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Local Autonomy of Gastrulation Movements After Dorsal Lip Removal in Two Anuran Amphibians

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Local Autonomy of Gastrulation Movements After Dorsal Lip Removal in Two Anuran Amphibians J. Embryol. exp. Morph. Vol. 33, 1, pp. 147-157, 1975 147 Printed in Great Britain Local autonomy of gastrulation movements after dorsal lip removal in two anuran amphibians By JONATHAN COOKE1 From Division of Development Biology, National Institute for Medical Research, Mill Hill SUMMARY The time-course of the remaining gastrulation movements has been investigated after removal of the dorsal lip, the presumptive foregut endoderm and the anterior mid-dorsal mesoderm as a plug-shaped mass of cells from beginning gastrulae of Xenopus laevis and Bombina orientalis. This embryonic region has been previously studied in its role as an organizer, when grafted into a host gastrula marginal zone. There is usually no effect of the removal of these cells, the first morphogenetically active ones, either upon rate of subsequent completion of the external aspects of gastrulation, or upon the internal evolution of the presumptive mesodermal mantle. This finding is discussed in connexion with results of a previous paper on pattern formation in early Xenopus develop- ment, since it may help to distinguish between possible types of explanation for those results. INTRODUCTION A previous paper (Cooke, 1973 a) reported certain features of the results of implanting second organizer regions into the marginal zone of Xenopus blastulae and early gastrulae. The present paper begins to explore in greater detail the anatomy of gastrulation and the causal relationships between movements in parts of the embryo around the time of these organizer implantations. It reports the results of removing a mass of cells, consisting of the surroundings of the earliest visible organizer activity, together with the underlying bottle cells (Holtfreter, 1943), endoderm cells and presumptive anterior mid-dorsal meso- derm, from early stage-10 Xenopus (Nieuwkoop & Faber, 1956) and the equivalent stage in Bombina. This excision operation, the same as that reported previously, has been followed by detailed observation of the completion of gastru- lation in comparison with individually paired, precisely synchronous controls. The rationale for including Bombina in the study was that due to the slower time-course of its gastrulation, a greater chance was offered for observation of possible retarding effects of the operation, since these might take some time to set in if they were of a physiological rather than a mechanical nature. 1 Author's address: Division of Developmental Biology, National Institute for Medical Research, The Ridgeway, Mill Hill, London, NW7 1AA, U.K. 148 J. COOKE Gastrulation involves the formation of bottle cells, and neuroectodermal spreading at the surface of the marginal zone, and the inrolling and animalward migration of presumptive mesoderm cells internally (Nieuwkoop & Florschutz, 1950; Lovtrup, 1965). These activities spread with time along an axis, the dorso- ventral, that corresponds with one of those for future pattern formation. Furthermore, when sites of the initially localized mid-dorsal activity are grafted to ventral regions of the margin, they can cause a similar spread of gastrulation movements in the surrounding cells as well as a new field of axial pattern formation subsequently (Cooke, 1972). It is thus likely that the time-course of gastrulation is originally co-ordinated and controlled by a gradient system identical with, or related to, that controlling the extent and proportions of the final pattern of cellular differentiation in the mesoderm. At some unknown early stage, this gradient system would then set, locally, the rate at which the physiology of cells evolved towards the initiation of those mechanical behaviours listed above as causing gastrulation. The question remains, however, as to how immediately cells can affect their neighbours during the actual progress of gastrulation. Are their interactions, along the dorso-ventral axis, at least partially of a mechanical and orientating or stretching nature, or are they solely physiological, reflecting the stability of a gradient system set up by earlier intercellular communication? If the latter, how stable is this gradient system? If a retarding effect were observed at any subsequent time during gastrulation, on removing the first mechanically active cells from the dorsal midline, it might have a mechanical explanation, showing that the process is controlled or 'led' mechanically from the dorsal lip area. Absence of such an effect would mean that control over the orderly dorso- ventral sequence of gastrulation is in fact of a 'physiological' character, and furthermore that by this time either the gradient or the cells' programmed response to it is sufficiently stable to avoid any effect of apex removal upon the schedule of morphogenetic movements. In fact, it is shown that there are normally no interactional effects of removing these first active cells, upon the subsequent cellular activities that complete the gastrulation process throughout the rest of the embryo. The consequences of this finding are discussed, for the interpretation of effects observed in the final patterns of cellular differentiation, when organizer implantation is combined in various ways with host organizer removal as described previously (Cooke, 1973 a). MATERIALS AND METHODS Eggs were obtained from matings induced by subcutaneous injection of human chorionic gonadotropin ('Pregnyl', Organon Laboratories Ltd) for both Xenopus and Bombina. 250 i.u. per female and per male was satisfactory for the latter species. Groups of embryos were dejellied and demembranated manually at the late blastula stage (Nieuwkoop & Faber stage 8 in Xenopus) and stored Autonomy of gastrulation after dorsal lip removal 149 Dorsal ca. 1 mm (C) Surface zone of marginal activity Internal Line of progress D.L. of internal / > mesodcrmal mantle Archenteron Fig. 1. The excision operation. A, Vegetal surface view of stage-10 gastrula. B, Sagittal section. Heavy dashed boundaries indicate region removed, shown as an isolate in centre. C, Vegetal surface view of the healed embryo some 2h later (Xenopus) on completion of ventral blastoporal lips. D, Combined lateral surface view and sagittal section of same stage as C. vegetal surface uppermost in black wax-bottomed dishes under two-thirds- strength Niu-Twitty solution (see Rugh, 1962) whose Ca2+ and Mg2+ concentra- tion had been doubled by means of the chlorides, and the pH brought to 7-0 by HC1. This solution frequently provides perfect healing and morphogenesis after operations in the present material. By inspection at 15 min intervals, pairs of embryos were selected whose activity of the bottle-shaped cells (surface pigment gathering and dimpling) at the incipient dorsal lip had started syn- chronously within this margin of error. They were placed side by side, and the organizer region cleanly removed with tungsten needles from one of them. To control for a possible physiological effect of laying open the blastocoel to the culture fluid, a small tear was also made in the animal region to open the blastocoel in each embryo. Between \ h and 45 min after this operation, the strength of the solution was lowered to 0-1 with glass-distilled water to avoid the exogastrulation which often occurs without this. Observation, with camera 150 J. COOKE Table 1. Time-course of completion of gastrulation movements after organizer excisions in Xenopus Time to completion of marginal zone Yolk plug closure Experiment Pair no. activity, i.e. lips of blastopore to stage 12\ 1 0* -1 + 1 + 1 + 1 0 0 + 1 -1 -2 -1 -2 -1 0 + 1 + 1 0 + 2 + 1 + 1 3 -2 -1 (low -1 -2 temperature) + 2 + 2 0 + 2 0 -2 -1 0 * 0, 1 or 2 indicates synchrony, delay ( + ) or advance (-) of the time of completion of the stated phase of gastrulation in the experimental as compared with its initially synchronous control, the unit inter-observational period being 20 min. lucida drawing, was made at 10-20 min intervals thereafter for each synchronous pair. Between observations, pairs of embryos were lying on the laboratory bench, away from intense lighting and at an even temperature of between 21 and 23-5 °C (as between different experiments). On one occasion, Xenopus embryos were kept between observations in a cooled incubator between 16-5 and 17-5 °C. The group of cells removed was that described in previous papers (Cooke, 1972, 1973 a), laying open the blastocoel and leaving initially an embryo in which none of the marginal cells were visibly different from those of stage-9 blastulae. The operation is shown in Fig. 1. The wound, which was cleared of cell debris by gentle aspiration with a micropipette before the first observation, had usually closed off the blastocoel within 30 min in Xenopus and 1 h in Bombina, at which times the first new gastrulation activity was beginning. The excised plugs of cells were used as implants into other embryos, where in Xenopus they often caused complete secondary axes as described previously. Selected embryos were fixed for 10 min in 4 % formalin in two-thirds-strength Niu-Twitty, halfway through gastrulation, before examination of the internal course of mesoderm morphogenesis by bisecting in the frontal plane and then chipping away the endodermal blastocoel floor. Autonomy of gastrulation after dorsal lip removal 151 Table 2. Time-course of completion of gastrulation movements after organizer excisions in Bombina Time to completion of marginal zone Yolk plug closure Experiment Pair no. activity, i.e. lips of blastopore to stage 12$ 11 0* +1 2 0 0 3 -1 0 4 -1 0 5 +1 +1 2 1 +1 +2 2 0 +1 3+1 0 4 -1 -1 5 -1 -2 3 1 +1 +1 2 0 +1 3 +2(35min) +2 4 +2(35min) +2 5 +2(25min) +2 * 0, 1 or 2 indicates synchrony, delay ( + ) or advance ( —) of the time of completion of the stated phase of gastrulation in the experimental as compared with its initially synchronous control, the unit inter-observational period being 20 min. RESULTS Twelve pairs of Xenopus embryos, from three different egg-batches in separate experiments, were observed at laboratory temperature (21-23 °C), and four more pairs in another experiment at 16-17 °C.
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