Beta-catenin patterns the cell cycle during maternal-to-zygotic transition in urochordate embryos

Abstract

During the transition from maternal to zygotic control of development, cell cycle length varies in different lineages, and this is important for their fates and functions. The maternal to zygotic transition (MZT) in metazoan embryos involves a profound remodeling of the cell cycle: S phase length increases then G2 is introduced. Although β-catenin is the master regulator of endomesoderm patterning at MZT in all metazoans, the influence of maternal β-catenin on the cell cycle at MZT remains poorly understood. By studying urochordate embryogenesis we found that cell cycle remodeling during MZT begins with the formation of 3 mitotic domains at the 16-cell stage arising from differential S phase lengthening, when endomesoderm is specified. Then, at the 64-cell stage, a G2 phase is introduced in the endoderm lineage during its specification. Strikingly, these two phases of cell cycle remodeling are patterned by β-catenin-dependent transcription. Functional analysis revealed that, at the 16-cell stage, β-catenin speeds up S phase in the endomesoderm. In contrast, two cell cycles later at gastrulation, nuclear β-catenin induces endoderm fate and delays cell division. Such interphase lengthening in invaginating cells is known to be a requisite for gastrulation movements. Therefore, in basal chordates β-catenin has a dual role to specify germ layers and remodel the cell cycle.

Keywords: Ascidian; Cell cycle; Gastrulation; MBT; S phase; Urochordate.