Abstract
In Cnidaria, modes of gastrulation to produce the two body layers vary greatly between species. In the hydrozoan species Clytia hemisphaerica gastrulation involves unipolar ingression of presumptive endoderm cells from an oral domain of the blastula, followed by migration of these cells to fill the blastocoel with concomitant narrowing of the gastrula and elongation along the oral-aboral axis. We developed a 2D computational boundary model capable of simulating the morphogenetic changes during embryonic development from early blastula stage to the end of gastrulation. Cells are modeled as polygons with elastic membranes and cytoplasm, colliding and adhering to other cells, and capable of forming filopodia. With this model we could simulate compaction of the embryo preceding gastrulation, bottle cell formation, ingression, and intercalation between cells of the ingressing presumptive endoderm. We show that embryo elongation is dependent on the number of endodermal cells, low endodermal cell-cell adhesion, and planar cell polarity (PCP). When the strength of PCP is reduced in our model, resultant embryo morphologies closely resemble those reported previously following morpholino-mediated knockdown of the core PCP proteins Strabismus and Frizzled. Based on our results, we postulate that cellular processes of apical constriction, compaction, ingression, and then reduced cell-cell adhesion and mediolateral intercalation in the presumptive endoderm, are required and when combined, sufficient for Clytia gastrulation.
Highlights
The process of gastrulation sets up the germ layers and fixes the embryonic axes to define the animal body plan
Cnidarian gastrulation includes a rich variety of modes (Kraus and Markov, 2017), of which two extreme modes are seen in the main laboratory model species Nematostella vectensis from Anthozoa and Clytia hemisphaerica from Hydrozoa
Nematostella gastrulation is largely based on invagination of the future “oral” side of the blastoderm corresponding to the presumptive endoderm territory (Kraus and Technau, 2006; Magie and Daly, 2007), while in Clytia (1⁄4 Phialidium) species, the endoderm forms entirely from cells detaching individually from the blastoderm at the future oral pole and migrating inward to fill the blastocoel, a process known as unipolar ingression (Byrum, 2001)
Summary
The process of gastrulation sets up the germ layers and fixes the embryonic axes to define the animal body plan. Species in the sister clade Cnidaria are considered “diploblastic”, i.e. they have only two germ layers, ectoderm and endoderm (sometimes termed entoderm) Within both Bilateria and Cnidaria the details of gastrulation vary between species, with specific cell populations of the single-layered blastula undergoing, in different combinations, cell sheet invagination, involution and epiboly as well as individual cell delamination and ingression (Gilbert, 2010). Nematostella gastrulation is largely based on invagination of the future “oral” side of the blastoderm corresponding to the presumptive endoderm territory (Kraus and Technau, 2006; Magie and Daly, 2007), while in Clytia (1⁄4 Phialidium) species, the endoderm forms entirely from cells detaching individually from the blastoderm at the future oral pole and migrating inward to fill the blastocoel, a process known as unipolar ingression (Byrum, 2001). While Nematostella invagination-based gastrulation has been described in detail and simulated (Tamulonis et al, 2011), little is yet known about the mechanical basis of hydrozoan gastrulation by unipolar ingression
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