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Formation of the egg-laying system in Pristionchus pacificus requires complex interactions between gonadal, mesodermal and epidermal tissues and does not rely on single cell inductions

Benno Jungblut^*, André Pires-daSilva and Ralf J. Sommer

Max-Planck Institut für Entwicklungsbiologie, Abteilung Evolutionsbiologie, Spemannstrasse 37-39, D-72076 Tübingen, Germany
^* Present address: Department of Biochemistry and Biophysics, UC San Francisco, San Francisco, CA 94143, USA

View larger version (29K): [in a new window]   Fig. 1. Evolutionary variations in vulval cell fate specification between C. elegans and P. pacificus (A) and a schematic summary of the multiple guidance mechanisms for sex myoblast migration in C. elegans (B). (A) During the L1 stage in C. elegans, the 12 ventral epidermal cells P(1-12).p are equally distributed between pharynx and rectum. P(1,2,9-11).p fuse with the hypodermal syncytium hyp7 (F, white ovals). P(3-8).p form the vulva equivalence group and adopt one of three alternative cell fates. P6.p has a 1° fate (blue oval), and P(5,7).p have a 2° fate (red ovals). P(3,4,8).p have a 3° fate and remain epidermal (yellow ovals). The anchor cell (AC, green circle) provides an inductive signal for vulva formation. In P. pacificus, P(1-4,9-11).p die by programmed cell death. P6.p and P(5,7).p have a 1° and 2° fate, respectively. P8.p has a 4° fate (black oval) and remains epidermal. Vulva induction is provided by several cells of the somatic gonad (green ellipse). (B) The SM cells are born midway between gonad and rectum and migrate anteriorly. A gonad-independent mechanism (blue arrow) guides the SMs to an anterior position. Precise positioning around the center of the gonad and vulva requires a gonadal attraction that involves an FGF-like molecule encoded by the egl-17 gene. egl-17 is expressed in several cells of the somatic gonad, the dorsal uterine precursors (DU), the ventral uterine precursors (VU) and the AC, but also in P6.p. A third signal influencing SM position is a gonad-dependent repulsion (pink bar). Repulsion has been identified in egl-17 mutants, in which the SM cells stay in the posterior region rather than migrating to the central body region by the gonad-independent mechanism. The precise role of gonad repulsion is unknown.

View larger version (27K): [in a new window]   Fig. 2. M lineage analysis in P. pacificus hermaphrodites. Divisions are anterior-posterior unless otherwise indicated. bm, body muscles; cc, coelomocytes; d, dorsal; v, ventral; l, left; r, right; a, anterior; p, posterior. See text for details.

View larger version (7K): [in a new window]   Fig. 3. Effects of gonad ablations on SM positioning in P. pacificus wild-type hermaphrodites. Z(1,4) were ablated at hatching. Each arrow represents the position of a single SM. SM position was scored with respect to the position of the remnants of the gonad and the position of P8.p. The position of P(5-7).p cannot be taken as a representative landmark, as these cells migrate slightly towards the posterior after gonad ablation.

View larger version (132K): [in a new window]   Fig. 4. Nomarski photomicrographs of various stages of the M lineage and rhodamine dextran injected P. pacificus wild-type and Ppa-mab-5 mutant animals. (A) Wild-type animal, 11 hours after hatching showing two of the four intermediate muscle precursors in the muscle quadrants. In this plane of focus, the ventral (M.vl) and dorsal (M.dl) cell in the left focal plane are visible. (B) Ppa-mab-5 mutant animals, 11 hours after hatching, showing all four progeny of M in the ventral region on the right side of the animal after both divisions occurred longitudinally. (C) Wild-type animal 19 hours after hatching showing the four and five progeny of M.dl and M.vl, respectively. Note that similar muscle lineages exist on the right side of the animal. The SM cell (SM) is already morphologically distinct from its sisters. (D) Ppa-mab-5 mutant animals 19 hours after hatching, showing a group of disorganized descendants of M. In this plane of focus, seven cells are visible (arrows) none of which has specific characters of SM-like or coelomocyte-like cells. (E) Wild-type animal 30 hours after hatching showing the AC and the progeny of P(5-7).p after two rounds of cell division. (F) The same animal in a left focal plane showing the undivided SM cell in the region of the vulva. (G) Rhodamine dextran injected wild-type animal with six coelomocytes. (H) Rhodamine dextran injected Ppa-mab-5 mutant animals, where the postembryonic coelomocytes are absent.

View larger version (23K): [in a new window]   Fig. 5. Model of the cell-cell interactions between the mesodermal and the epidermal parts of the egg-laying system in P. pacificus wild-type (A) and Ppa-mab-5 mutant (B,C) animals. (A) In wild-type animals, several cells of the somatic gonad induce P(5-7).p to form vulval tissue in a continuous interaction. P8.p and the descendants of M, here indicated at the level of the intermediate precursors Md/v,l/r, influence the cell fate decision of P(5,7).p upon gonadal signaling (lateral inhibition). Negative signaling by P8.p prevents the gonad-independent differentiation of P(5-7).p. (B) Cell-cell interaction during early development in Ppa-mab-5 mutants. Early in larval development, the M cell itself inhibits the ectopic differentiation of P8.p. The inductive source for this differentiation remains unknown and might even be P8.p itself. (C) Cell-cell interactions during late development in Ppa-mab-5 mutants. The gonad induces vulva formation, as in wild-type animals. The descendants of M induce the ectopic differentiation of P8.p. This interaction is most likely neomorphic.