Epiblast lumenogenesis is not a mammalian-specific trait

Abstract

Abstract Epiblast lumenogenesis is a hallmark of mammalian embryogenesis, and crucial for the subsequent processes of anterior-posterior patterning and gastrulation. Based on avian model-organisms, reptile epiblasts are thought to form a monolayered flat disc to undergo these developmental events. Here, we report that the squamate, veiled chameleon ( Chameleo calyptratus ), exhibits epiblast lumenogenesis prior to anterior-posterior patterning. Using SEM, immunofluorescence, and histology techniques, we demonstrate that chameleon epiblast lumenogenesis occurs via a purse-string-like mechanism involving the formation and constriction of concentric rings of supracellular actin cables around the epiblast. Through expression analyses of Nodal1 , Nodal2 , Cerberus , Lefty , Brachyury , Wnt3A , and Bmp2 , and immunostaining for Brachyury, we uncovered a Wnt3 A - and Brachyury-positive ring at the edge of the epiblast concomitant with lumenogenesis. Furthermore, our data suggest that anterior-posterior patterning in veiled chameleons may occur independently of Cerberus and Lefty. These processes result in chameleon embryos exhibiting human embryo-like morphology, despite 300 million years of evolutionary separation. Collectively, we show that pre-gastrulation epiblast lumenogenesis is not mammalian-specific but has also evolved in some non-avian reptiles.