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Somitogenesis in Amphibian Embryos

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Somitogenesis in Amphibian Embryos J.\Embryol. exp. Morph. Vol. 51, pp. 21-50, 1979 27 Printed in Great Britain @? Company of Biologists Limited 1979 Somitogenesis in amphibian embryos I. Experimental evidence for an interaction between two temporal factors in the specification of somite pattern By MURRAY PEARSON1 AND TOM ELSDALE2 From the MRC Unit of Clinical and Population Cytogenetics, Western General Hospital, Edinburgh SUMMARY Somitogenesis is described in two species of anuran amphibians, Xenopus laevis and Rana temporaria, in which the cellular mechanics of somite formation are distinctly different. Heat shocks are employed to demonstrate a wave of cellular change which precedes somite forma- tion down the body axis. This prior wave is shown to be kinematic. It is not a propagated wave. It is a consequence of the temporal activities of the cells laid out in space, but there is no evidence that these activities depend upon an interpretation of their position. Heat shocks cause characteristic segmental abnormalities over a zone of somites which is formed several hours after the shock. Evidence from double heat shock experiments suggests that the pattern of abnormality is the result of (i) a disturbance of co-ordination between pre-somitic cells, and (ii) the time available to those cells for recovery before they are recruited into a segmental pre-pattern at the time of passage of the prior wave. It is a temporal co- ordination that is disturbed and subsequently recovered following a heat shock. This temporal co-ordination of pre-somitic cells does not depend upon position along the axis. The evidence for two physiologically independent temporal patterns of cellular processes, which interact to specify the segmental pattern of somites (their size, shape and number), gives experimental support for the theoretical account of somitogenesis proposed by Cooke & Zeeman (1976). INTRODUCTION Segmentation is characteristic of the development of many animal forms and a basic principle of their morphogenesis. Somitogenesis in the vertebrate embryo is a striking example. The various aspects of somitogenesis in amphibians have been discussed by Deuchar & Burgess (1967) and Cooke & Zeeman (1976): the craniocaudal sequence; the constancy of the pattern within a species; the co- ordination with the whole body pattern; the precision and versatility of the control mechanisms that regulate the number and size of somites, not only under normal conditions, but also abnormal regimes of ploidy (Hamilton, 1969) and experimental manipulation (Cooke, 1975). In our approach to the problem of somitogenesis we deal first with temporal 1 Author's address: 30 Albion Hill, Brighton, Sussex, U.K. 2 Author's address: MRC Unit of Clinical and Population Cytogenetics, Western General Hospital, Crewe Road, Edinburgh, EH4 2XU, Scotland. 28 M. PEARSON AND T. ELSDALE aspects of the process because only by doing so shall we gain insight into the essential continuity of the whole process as well as the mechanism of dis- continuity between somites. Segmentation begins just behind the head and sweeps down the axis to the end of the tail; we refer to this as a wave of somite formation. (When we refer to a wavefront we mean the movement of the frontier, for instance in this case the frontier between segmented and not yet segmented tissue.) In temporal terms, the problem of the specification of segmental pattern is to understand how the period taken by the wave of somite formation to traverse the axis is specified, and how it is partitioned into just so many of the shorter intervals between the formation of one somite and the next. We have previously demonstrated (Elsdale, Pearson & Whitehead, 1976) how we can identify a crucial change in the properties of the pre-somitic tissue occurring some hours before participation in somite formation. The basic observation was that heat shocks given just before or during somitogenesis lead to abnormalities in the segmental pattern. Heat shock does not disturb already formed somites, and for a while afterwards new somites continue to form as if nothing had happened. After a standard number of normal somites have been made, however, abnormal somites begin to appear. Abnormal segmentation continues for a longer or shorter time depending on the severity and duration of the shock; eventually there is a return to normal segmentation. The anterior part of the abnormal zone is the most disturbed; and the last normal somite is immediately followed by maximally disturbed tissue to give a sharp anterior boundary. Across this boundary, tissue immune to heat shock lies immediately adjacent to tissue maximally disturbed. This means that tissue disturbable by heat shock earlier in its maturation suddenly becomes insensitive in the run up to somite formation. Abnormal zones commencing further and further caudally are produced by shocks to progressively older embryos, from which it follows that the frontier between immune and disturbable tissue moves as a wavefront down the axis ahead of visible segmentation. The wave of somite formation is preceded by a prior wave of change which confers immunity to heat shock. It is not clear, however, whether the normal segmental pattern is specified at this time of acquisition by cells of an immunity to heat shocks, or whether cells then merely become insensitive to any disruption of a segmental prepattern which has already been set. In this paper we present observations and experi- ments to show that the prior wave of cellular change is concomitant with seg- mental specification. Several observations support the inference that although heat shock is used to demonstrate the existence of the prior wave, this wave itself is not directly affected by heat shock. There is another component in the specification of segmental pattern. The demonstration of another component which is sensitive to heat shock comes from analysis of the abnormal zone following a single or two successive shocks, and leads to the conclusion that heat shock disturbs a co-ordination of the paraxial mesoderm cells established before the arrival of the wave. Somitogenesis in amphibian embryos. I 29 The results are interpreted according to a scheme for the specification of the somite pattern which involves the coupling of both components, a wave of cellular change by which cells are committed to subsequent somitogenesis, and a co-ordinated periodicity, in the establishment of a segmental prepattern: there is a wave of somite determination. Finally a model coupling suggested by Cooke & Zeeman (1976) is discussed. MATERIALS AND METHODS Rearing Xenopus embryos came from the Genetics Department, University of Edin- burgh, or from Dr C. Ford, School of Biological Sciences, University of Sussex, from spawnings induced by the injection of chorionic gonadotrophin. Embryos were reared in dechlorinated tapwater, sorted into batches of the same stage during blastula, and again at gastrula stages. Synchronous groups were reared at room temperature or controlled temperatures. Observations on somites were carried out after stripping the epidermis (Elsdale et al. 1976). Clutches of Rana embryos were collected from natural habitats in Perthshire. Synchronous batches were reared in pondwater. Heat shocks After removal of their outer jelly coats, embryos were pipetted into bottles containing 150 ml of water and standing in a 37 °C water bath. After the measured period, usually 15 min for Xenopus and 8 min for Rana, they were pipetted back into an excess of water at room temperature or some other controlled temperature. Microscopy Material fixed in Smith's or Bouin's fixative was dehydrated, embedded in paraffin wax and sectioned at 5-6 ^m. The sections were lightly stained with haemalum for histological examination. For scanning electron microscopy, specimens were prepared by the method described by Bard, Hay & Mellor (1975) and examined in a Cambridge Stereo- scan SI 80. Bisection o/Rana embryos Embryos were cut in two with tungsten needles in agar dishes containing a solution of 65 % Dulbecco's medium. After 1 h the fragments were cleaned of dead cells and the medium drawn off to be replaced by a 5 % Dulbecco solution. Anterior halves were stripped for scoring at a relatively early stage; the tail halves were cultured longer, until segmentation in controls was complete, and then fixed and stripped. 3 EMB 51 30 M. PEARSON AND T. ELSDALE RESULTS 1. Normal somitogenesis Somite formation in Xenopus is shown in Fig. 1. Paraxial mesoderm cells first elongate perpendicular to the notochord; then a bundle of the most anterior cells turns through 90° to give a somite, with myoblasts now lying parallel to the notochord. After several hours these myoblasts differentiate as uninucleate muscle fibres stretching from end to end of the somite. The process has been fully described by Hamilton (1969). In Rana the mechanics of somite formation are different. The somites form before cell elongation, and in a manner comparable to many other vertebrates where each somite forms initially as a rosette (Fig. 3). The adhesion between cells of a segmenting somite confers a roughly radial organization on the group, and de-adhesion from the non-segmenting cells posteriorly creates an inter- somitic fissure (Fig. 2). Later, myoblasts elongate within the somite and fuse to give multinucleate muscle fibres (Figs. 4 and 5). Counts for the total number of somites formed in Rana vary from 39 to 45, but it is unclear how great is the genuine variation between embryos because boundaries between the small, last formed somites are very difficult to see once myoblasts fuse, and yet before fusion one cannot be certain that the final somite has formed. In Xenopus some 46 somites form to the end of the tail proper; thereafter very small somites are added to the curious tail process which grows throughout larval life. FIGURES 1-5 Fig. 1. Somite formation at ca. 26-somite stage in Xenopus laevis. A horizontal section showing each segmental group of cells turning through 90°.
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