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. 2012 Jul 2;3(1):13.
doi: 10.1186/2041-9139-3-13.

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

Jens Schulze  1 , Wouter Houthoofd, Jana Uenk, Sandra Vangestel, Einhard Schierenberg
Affiliations

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

Jens Schulze et al. Evodevo. .

Abstract

Background: Recent 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.

Methods: The study was conducted using 4-D lineage analysis, 3-D modeling of developing embryos and laser-induced ablation of individual blastomeres.

Results: Detailed 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.

Conclusions: Our 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.

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Figures

Figure 1
Figure 1
Embryogenesis in Plectus sambesii . (a) 1-cell stage (P0) with single pronucleus; (b) 2-cell stage with larger somatic founder cell S1 and smaller germline cell P1; (c) T-shaped 4-cell stage after transverse division of S1 and longitudinal division of P1; (c’) rarely S1 divides with longitudinal spindle orientation; (d) diamond-shaped 4-cell stage after rearrangement of blastomeres; (e) 8-cell stage, with gut precursor S2p (yellow) and germline cell P3 (red); (f) approximately 16-cell stage, S2p (yellow) has migrated to the center but keeps contact with the primordial germ cell P4 on the surface (red; mostly out of focus); (g) embryo with 4-cell gut primordium (yellow); (h-k) formation and closure of blastopore (blue) on the ventral surface of the developing embryo; (l) twofold stage (early morphogenesis) with future head region (hr) top and tail region (tr) bottom; (m) early cell lineage, divisions of germline (P1 to P4; changing position indicates ‘polarity reversal’ as described for C. elegans; Schierenberg, 1987) generate somatic founder cells (S1 to S4), the eight descendants of S1 are color coded; S2 divides into pharynx/muscle precursor S2a (orange) and gut precursor S2p (yellow). Arrowheads indicate asymmetric divisions. DIC optics. Orientation: anterior, left. Bar, 10 μm.
Figure 2
Figure 2
Formation of bilateral symmetry. Three-dimensional models of embryonic cell nuclei. In C. elegans, symmetry formation within individual lineages is not very apparent in early stages due to oblique division of somatic founder cells, but becomes successively more obvious even though not perfect. This is exemplified by the behavior of the S3 cells (green spheres; (a-l)). In contrast, P. sambesii performs strict left-right divisions of founder cells, generating in this way an essentially perfect bilaterally symmetric early embryo (m-x). Color code: S1 (AB), blue; S2a (MS), orange; S2p (E), yellow; S3 (C), green; S4 (D), purple, germline (P), red.
Figure 3
Figure 3
Cleavage behavior after cell elimination in P. sambesii . (a-c) After ablation of P1, the S1 descendants divide and form a blastocoel (marked with asterisk); (d, e) after ablation of P1, the S1 descendants can express normal synchronous cell cycles (d) or S1p descendants cleave asynchronously (e); (f-m) after early P2 ablation, S2 descendants lose their ability for asynchronous cell cycles (m) but after late ablation the normal cell cycle differences are expressed (l); (i-k) not after early (j) but after late extrusion of P2 (i), fluorescent marker dye accumulates in the gut primordium (k); (n-q) after early ablation of S3 (or P1/P2, see text), the typical retardation of cell cycles in three S1 descendants (see Figure 6) is lost (q). a-i, n-p: DIC optics; j, k, epifluorescence. Bar, 10 μm.
Figure 4
Figure 4
Variable arrangement of S1 descendants. Three-dimensional models of embryonic cell nuclei. With respect to the spatial arrangement of S1 blastomeres, four different cleavage types can be defined in the 8-cell stage (R, S1 blastomeres on the right side are positioned posterior to their left counterparts (a); L, S1 blastomeres on the left side are positioned posterior to their right counterparts (s); M1/M2, with respect to anterior/posterior S1 blastomeres on both sides occupy equivalent positions (g/m), but with respect to dorsal/ventral they occupy opposite positions (g*, m*). With the division of 16 S1 cells, cleavage types R and L each reproducibly split into two further spatial variants (d + d’; v + v’) due to shifts of left and right S1 descendants relative to each other. To better visualize that in the 64 S1 cell stage, specific positions on the left and right sides (e-w’) and at the anterior pole (f-x’) of the embryo are occupied by blastomeres from variable lineage origin, selected cells are marked with asterisks. Color code: members of the eight S1 descendants are marked as shown in Figure 1. Non-S1 cells are shown in light grey.
Figure 5
Figure 5
Cell contacts of S2a cells. Three-dimensional models of embryonic cell nuclei. In the 12-cell stage in C. elegans, S2a (MS) contacts and induces two of the four S1a descendants ((a); red arrows). In P. sambesii in the three different spatial variants, S2a (MS; orange) contacts all four S1a (ABa) descendants ((b-d); white arrows). In the 26-cell stage in C. elegans, MSap contacts and induces a single AB descendant ((e); red arrow). In P. sambesii either both ((f, g); white arrows) or none (h) of S1 (AB) sister cells contacts the corresponding S2a (MSa) cell. Black bars connect selected sister cells. For nomenclature of spatial variants, see Figure 4.
Figure 6
Figure 6
Different lineage, same fate. (a1-f2) Three-dimensional models of embryonic cell nuclei. In early Plectus embryos, five S1 descendants are contacted by S3 (white and blue arrows). Two of these are contacted in addition by P3 (red arrows). The three S1 blastomeres contacted exclusively by S3 (white arrows) generate descendants that occupy posterior dorsal and posterior lateral positions (b1, c1). These cells (light orange; remainder of S1, black) contribute to hypodermis (a2-c2) and later express retarded cell cycles (c3). In cleavage types M1L, R and L, different sets of three S1 cells are exclusively contacted by S3 (not shown). Nevertheless, they all occupy the same positions as those in type M2L (d1-f1), contribute to posterior hypodermis (d2-f2) and express retarded cell cycles (d3-f3). For nomenclature of spatial variants, see Figure 4.
Figure 7
Figure 7
Position of early S1 (AB) descendants and handedness of adults. (a-e) Three-dimensional models of embryonic cell nuclei. In C. elegans, the four descendants of S1 form an early left/right asymmetry, (d) resulting in a specific arrangement of gut and gonad ((f), ‘normal development’). Experimentally induced mirror-image arrangement of S1 descendants (e) results in a ‘situs inversus’ (g). In Plectus sambesii, positions of S1 cells differ considerably (a-c), but all variants develop into adults with normal handedness (f). For nomenclature of spatial variants, see Figure 4.
Figure 8
Figure 8
Phylogeny and development. Phylogenetic tree of nematodes ([19], modified [17]) comprising 12 clades. In the 23 studied members of clades 7 to 12, an invariant monomorphic development of S1 descendants was found, while all five representatives of clade 6 follow a variable polymorphic pattern. Based on these findings and additional data referenced in the text, a separation of ‘Chromadorea’ into ‘Rhabditia’ and ‘Chromadoria’ is supported.
Figure 9
Figure 9
Cleavage type and cell pattern. Three-dimensional models of embryonic cell nuclei. A very similar arrangement of 64 S1 descendants is found in three nematode species with different early cleavage patterns (T1, T2, I2; see [17]). A-C, ventral view; a-c, dorsal view. Orientation: anterior, left. For color code, see Figure 1.
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