Ectodermal Cell Differentiation by Unequal Cell Division in the Stony Coral Acropora tenuis

Background In Anthozoa, the ectoderm contains the epidermis, progenitor/undifferentiated cells, and nerve cells; however, their embryonic origin and development remain unclear. In the stony coral Acropora tenuis , both blastula formation and gastrulation are quite unique. Endodermal cells form by ingression from the presumptive pseudo-archenteron, while ectodermal cell differentiation is poorly understood. Results Ultrastructural studies on A. tenuis showed that the ectoderm consisted of four cell layers stratified apicobasally from the glandular epithelium to yolk cells through undifferentiated-like cells and nerve lineage cells. A 12-hour ‘prawnchip’ embryo had a U-shaped outline devoid of blastocoel. Blastomeres of the embryo were monolayered and the outer blastomeres began to elongate in 17-hour embryos. The elongating blastomeres segregated Snail/Etv6-expressing yolk cells from their growing tips into the narrow blastocoel. In 28-hour ‘donut’ embryos, the nuclei of elongated ectodermal blastomeres translocated to the growing extremities of cells that became the glandular epithelium. Secondary segregation occurred herein in 40-hour embryos to produce ‘bottom’ cells labeled with SoxB2/SoxC near the yolk cells at the bottom of the ectoderm. In 60-hour embryos, the third segregation occurred to produce ‘middle’ cells in the middle region of the ectoderm. The segregated cells expressed lysine-specific demethylase 5 (KDM5) at embryonic stages, and they were tagged by trimethylated histone H3 at lysine 4 at larval stages. Conclusions The present study shows that in A . tenuis embryonic outer blastomeres and the blastomere-derived glandular epithelium expresses Snail, Etv6, C-Jun, SoxB2, SoxC, and KDM5. The glandular epithelium contains founder cells that give rise to yolk cells and progenitor/undifferentiated cells via three steps of unequal cell division. Every segregation accompanies the expression of C-Jun. The initial segregation event accompanies Snail/Etv6 expression, resulting in the yolk cell formation. The secondary and third segregation events accompany SoxB2/SoxC and KDM5, respectively. The former gave rise to nerve progenitors through ‘bottom’ cells, and the latter formed undifferentiated-like cells through ‘middle’ cells. Our results suggest that the ectodermal cell differentiation in Acropora depends on spatiotemporal condition of unequal segregation.