The spindle assembly checkpoint functions during early development in non-chordate embryos

Abstract

In eukaryotic cells, a spindle assembly checkpoint (SAC) ensures accurate chromosome segregation. This control mechanism monitors proper attachment of chromosomes to spindle microtubules and delays mitotic progression if connections are erroneous or absent. The SAC operates in all eukaryotic cells tested so far, but is thought to be relaxed during early embryonic development in animals. Here, we evaluate the checkpoint response to lack of kinetochore-spindle microtubule interactions in early embryos of diverse animal species from the main metazoan groups. Our analysis shows that there are two classes of embryos, either proficient or deficient for SAC activation during cleavage. Sea urchins, mussels and jellyfish embryos show a prolonged mitotic block in the absence of spindle microtubules from the first cleavage division, while ascidian and amphioxus embryos, like those of Xenopus and zebrafish, continue mitotic cycling without delay. SAC competence during early development shows no correlation with cell size, chromosome number or kinetochore to cell volume ratio, ruling out the hypothesis that lack of checkpoint activity in early embryos is due to the large egg volume. Our results instead indicate that there is no inherent incompatibility between SAC activity and large fast-dividing embryonic cells. We suggest that SAC proficiency is the default situation of metazoan embryos, and that SAC activity is specifically silenced in chordate species with fast dividing embryos.