Different roads to form the same gut in nematodes.
The morphogenesis of a gut from the endoderm has been well studied among the animal kingdom and is also well described in the nematode Caenorhabditis elegans. But are there other ways to build a nematode intestine? Sulston et al. (1983) described a different intestinal cell lineage in the species Panagrellus redivivus and Turbatrix aceti that includes two programmed cell deaths. However, no details are known about the three-dimensional (3D) configuration and the role of the cell deaths. Here, we describe the intestinal morphogenesis of P. redivivus and five other nematode species by means of four-dimensional microscopy, which gives us a 3D representation of gut formation at the cellular level. The morphological pathway of gut formation is highly conserved among these distantly related species. However, we found the P. redivivus pattern in another related species Halicephalobus gingivalis. In this pattern, the intestinal precursors migrate inward in concert with the mesoderm precursors. Based on the observations, we propose a hypothesis that could explain the differences. The positions of the mesoderm precursors create a possible spatial constraint, by which the establishment of bilateral symmetry in the intestine is delayed. This symmetry is corrected by cell migrations; other cells are eliminated and compensated by supplementary cell divisions. This pattern leads to the same result as in the other nematodes: a bilateral symmetrical intestine with nine rings. This illustrates how conserved body plans can be achieved by different developmental mechanisms.
Houthoofd
Wouter
W
Department of Biology, Ghent University, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium.
Willems
Maxime
M
Vangestel
Sandra
S
Mertens
Clarinda
C
Bert
Wim
W
Borgonie
Gaëtan
G
D000818:Animals; D005075:Biological Evolution; D002107:Caenorhabditis / Q000196:embryology; D041981:Gastrointestinal Tract / Q000196:embryology*; D009348:Nematoda / Q000196:embryology*; D010802:Phylogeny