The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation

Abstract

Continued elongation of the archenteron during sea urchin gastrulation has long been thought to occur as a result of contraction of filopodia which are extended by secondary mesenchyme cells from the tip of the gut rudiment to the blastocoel roof. Here we present four lines of evidence which strongly suggest that forces generated within the archenteron itself can cause it to elongate. First, computer simulations based on the theory of solid mechanics show that filopodial pulling alone results in deformations not seen in vivo, and that observed shape changes can only be obtained by assuming that the archenteron is much less stiff than the rest of the embryo. Second, our transverse tissue sections of Strongylocentrotus purpuratus and similar sections of Lytechinus pictus reveal a marked decrease in the number of cells comprising the circumference of the archenteron during its elongation, demonstrating that the cells in the archenteron repack to form a longer, narrower array. Third, morphometric analysis of Nomarski DIC micrographs indicates no significant increase in the length/width ratios of cells in the archenteron due to filopodial pulling. Finally, L. pictus and S. purpuratus exogastrulae induced by treatment with 10 m M LiCl show complete gut extension accompanied by cell repacking without the action of secondary mesenchyme cells. These results strongly suggest that, in addition to any passive lengthening which may occur, the gut rudiment itself possesses an inherent capacity to elongate independent of filopodial pulling. On the basis of these findings, we propose that in at least some species, active cell rearrangement in the wall of the archenteron is the major contributing factor in the elongation of the gut rudiment, while the filopodia may primarily serve to guide the archenteron to the site of stomadeum formation.