Sandra Vangestel

Embryonic cell lineage of the marine nematode Pellioditis marina.

We describe the complete embryonic cell lineage of the marine nematode Pellioditis marina (Rhabditidae) up to somatic muscle contraction, resulting in the formation of 638 cells, of which 67 undergo programmed cell death. In comparison with Caenorhabditis elegans, the overall lineage homology is 95.5%; fate homology, however, is only 76.4%. The majority of the differences in fate homology concern nervous, epidermal, and pharyngeal tissues. Gut and, remarkably, somatic muscle is highly conserved in number and position. Partial lineage data from the slower developing Halicephalobus sp. (Panagrolaimidae) reveal a lineage largely, but not exclusively, built up of monoclonal sublineage blocs with identical fates, unlike the polyclonal fate distribution in C. elegans and P. marina. The fate distribution pattern in a cell lineage could be a compromise between minimizing the number of specification events by monoclonal specification and minimizing the need for migrations by forming the cells close at their final position. The latter could contribute to a faster embryonic development. These results reveal that there is more than one way to build a nematode.

Different roads to form the same gut in nematodes

SUMMARY The morphogenesis of a gut from the endoderm has been well studied among the animal kingdom and is also well described in the nematode Caenorhabditis elegans. But are there other ways to build a nematode intestine? Sulston et al. (1983) described a different intestinal cell lineage in the species Panagrellus redivivus and Turbatrix aceti that includes two programmed cell deaths. However, no details are known about the three‐dimensional (3D) configuration and the role of the cell deaths. Here, we describe the intestinal morphogenesis of P. redivivus and five other nematode species by means of four‐dimensional microscopy, which gives us a 3D representation of gut formation at the cellular level. The morphological pathway of gut formation is highly conserved among these distantly related species. However, we found the P. redivivus pattern in another related species Halicephalobus gingivalis. In this pattern, the intestinal precursors migrate inward in concert with the mesoderm precursors. Based on the observations, we propose a hypothesis that could explain the differences. The positions of the mesoderm precursors create a possible spatial constraint, by which the establishment of bilateral symmetry in the intestine is delayed. This symmetry is corrected by cell migrations; other cells are eliminated and compensated by supplementary cell divisions. This pattern leads to the same result as in the other nematodes: a bilateral symmetrical intestine with nine rings. This illustrates how conserved body plans can be achieved by different developmental mechanisms.

The early embryonic development of the satellite organism Pristionchus pacificus: differences and similarities with Caenorhabditis elegans

As a comparative counterpart for the model organism Caenorhabditis elegans , the nematode Pristionchus pacificus was established as a satellite organism to study developmental processes. However, these studies mainly focused on post-embryonic development and little is known about the early embryonic development. Using 4D microscopy we reconstructed the early embryonic cell lineage of 12 individuals of P. pacificus . By analysing several parameters of early development, including the division sequence, the spatial arrangement of blastomeres, the cell cycle patterns of the AB lineage and cell-cell contacts in different cell stages of the embryo, it was shown that the early embryonic development is nearly identical to C. elegans . Known cell-cell contacts necessary for induction of blastomere fates in C. elegans are also present in P. pacificus . Thus, the spatio-temporal conditions that would allow possible homologous inductions are present. However, at least one model for blastomere specification seems not to apply to P. pacificus since the third division in the AB lineage differs from that of C. elegans . Furthermore, naturally occurring variability of early development was demonstrated, which is clearly permitted since there seems to be no influence on further development into an adult worm.

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

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.

Early development of the root-knot nematode Meloidogyne incognita.

Detailed descriptions of the early development of parasitic nematodes are seldom available. The embryonic development of the plant-parasitic nematode Meloidogyne incognita was studied, focusing on the early events. A fixed pattern of repeated cell cleavages was observed, resulting in the appearance of the six founder cells 3 days after the first cell division. Gastrulation, characterized by the translocation of cells from the ventral side to the center of the embryo, was seen 1 day later. Approximately 10 days after the first cell division a rapidly elongating two-fold stage was reached. The fully developed second stage juvenile hatched approximately 21 days after the first cell division. When compared to the development of the free-living nematode Caenorhabditis elegans, the development of M. incognita occurs approximately 35 times more slowly. Furthermore, M. incognita differs from C. elegans in the order of cell divisions, and the early cleavage patterns of the germ line cells. However, cytoplasmic ruffling and nuclear migration prior to the first cell division as well as the localization of microtubules are similar between C. elegans and M. incognita.

The somatic female gonad of Cephalobidae (Nematoda): cellular architecture and associated function

The female reproductive system of the free-living nematode family Cephalobidae is examined by means of differential interference contrast, scanning electron and fluorescent microscopy. The model nematode Caenorhabditis elegans and the predatory nematode Prionchulus punctatus are also included in this study; the former mainly to test our results with the very detailed knowledge of this model organism, the latter to provide a representative of the more distantly related Enoplea. In this comparative approach, the analysed gonad structures are discussed with respect to their functional and phylogenetic significance. The general cellular composition of the cephalobid gonad – namely an oviduct comprising two rows of four cells, a distinctly offset spermatheca consisting of 8-16 cells, and a uterus composed of distinct cell rows – differs from all known Nematoda except that of the plant-parasitic Tylenchomorpha. Despite the striking evolutionary conservation of the cellular architecture of the cephalobid gonad there is a complex subcellular specialisation, namely a significant and functionally relevant variation in myofilament organisation, both among Cephalobidae and between major groups of nematodes. We demonstrate the presence of microfilaments that vary in pattern among species and that may play an important role in egg propulsion. The phenomenon of endotokia matricida, in which eggs do not leave the female body, is found to be associated with a massive rupture of the cytoskeleton in the uterus wall. The complexity of the myofibril structure and the associated potential to propagate oocytes actively cannot be solely explained by differences in phylogenetic history, but is also linked to body diameter. In the larger Acrobeloides maximus, the proximal end of the ovary sheath is adorned with 12 distinct longitudinal bands, antibody binding positively for paramyosin, while in the smaller Cephalobus cubaensis myofilament organisation is at random.