Cell fate analysis of teloblasts in the Tubifex embryo by intracellular injection of HRP

Abstract

As in other clitellate annelids, embryonic development in the oligochaete Tubifex is characterized by the generation of five bilateral pairs of teloblasts (designated M, N, O, P and Q), which serve as embryonic stem cells to produce germ bands on either side of the embryo. A large part of the tissues comprising body segments has been assigned to the progenies of the teloblasts; however, the developmental fate of each teloblast has been inferred only from its initial position in the embryo. In the present study, the fate of the progenies of each teloblast was followed by means of intracellular injection of a tracer enzyme, horseradish peroxidase. Cell fate maps for teloblasts in the Tubifex embryo were constructed. M teloblasts gave rise to nearly all of the mesodermal tissues, which included circular and longitudinal muscles, coelomic walls, nephridia (in segments VII and VIII) and primordial germ cells (in segments X and XI). Although few in number, M teloblasts also contributed cells to the ventral ganglion. Similarly, each of the ectoteloblasts, N, O, P and Q, made a topographically characteristic contribution to the ectodermal tissues such as the nervous system (i.e. ganglionic cells and peripheral neurones) and epidermis, all of which exhibited a segmentally repeated distribution pattern. The P and Q teloblasts uniquely gave rise to additional ectodermal tissues, namely ventral and dorsal setal sacs, respectively. Furthermore, O teloblasts made a contribution to the nephridiopores in segments VII and VIII as well. These results confirm the previously held view that ectoteloblasts and mesoteloblasts are the main source of ectodermal and mesodermal segmental tissues, respectively, but also suggest that all of the teloblasts produce more types of tissue than has previously been thought.

Segment formation in Annelids: patterns, processes and evolution

“…Teloblasts very similar to the leech are found in non-leech clitellates (Tubifex for instance, Goto et al, 1999, Nakamoto et al, 2000. Non-leech clitellates however do not have a determinate number of segments and segments are sequentially added after embryogenesis during juvenile development and also during posterior regeneration.…”

Transient occurrence of vasa-expressing cells in nongenital segments during embryonic development in the oligochaete annelid Tubifex tubifex

“…A previous cell-lineage study has shown that PGCs, which are located in segments X and XI of stage 18 embryos, are derived from the mesodermal teloblast (M) lineage (Goto et al 1999a). …”

“…This animal has testes and ovaries in body segments X and XI, respectively (Dixon 1915). It appears that PGCs are situated in these genital segments as early as the end of embryogenesis (Meyer 1929); it has been demonstrated that these cells are derived from the mesodermal teloblast lineage (Goto et al 1999a). The precise embryonic origin of the PGCs in T. tubifex remains to be determined, however.…”

Expression pattern of annelid Zic in embryonic development of the oligochaete Tubifex tubifex

“…The processes of Tubifex development have been described in previous studies (Shimizu 1982;Goto et al 1999a;Nakamoto et al 2000). Figure 1a summarizes the Tubifex developmental processes relevant to this study; we used this figure as a staging diagram.…”

“…As a model lophotrochozoan animal, the oligochaete annelid Tubifex tubifex, a freshwater sludgeworm, has a body organization that is notable for its clear segmentation (Shimizu 1982;Goto et al 1999a;Nakamoto et al 2000). The ectodermal and mesodermal segmental structures arise from five bilateral pairs of coherent longitudinal columns (bandlets) of blast cells that are formed by five bilateral pairs of embryonic stem cells called teloblasts (named M, N, O, P, and Q).…”