An Equatorial Contractile Mechanism Drives Cell Elongation but not Cell Division

Abstract

A cytokinesis-like contractile mechanism is co-opted in a different developmental scenario to achieve cell elongation instead of cell division in Ciona intestinalis.

Abstract

Cell shape changes and proliferation are two fundamental strategies for morphogenesis in animal development. During embryogenesis of the simple chordate Ciona intestinalis, elongation of individual notochord cells constitutes a crucial stage of notochord growth, which contributes to the establishment of the larval body plan. The mechanism of cell elongation is elusive. Here we show that although notochord cells do not divide, they use a cytokinesis-like actomyosin mechanism to drive cell elongation. The actomyosin network forming at the equator of each notochord cell includes phosphorylated myosin regulatory light chain, α-actinin, cofilin, tropomyosin, and talin. We demonstrate that cofilin and α-actinin are two crucial components for cell elongation. Cortical flow contributes to the assembly of the actomyosin ring. Similar to cytokinetic cells, membrane blebs that cause local contractions form at the basal cortex next to the equator and participate in force generation. We present a model in which the cooperation of equatorial actomyosin ring-based constriction and bleb-associated contractions at the basal cortex promotes cell elongation. Our results demonstrate that a cytokinesis-like contractile mechanism is co-opted in a completely different developmental scenario to achieve cell shape change instead of cell division. We discuss the occurrences of actomyosin rings aside from cell division, suggesting that circumferential contraction is an evolutionally conserved mechanism to drive cell or tissue elongation.

Author Summary

The actomyosin cytoskeleton is the primary force that drives cell shape changes. These fibers are organized in elaborate structures that form sarcomeres in the muscle and the contractile ring during cytokinesis. In cytokinesis, the establishment of an equatorial actomyosin ring is preceded and regulated by many cell cycle events, and the ring itself is a complex and dynamic structure. Here we report the presence of an equatorial circumferential actomyosin structure with remarkable similarities to the cytokinetic ring formed in postmitotic notochord cells of sea squirt Ciona intestinalis. The notochord is a transient rod-like structure found in all embryos that belong to the phylum Chordata, and in Ciona, a simple chordate, it consists of only 40 cylindrical cells arranged in a single file, which elongate individually during development. Our study shows that the activity of the equatorial actomyosin ring is required for the elongation of the notochord cells. We also find that cortical flow contributes significantly to the formation of the ring at the equator. Similar to cytokinetic cells, we observe the formation of membrane blebs outside the equatorial region. Our analyses suggest that cooperation of actomyosin ring-based circumferential constriction and bleb-associated contractions drive cell elongation in Ciona. We conclude that cells can utilize a cytokinesis-like force generation mechanism to promote cell shape change instead of cell division.