Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages

Ctenophores are marine invertebrates that develop rapidly and directly into juvenile adults. They are likely to be the simplest metazoans possessing d efinitive muscle cells and are possibly the sister group to the Bilateria. All ctenophore embryos display a highly stereotyped, phylum-specific patter n of development in which every cell can be identified by its lineage histo ry. We generated a cell lineage fate map for Mnemiopsis leidyi by injecting fluorescent lineage tracers into individual blastomeres up through the 60- cell stage. The adult ctenophore body plan is composed of four nearly ident ical quadrants organized along the oral-aboral axis. Each of the four quadr ants is derived largely from one cell of the four-cell-stage embryo. At the eight-cell stage each quadrant contains a single E ("end") and M ("middle" ) blastomere. Subsequently, micromeres are formed first at the aboral pole and later at the oral pole. The ctene rows, apical organ, and tentacle appa ratus are complex structures that are generated by both E and M blastomere lineages from all four quadrants. All muscle cells are derived from microme res born at the oral pole of endomesodermal precursors (2M and 3E macromere s). While the development of the four quadrants is similar, diagonally oppo sed quadrants share more similarities than adjacent quadrants. Adult ctenop hores possess two diagonally opposed endodermal anal canals that open at th e base of the apical organ. These two structures are derived from the two d iagonally opposed 2M\ macromeres. The two opposing 2M/ macromeres generated a unique set of circumpharyngeal muscle cells, but do not contribute to th e anal canals. No other lineages displayed such diagonal asymmetries. Clone s from each blastomere yielded regular, but not completely invariant patter ns of descendents. Ectodermal descendents normally, but not always, remaine d within their corresponding quadrants. On the other hand, endodermal and m esodermal progeny dispersed throughout the body. The variability in the exa ct complements of adult structures, along with previously published cell de letion experiments, demonstrates that cell interactions are required for no rmal cell fate determination. Ctenophore embryos, like those of many bilate rian phyla (e.g., spiralians, nematodes, and echinoids), display a highly s tereotyped cleavage program in which some, but not all, blastomeres are det ermined at the time of their birth. The results suggest that mesodermal tis sues originally evolved from endoderm tissue. (C) 1999 Academic Press.