Plectus - a stepping stone in embryonic cell lineage evolution of nematodes

Abstract

BackgroundRecent studies have challenged the widespread view that the pattern of embryogenesis found in Caenorhabditis elegans (clade 9) is characteristic of nematodes in general. To understand this still largely unexplored landscape of developmental events, we set out to examine more distantly related nematodes in detail for temporospatial differences in pattern formation and cell specification. Members of the genus Plectus (clade 6) seem to be suitable candidates to show variety, with certain idiosyncratic features during early development and the convenient availability of cultivatable species.MethodsThe study was conducted using 4-D lineage analysis, 3-D modeling of developing embryos and laser-induced ablation of individual blastomeres.ResultsDetailed cell lineage studies of several Plectus species reveal that pattern formation and cell fate assignment differ markedly from C. elegans. Descendants of the first somatic founder cell S1 (AB) - but not the progeny of other founder cells - demonstrate extremely variable spatial arrangements illustrating that here distinct early cell-cell interactions between invariant partners, as found in C. elegans, cannot take place. Different from C. elegans, in Plectus alternative positional variations among early S1 blastomeres resulting in a ‘situs inversus’ pattern, nevertheless give rise to adults with normal left-right asymmetries. In addition, laser ablations of early blastomeres uncover inductions between variable cell partners.ConclusionsOur results suggest that embryonic cell specification in Plectus is not correlated with cell lineage but with position. With this peculiarity, Plectus appears to occupy an intermediate position between basal nematodes displaying a variable early development and the C. elegans-like invariant pattern. We suggest that indeterminate pattern formation associated with late, position-dependent fate assignment represents a plesiomorphic character among nematodes predominant in certain basal clades but lost in derived clades. Thus, the behavior of S1 cells in Plectus can be considered an evolutionary relict in a transition phase between two different developmental strategies.

From “the Worm” to “the Worms” and Back Again: The Evolutionary Developmental Biology of Nematodes

“…On the other hand, the more derived Chromadoria are characterized by a fast embryonic development with largely deterministic lineages ( Malakhov 1994 ; Schulze and Schierenberg 2011 ). Plectus species (Plectida) seem to have an intermediate way to specify cell types between Enoplia (no early founder cells) and Rhabditina (six founder cells established by the 16-cell stage): while the P lineage is clearly specified, the AB lineage is highly variable, leading to variable cell–cell contacts from one embryo to the other ( Schulze et al 2012 ). Within the Chromadoria, the early lineages of many species resemble C. elegans .…”

Laser‐mediated cell ablation during post‐implantation mouse development

“…Laser-mediated cell ablation has been used to study cell lineage, regeneration, and tissue-specific signaling of externally developing organisms such as C. elegans (Yanik et al, 2004;Fang-Yen et al, 2012;Schulze et al, 2012), zebrafish (Kohli and Elezzabi, 2008;Zhang et al, 2012), frogs (Mondia et al, 2011), and Drosophila (Kiehart et al, 2000;Supatto et al, 2005;Soustelle et al, 2008;Abreu-Blanco et al, 2011). An advantage of laser ablation is that it can be used with both temporal and spatial specificity and is hindered only by the target cells' accessibility.…”

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

“…Nevertheless, it should be noted that (again similar to Lophotrochozoa) Nematoda exist not developing with invariant handedness and where a chiral cellular arrangement does not seem to be the decisive L/R patterning step also exist [203,204]. It will be interesting to explore (a) whether intracellular chirality on the level of the actomyosin cytoskeleton is modified here; (b) whether intracellular chirality competes with other forms of intracellular chiral systems (e.g., microtubules); or (c) whether different mechanisms of amplification of cellular chirality exist that lead to different mechanisms for global L/R asymmetry.…”