Genesis of Endoderm from a Syncytial Yolk Cell

It was originally assumed that the supernumerary blast cells described earlier were fated to die after they failed to enter the germinal bands and germinal plate, from which segments arise (Shankland 1984), and that the segmented midgut structures arose exclusively from the three non-D quadrants of the early embryo as proposed by C.O. Whitman in the 19th century, after they had completed producing micromere production, perhaps in combination with the teloblasts after they had ceased dividing (Sawyer 1986; Nardelli-Haefliger and Shankland 1993; Shankland and Savage 1997). As with other aspects of leech segmentation, these assumptions are not entirely correct, and the cellular origins of the segmented midgut are quite interesting.

Generally speaking, the two goals of gut formation for any embryo are (1) to provide a mechanism for digesting the egg’s yolk as fuel for completing development, and (b) to provide a lumenal organ (appropriately connected to feeding and excretory tubes) for storing and digesting food in the adult. There are various morphogenetic strategies by which these goals are achieved in different taxa. In Drosophila, for example, cel- lularization of the syncytial blastoderm generates prospective endodermal cells at the anterior and posterior ends of the embryo, while the bulk of the yolk remains contained in an internal syncytial cell. In later development, the endodermal precursors move inside to cover the yolk, which thus ends up in the lumen of the gut. The situation in oligochaete annelids has not been fully described, but it appears that the non-D mac- romeres continue dividing more or less equally long after the D quadrant teloblasts have formed, making progressively smaller endodermal cells that eventually form a gut tube. If so, then in this case, the maternally provided nutrients are inside the endodermal cells themselves. Whether or not the oligochaete teloblasts contribute to this or remain separate and transition to form the posterior growth zone for post-embryonic development is one of the great remaining questions in our subfield.

In Helobdella, gut formation proceeds by yet another route, involving a series of stepwise cell fusions that lead to a syncytial yolk cell (SYC) with three distinct classes of nuclei (Liu et al. 1998; Desjeux and Price 1999). The endodermal epithelium arises by cellularization of the SYC (Nardelli-Haefliger and Shankland 1993), under the inductive influence of visceral mesoderm (Wedeen and Shankland 1997); this midgut epithelium thus surrounds the yolk within the lumen of the nascent anterior and posterior midgut segments, connected to the foregut and hindgut tubes, neither of which exhibit metamerism.

Cell fusions are monitored and scored by the relatively sudden leakage of injected tracers from one cell to another. In the early embryo, virtually all cells are coupled via gap junctions (Bissen and Weisblat 1989, 1991), but these are impermeable to molecules of great than ~1200 daltons (Simpson et al. 1977), so marker enzymes (e.g., HRP or lacZ) or fluorescently labeled dextrans are initially confined to the cell into which they are injected and its mitotic progeny. The first fusion is between macro- meres A'" and B"' to form SYC A/В; tracer injected into either cell remains confined to that cell until near the end of stage 7, at which time the injected tracer is observed to spread bidirectionally between just these two cells. Intriguingly, the A"'-B"' fusion event depends on an inductive signal from the D quadrant blastomeres (Isaksen et al. 1999). Subsequently, macromere C" fuses with A/В to form SYC A/B/C during late stage 8; and after the teloblasts have formed their entire complements of segmental founder cells, plus a variable number of supernumerary blast cells, the teloblasts and supernumerary blasts cells fuse with the SYC as well. However, since the N and Q teloblasts make roughly twice as many blast cells as do the M and О/P teloblasts, the M and О/P teloblasts have generated their full complements or segmental founder cells and then fuse with the SYC while the N and Q teloblasts are still generating segmental founder cells (Liu et al. 1998; Yoo and Bylsma in preparation).

Thus, the cellular processes by which the segmental repeats in the anterior and posterior midgut (crop and intestine) arise are dramatically different from the stem cell divisions of the PGZ that form segmental ectoderm and mesoderm.

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