unequal first cleavage is essential for invariably successful embryonic development of C. elegans.
Highlights
Asymmetric divisions generate cell fate diversity during development and differentiation
To address whether the size difference between AB and P1 that derives from the unequal division of the C. elegans zygote is important for subsequent development, we took advantage of the temperature-sensitive lin-5(ev571) mutant allele (Lorson et al, 2000)
We discovered that shifting lin-5 zygotes from 17 ̊C to 27 ̊C for ~5 min during mitosis results in the spindle remaining in the cell center, yielding AB and P1 cells of more similar sizes than normal (Figure 1A–C, Figure 1—figure supplement 1, Videos 1–3)
Summary
Asymmetric divisions generate cell fate diversity during development and differentiation Daughter cells of such divisions can differ in their asymmetric inheritance of fate determinants and in their relative size. Induced size equalization of the neuroblast division prevents such differentiation despite proper asymmetric inheritance of the neuronal fate determinant Prospero (Cabernard and Doe, 2009; Kitajima et al, 2010). These examples illustrate how size differences can have a drastic consequence on the fate of resulting daughter cells. Unequal divisions are prevalent during early embryogenesis in many systems, but the specific importance of size differences at this early stage for successful completion of development has been scarcely addressed
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