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Somitomeres: Mesodermal Segments of Vertebrate Embryos

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Somitomeres: Mesodermal Segments of Vertebrate Embryos Development 104 Supplement, 209-220 (1988) 209 Printed in Great Britain @ The Company of Biologists Limited 1988 Somitomeres: mesodermal segments of vertebrate embryos ANTONE G. JACOBSON Department of Zoology, Center for Developmental Biology, (Jniversity of Texas, Austin, Texas 78712, USA Summary Well before the somites form, the paraxial mesoderm the early presence of these new morphological units, of vertebrate embryos is segmented into somitomeres. the somitomeres. When newly formed, somitomeres are patterned &r- Somitomeres were discovered in the head of the rays of mesenchymal cells, arranged into squat, bi- chick embryo (Meier , 1979), with the use of stereo laminar discs. The dorsal and ventral faces of these scanning electron microscopy. The old question of discs are composed of concentric rings of cells. Somito- whether the heads of the craniates are segmented is meres are formed along the length of the embryo now settled, ilt least for the paraxial mesoderm. during gastrulation, and in the segmental plate and Somitomeres have now been identified in the embryos tail bud at later stages. They form in strict cranial to of a chick, quail, mouse, snapping turtle, newt, caudal order. They appear in bilateral pairs, just anuran (Xenopus) and a teleost (the medaka). In all lateral to Hensen's node in the chick embryo. When forms studied, the first pair of somitomeres abut the the nervous system begins to form, the brain parts and prosencephalorr but caudal to that, for each tandem neuromeres are in a consistent relationship to the pair of somitomeres in the amniote and teleost, there is somitomeres. Somitomeres first appear in the head, but one somitomere in the amphibia. The mesodermal and the cranial somitomeres do not become somites, segments of the shark embryo are arranged like those but disperse to contribute to the head the same cell of the amphibia. types contributed by somites in the trunk region. In the trunk and tail, somitomeres gradually condense and epithelialize to become somites. Models of ver- Key words: somitomere: p&raxial mesoderm, chick, head, tebrate segmentation must now take into account quail, mouse, amphibia. lntroduction point that is often a cell. These faces are usually concave or convex with the central point of the It is now known that the paraxial mesoderm of somitomere at the deepest point of the concavity, or vertebrate embryos is segmented from the tip of the the highest point of the convexity. The cells compos- head to the tip of the tail. Ten years ago, in the course ing the dorsal aspect of the somitomeres, facing the of a study of the induction of the otic placode in chick ectoderffi, send up cell processes from the boundaries embryos, Stephen Meier removed the head ectoderm of the concentric rings of cells toward the ectoderm and examined the underlying paraxial head meso- (Fig. L). The three-dimensional affangement of the derm with stereo scanning electron microscopy, his cell processes helps emphasize the pattern, and somi- intent being to visu alize the material that he thought tomeres are most easily recognized in stereo. Often was inducing the otic placode. He serendipitously alignments of cells and cellular processes perpendicu- discovered that the paraxial head mesoderm beneath lar to the long axis and traversing the midline of the the prospective otic placode is organizedinto segmen- somitomere divide the somitomere into anterior and tal units, which he named 'somitomeres' (Meier, posterior compartments. The borders between suc- reTe). cessive somitomeres are especially apparent because These units are composed of loose mesenchymal the outermost concentric array of cells of each somi- cells organized into squat bilaminar discs. On the tomere curves away from that of its neighbour. dorsal and ventral faces of each somitomere, the cells Borders between somitomeres are also more appar- are arranged in concentric arrays around a central ent in stereo because they are ridges between success- 2r0 A. G. Jacobson Fig. 1. SEM dorsal view of a somitomere in the segmental plate of a quail embryo. This oblique view facing caudally accentuates the concentric affangement of cellular processes that are reaching toward the epidermis that has been removed. The centre of the somitomere is in the centre of the photograph. The neural tube runs down the right side. (From Jacobson & Meier,1986.) Bar, 50 pm. ive concavities or valleys between successive convexi- there is an early segmentation in the head mesoderm ties and, at the borders, cell processes are thrown up of a cramate, settlin g an old controversy. in ridges. The ventral face of the somitomere, which There is another part of the paraxta( mesode\s\sK apposes the endoderm, usually has a patch of more somewhat older embryos that is not obviously seg- densely packed cells at the centre of the somitomere, mented when viewed with light microscopy. This is and these cells contact the endoderm by means of a the segmental plate, a stretch of paraxial mesoderm tuft of cellular processes (Fig.2). The endoderm has reaching from the last-formed somite to the retreating a similar tuft of cellular processes that sticks out primitive streak in the bird embryo. The segmental towards the yolk. The pattern of cell affangement in plate cleaves somites from its rostral end and adds the endoderm beneath the somitomere mimics that in more paraxial mesoderm at its caudal end, either the somitomere and the tufts on the endoderm appear from the anterior end of the streak, or later from the to centre on the somitomere that lies, of that will lie, tail bud. The segmental plate is thus a constantly above it (Meier,1979). changing population of cells moving caudally in the The patterned cell affangement that constitutes a embryo. Packard & Jacobson (1976) have shown that somitomere is subtle. In some preparations, the the isolated segmental plate of the chick embryo will extracellular matrix obscures the pattern. Removal of form ten to twelve somites, and concluded that a much of this matrix by washing in buffer after covert segmentation must exist in the segmental dissecting away the ectoderm (ot endoderm) is an plate. Meier (1979) examined the segmental plate of important step in preparittg specimens to be exam- the chick with stereo SEM and found that it is ined for somitomeres by scanning electron mi- organized into ten to twelve somitomeres. Segmen- croscopy (SEM). Somitomeres are found in the same tation, therefore, is not occurring in the segmental places at the same stages in different embryos, and a plate, which is already segmented, but must occur somitomere visualized on one side of the axis has a before or during formation of the somitomeres. mirror-image mate on the other side. They are always Since somitomeres ate circular, they do not occupy found in consistent relationships to the parts of the all the space in the band of paraxial mesoderm. Some brain and cranial neural crest migrates on the cranial cells that may not be part of the somitomeres are left somitomeres in a characteristic pattern (Jacobson, in the crotches at the lateral and medial borders LeBT). between adjacent tandem circular somitomeres. Somitomeres were discovered in the head paraxial Meier (personal communication) thought that these mesoderm and their discovery makes it clear that cells probably contribute to vascular tissue. Vascular Somitomeres 21I Fig. 2. SEM ventral view of the most recently formed somitomere of a stage-5 chick embryo. A central tuft of cell processes marks the centre of the circular somitomere. The top of the figure is caudal. The fragment of endoderm in the upper right has on its ventral surface (toward the viewer) a tuft of cell processes that predicts the centre of the next somitomere that will form. (From Meier, 1979.) Bar, 50 pm. elements appear early, especially on the ventral mediate mesoderm can be viewed dorsally with SEM surface of the mesoderm, and these cells are active in (before the lateral plate folds over the intermediate migration. Meier (1980) showed an anastomosing mesoderm and abuts the somites) there are many vascular network covers the ventral surface of the cells that lie on the intermediate mesoderm perpen- mesoderm, but appears to have a border that co- dicular to the long axis and the somite border. These incides with the lateral border of the somitomeres at cells were shown to be vascular by their binding with a stage 10. Flowever, England (1986) has shown by quail vascular endothelial marker, QH1 (Solursh et SEM of dissected chick embryos and ink injections al. 1987). Jacob et al. (1978) implanted quail somites into the vascular system that vascular openings from into chick embryos, then found quail cells migrating the aorta penetrate intersegmentally between somito- across the intermediate mesoderm and suggested that meres. Early vascular elements from the paraxial such cells were migrating myogenic cells, but prob- mesoderm, already in position, may contribute to ably they were vascular elements and the myogenic these intersegmental vessels. cells migrate later and may follow the pathways of the It has also been suggested that prospective vascular vascular tissue. Meier (1980) pointed out that the elements migrate from the paraxial mesoderm into lateral plate mesoderm has grooves perpendicular to the lateral plate region. At stages when the inter- the long axis and coincident with intersomitomeric 2I2 A. G, Jacobson boundaries. Meier & Burton (1986) suggest that by Hamburger & Hamilton, 1951), while the primi- migrating vascular elements exploit these grooves tive streak is still elongating, the first pair of somito- and form vascular pathways that later migrating meres is formed to each side of the anterior tip of the myoblasts follow from the somites as they move to primitive streak, and the prechordal plate, which the wing bud. resembles a somewhat condensed somitomere, is formed in the midline anterior to the streak and When do somitomeres form? between the two somitomeres (Fig.
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