Acquisition of the spindle assembly checkpoint and its modulation by cell fate and cell size in a chordate embryo

The spindle assembly checkpoint (SAC) is a surveillance system that preserves genome integrity by delaying anaphase onset until all chromosomes are correctly attached to spindle microtubules. Recruitment of SAC proteins to unattached kinetochores generates an inhibitory signal that prolongs mitotic duration. Chordate embryos are atypical in that spindle defects do not delay mitotic progression during early development, implying that either the SAC is inactive or the cell-cycle target machinery is unresponsive. Here, we show that in embryos of the chordate Phallusia mammillata, the SAC delays mitotic progression from the 8th cleavage divisions. Unattached kinetochores are not recognized by the SAC machinery until the 7th cell cycle, when the SAC is acquired. After acquisition, SAC strength, which manifests as the degree of mitotic lengthening induced by spindle perturbations, is specific to different cell types and is modulated by cell size, showing similarity to SAC control in early Caenorhabditis elegans embryos. We conclude that SAC acquisition is a process that is likely specific to chordate embryos, while modulation of SAC efficiency in SAC proficient stages depends on cell fate and cell size, which is similar to non-chordate embryos.

Automated summary

The spindle assembly checkpoint (SAC) is responsible for delaying anaphase onset until all chromosomes are correctly attached to spindle microtubules, maintaining genome integrity. In chordate embryos, SAC is inactive or cell-cycle target machinery is unresponsive during early development, allowing mitotic progression despite spindle defects. However, in Phallusia mammillata embryos, the SAC delays mitotic progression from the 8th cleavage divisions and unattached kinetochores are recognized by the SAC machinery after the 7th cell cycle. The strength of SAC and its modulation by cell fate and size resemble SAC control in non-chordate embryos.