Amniogenesis occurs in two independent waves in primates

In primates, the amnion emerges through cavitation of the epiblast during implantation, whereas in other species it does so later at gastrulation by the folding of the ectoderm. How the mechanisms of amniogenesis diversified during evolution remains unknown. Unexpectedly, single-cell analysis of primate embryos uncovered two transcriptionally and temporally distinct amniogenesis waves. To study this, we employed the naive-to-primed transition of human pluripotent stem cells (hPSCs) to model peri-implantation epiblast development. Partially primed hPSCs transiently gained the ability to differentiate into cavitating epithelium that transcriptionally and morphologically matched the early amnion, whereas fully primed hPSCs produced cells resembling the late amnion instead, thus recapitulating the two independent differentiation waves. The early wave follows a trophectoderm-like pathway and encompasses cavitation, whereas the late wave resembles an ectoderm-like route during gastrulation. The discovery of two independent waves explains how amniogenesis through cavitation could emerge during evolution via duplication of the pre-existing trophectoderm program.

Automated summary

Two transcriptionally and temporally distinct waves of amniogenesis were uncovered in primate embryos, with one resembling trophectoderm-like pathway and the other resembling an ectoderm-like route. Using human pluripotent stem cells, researchers were able to model the peri-implantation epiblast development and recapitulate the two independent differentiation waves, providing insights into the diversification of amniogenesis mechanisms during evolution.