Mesoteloblast‐Like Mesodermal Stem Cells in the Polychaete Annelid Platynereis dumerilii (Nereididae)

Abstract

Spiral cleavage is observed in animals that belong to the lophotrochozoa, a large group of marine invertebrates. As characteristic for spiral cleavage, the bulk of mesoderm forms from one cell, the "4d blastomere." This process has not yet been followed in cellular detail in annelids except in the leech, where "mesoteloblasts," a pair of mesodermal stem cells, generate two bands of mesoderm precursor cells in an iterative fashion. It is so far unknown whether such stem cell-like lineage is a general property of 4d-derived mesoderm in spiralian larvae. To address this, we have analyzed the cell lineage of the 4d blastomere in the polychaete annelid Platynereis dumerilii, an emerging model for lophotrochozoan and spiralian embryology (Fischer et al., 2010), by 4D microscopy, a semi-automated cell tracking technique based on differential interference contrast serial imaging (Schnabel et al. '97). Our data reveal that the two daughter cells of the 4d cell undergo seven consecutive rounds of unequal cell divisions. They bud off smaller cells in ventral-vegetal orientation and thus show mesoteloblast- and stem cell-like behavior. Based on these findings, we suggest that mesoteloblast-like mesodermal stem cells that form continuous mesodermal bands are part of the Errantia + Sedentaria ground pattern. In the course of annelid evolution, the number consecutive divisions of these cells would have been low initially with <10 division cycles, giving rise to larval segments only, and then increased up to 35 as observed in clitellates.

Spiralian model systems

“…Additional work was carried out by their counterparts in Europe (e.g., Heymons, 1893;Wierzejski, 1905). That early work has been extended in recent decades using modern cell-autonomous lineage tracers for a number of species (i.e., the gastropod molluscs Crepidula fornicata and C. convexa, Hejnol et al, 2007;Lyons et al, 2012, and Ilyanassa obsoleta, Render 1991, 1997Chan and Lambert 2014; the polyplacophoran mollusc, Chaetopleura apiculata, Henry et al, 2004; the nemerteans, Cerebratulus lacteus, Carinoma tremaphoros, Maslakova et al, 2004a,b; the polyclad turbellarian Hoploplana inquilina, Boyer et al, 1996Boyer et al, , 1998; and the annelids Capitella teleta, , Meyer and Seaver, 2009, 2010, and Platynereis dumerilii, Ackerman et al, 2005Fischer and Arendt, 2013). Together, this body of work has revealed that the ultimate fates of these quadrants are, to a large extent, homologous across the embryos of different spiralian phyla.…”

Segment formation in Annelids: patterns, processes and evolution

“…These cells express the gene vasa (Rebscher et al, 2007) and comprise the primordial germ cells of the worm as well as the precursors of the mesodermal teloblasts. Fischer and Arendt (2013) have determined that the embryonic precursors to the mesodermal teloblasts undergo a series of stereotyped asymmetric cell divisions to produce first the primordial germ cells and subsequently the precursor cells of the mesoderm of the 3-segment larva in the same way as the leech M teloblasts. The injection of the 2d lineage, homologous to the DNOPQ lineage of the leech has not been carried out to date in Platynereis.…”

Cell Proliferation Pattern and Twist Expression in an Aplacophoran Mollusk Argue Against Segmented Ancestry of Mollusca

“…Yet, in mollusks, the mesodermal bands have generally been described as mostly less extensive and rather short lived, especially when compared to the situation in annelids (Korschelt and Heider, 1936; Raven, 1966; Fioroni, 1971, 1992; Wanninger and Wollesen, 2015). In the worm‐shaped solenogasters, however, the mesodermal bands seem to acquire larger dimensions and persist for a considerable period of time–a condition, which is more similar to other spiralians, especially annelids (e.g., Mead, 1897; Schmidt, 1925; Okada, 1940; Anderson, 1959, 1966, 1973; Goto et al., ’99; Ackermann et al., 2005; Seaver et al., 2005; Dill et al., 2007; Woodruff et al., 2007; Fischer and Arendt, 2013). Furthermore, the situation we observed is in agreement with classical descriptions on mesoderm formation and differentiation of solenogasters and polyplacophorans (Pruvot, 1890, 1892; Heath, 1899; Naef, 1924; Hammarsten and Runnström, 1925; Baba, 1938; Thompson, 1960; Salvini‐Plawen and Bartolomaeus, 1995) but is demonstrated here for the first time over the entire course of development using state‐of‐the‐art techniques.…”