Cell shape changes during larval body plan development in Clytia hemisphaerica

Abstract

The cnidarian "planula" larva shows radial symmetry around a polarized, oral-aboral, body axis and comprises two epithelia cell layers, ectodermal and endodermal. This simple body plan is set up during gastrulation, a process which proceeds by a variety of modes amongst the diverse cnidarian species. In the hydrozoan laboratory model Clytia hemisphaerica, gastrulation involves a process termed unipolar cell ingression, in which the endoderm derives from mass epithelial-mesenchymal transition (EMT) at the future oral pole of a monoepithelial blastula. This contrasts markedly from the gastrulation mode in the anthozoan cnidarian Nematostella vectensis, in which endoderm formation primarily relies on cell sheet invagination. To understand the cellular basis of gastrulation in Clytia we have characterized in detail successive cell morphology changes during planula formation by Scanning and Transmission Electron Microscopy combined with confocal imaging. These changes accompany epithialization of the blastoderm, bottle cell formation followed by EMT in the oral domain, cohesive migration and intercalation of ingressed mesenchymal cells, and re-epithelialization of the endoderm. From our data we have reconstructed the cascade of morphogenetic events leading to the formation of planula larva. We also matched the domains of cell morphology changes to the expression of selected regulatory and marker genes expressed during gastrulation. We propose that cell ingression in Clytia not only provides the endoderm, but generates internal forces that shape the embryo in the course of gastrulation. These observations help build a more complete understanding of the cellular basis of morphogenesis and of the evolutionary plasticity of cnidarian gastrulation modes.

Apolar mode of gastrulation leads to the formation of polarized larva in a marine hydroid,Dynamena pumila

“…To study the specification of germ layers and its dynamics in the embryonic development of D. pumila , we visualized the expression of FoxA and Snail, known endodermal markers in hydrozoans (Lapébie et al, 2014; Kraus et al, 2015; Bagaeva et al, 2019; Kraus et al, 2020). For example, their expression is colocalized with an oral region at the beginning of polar gastrulation in C. hemisphaerica (Kraus et al, 2020).…”

“…However, in H. echinata , the blastula always forms at the 16-cell stage (Kraus et al, 2014). Unlike H. echinata , the contact surfaces of blastomeres never exceed free surfaces in length in the blastulae of D. pumila , thus resembling early blastulae in C. hemisphaerica (Kraus et al, 2014; Kraus et al, 2020).…”

“…An embryo of this type can be considered as parenchymula (Figure 8B). Other hydrozoans pass through the parenchymula stage in the course of development as well (Metschnikoff, 1886; Kraus et al, 2014; Burmistrova et al, 2018; Kraus et al, 2020), but this does not always happen during the development of D. pumila . Gastrulation might result in the formation of an embryo with a cavity, which is connected with the external environment through the last unclosed toroidal opening (Figure 8D-F).…”

A flagellate-to-amoeboid switch in the closest living relatives of animals

“…Crawling cell motility is found in virtually all animal lineages and is important for embryonic development (e.g. in neural crest migration [ Berndt et al, 2008 ], gastrulation [ Kraus et al, 2019 ], and primordial germ cell migration [ Grimaldi and Raz, 2020 ; Barton et al, 2016 ; Kardash et al, 2010 ]), wound healing ( Lamouille et al, 2014 ), and immunity (e.g. in phagocytes patrolling tissues [ Kopf et al, 2020 ]).…”

A flagellate-to-amoeboid switch in the closest living relatives of animals

“…Crawling cell motility is found in virtually all animal lineages and is important for embryonic development (e.g. in neural crest migration 65 , gastrulation 66 and primordial germ cell migration 17,18,67 ), wound healing 19 , and immunity (e.g. in phagocytes patrolling tissues 14 ).…”