Segment Development in Platynereis dumerilii
In the errant nereid Platynereis dumerilii, the 4d cell divides bilaterally into a pair of M cells: Ml and Mr (Ackermann, Dorresteijn, and Fischer 2005; Fischer and Arendt 2013; Ozpolat et al. 2017). Each undergoes two highly asymmetrical divisions, giving rise to four cells (ml1, mr1, ml2, and mr2) that become the founders of the germline (Rebscher et al. 2007; Ozpolat et al. 2017). The next two also highly asymmetrical divisions yield four cells (ml3, mr3, ml4, and mr4) that undergo a limited number of symmetric divisions and then migrate toward the anterior end of the embryo, likely to form anterior non-segmental mesoderm (Ozpolat et al. 2017). Each of the following four divisions yields a pair of cells that further proliferate to form a segmental unit: the clones descended from ml5 and mr5 form “segment 0,” a cryptic segmental unit that bears no chaetae and is integrated into the head (Steinmetz et al. 2011), while the clones formed by ml6 and mr6, ml7 and mr7, and mls and mr8 respectively form larval segments 1 through 3 (Figure 4.6A-B). After that, 8M1 and 8Mr, sisters to ml8 and mr8, divide once more; then, while a daughter from each remains quiescent, the other undergoes two rounds of mitosis, yielding a total of five
FIGURE 4.5 Development of segmental mesoderm in Owenia sp. Left column shows diagrammatic sagittal sections (modified after Smart and Von Dassow, 2009); right column shows histological sagittal sections located approximately at the position indicated on the dashed boxes (modified after Wilson. 1932a). A: Mitraria larva, -2-3 days old; a mesoblast progenitor (M cell) is located at the internal angle between posterior ectoderm and posterior endoderm. B: Mitraria larva, -12 days old; two clusters of cells (tsl and ts2), presumptive progeny of the posterior mesoblast, can be seen. C: Mitraria larva, -17 days old; trunk mesoderm composed of 11 cell clusters (tsl, ts2, ts3, ts4, ..., tslO) showing an anteroposterior developmental gradient. A coelomic cavity has appeared in most clusters. The prospective trunk ectoderm adjacent to the anterior-most clusters begins to show indentations with segmental periodicity.
descendants for each of 8M1 and 8Mr (Figure 4.6B). Those ten cells form a ring and become the mesodermal precursors of the PGZ that will generate segments during post-larval life.
Cell tracing of the 4d lineage during early development of Platynereis shows that segmental larval mesoderm formation clearly fulfills the expectations of a lineage- driven mechanism (Figure 4.6C). Whether post-larval segment formation is also lineage-driven remains an open question: even though mesoteloblasts shrink in size
FIGURE 4.6 Origin of segmental mesoderm in Platynereis dumerilii. A: Simplified mid- trochophore larva, as seen in ventral view (anterior to the right). The eye symbol shows the point of view of В and С. B-C: Diagrammatic representation of cell progeny of the M meso- teloblasts in ~28 hours post-fertilization (hpf) (A) and ~37 hpf (B) mid-trochophore larvae. Each color represents descendants from the same blast cell (shown in D). D: Cell lineage tree of the progeny of the 4d cell. MPGZ, posterior growth zone mesodermal stem cells; ml" and mr' blast cell produced by the nth division of the left or right mesoteloblast; nMl and nMr: left or right mesoteloblast after the nth division; pPGCs, putative primordial germ cells. A modified after Fischer et al. (2010),• B-C modified after Ozpolat et al. (2017).
and split into several pairs as they become the founder mesodermal cells of the PGZ, whether they continue giving birth to single cells whose progeny is confined to a segment’s worth of tissue or else switch to a boundary-driven mechanism (like the one described for regeneration in Chapter 10) is not yet known. Interestingly, both the rate and the degree of asymmetry of mesoteloblast divisions is gradually reduced in the M to 8M lineage (Ozpolat et al. 2017): the first five rounds of mitosis happen with approximately 30 minutes intervals and then they slow down (40 minutes for 6M and 50 minutes for 7M). As 8M divides to generate the founder MPGZ cells, intervals become much longer (around 150 minutes). Cell asymmetry also changes; initial divisions are highly unequal (M being larger than m), but size difference between daughter cells decreases each round, until reaching equal size between 7M and 7m. The trend continues, so that the next division is again unequal, but this time 8M is smaller than its sister 8m.
As 4d lineage cells begin generating the mesodermal precursors of the larval segments, the 2d112 micromere, located mid-dorsally at the embryo’s hyposphere, divides bilaterally and proceeds to proliferate a pair of ectodermal sheets that converge toward the ventral midline (Ackermann, Dorresteijn, and Fischer 2005). However, whether larval segmental ectoderm formation follows a teloblastic behavior similar to that of 4d descendants, including foundation of the ectoteloblast ring at the PGZ, has not yet been determined conclusively (Gazave et al. 2013). Given our current knowledge, ectodermal segmentation could be either lineage-driven initially or boundary-driven throughout development.