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J Morphol
2024 Feb 01;2852:e21664. doi: 10.1002/jmor.21664.
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Epichordal vertebral column formation in Xenopus laevis.
Takahashi Y
,
Wakabayashi R
,
Kitajima S
,
Uchiyama H
.
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Although Xenopus Laevis is the most widely used model amphibian, skeletal development of its vertebral column has not been well illustrated so far. The mode of vertebral column development in anurans has been classified into two modes: perichordal and epichordal. Xenopus vertebral column formation is believed to follow the epichordal mode, but this aspect has been underemphasized, and illustrative examples are currently unavailable to the scientific community. This study documents the entire process of vertebral column formation in X. laevis, from the initial neural arch formation to the completion of metamorphosis. These images reveal that the neural arch arises from the dorsal lamina and lateral pedicle primordia, with no strict adherence to an anteroposterior sequence. Unlike other species, Xenopus centrumprimordia exclusively form at the expanded ventral margins of neural arches, rather than from the cartilaginous layer surrounding the notochord. These paired centrumprimordia then fuse at the ventral midline, dorsal to the notochord, and subsequently the notochord degenerates. This mode of centrum formation differs from the traditional epichordal mode, indicating that Xenopus might have lost the ability to form a cartilaginous layer around the notochord. Instead, the neural arch's ventral margin appears to have evolved to incorporate centrum precursor cells at its base, thereby forming a centrum-like structure compensating for the absence of a true centrum. It is widely accepted that postsacral vertebrae lack centra, only possessing neural arches, and eventually fuse with the hypochord to form the urostyle. However, we have shown that the paired ventral ends of the postsacral vertebrae also fuse at the midline to form a centrum-like structure. This process might extend to the trunk region during centrum formation. In addition to these findings, we offer evolutionary insights into the reasons why Xenopus retains centrumprimordia at the base of neural arches.
Figure 1
Xenopus laevis, initial phase of neural arch formation. Three representative larvae (Stage [St.] 48a, 48b, and 48c) are shown in lateral (a, c, e) and dorsal (b, d, f) views. Arrows indicate the triangular primordia of the lamina, and arrowheads mark the small circular spot-like primordia of the pedicle. The lateral spots at the third, fourth, and fifth positions elongate dorsally and fuse with the dorsal triangles to form the shape of neural arches (e). Asterisks in c and d show the fifth primordia at an asymmetric position. Sp, spinal cord; nt, notochord. The scale bar is common among a–f.
Figure 2
Xenopus laevis, formation of cartilaginous neural arches in the trunk region. (a) One larva at Stage (St.) 50 with the third, fourth, and fifth neural arches formed. (b) Another St. 50 larva with the second to sixth arches. The first pedicle is not yet formed. (c, d, e) St. 51 larvae with the ninth, 10th, and 11th arches being formed, respectively. When posterior arches are formed, the first arch is formed at the anterior margin of the triangle (d, e). Arrowheads indicate anterior inclination of the first arch. Sp, spinal cord; nt, notochord. Scale bar in a is common to a and b. Scale bar in c is common among c–e.
Figure 3
Xenopus laevis, ossification of neural arches and appearance of epichordal centra. (a) The larva with four ossified arches and one pair of centra. (b) Seven ossified arches and four pairs of centra. (c) Nine ossified arches and five pairs of centra. (d) Ten ossified arches and eight pairs of centra. Some of the paired centra are fused at the midline (refer to Figure 5). Black arrowheads indicate positions of initial ossification. poz, postzygapophysis; prz, prezygapophysis. White arrowheads indicate cartilage formation in the lateral portion of perichordal tube. Arrows indicate ventralcartilage layer.
Figure 4
Xenopus laevis, centrum of the first vertebra (atlas) separated from the occipital region. Occipital regions in the ventral view of (a) Stage (St.) 49, (b, c) St. 50, (d, e) St. 51, and (f) St. 52 larvae. Note the separation from the occipital region and connection with the neural arch of the centrumprimordium. Arrows indicate notches and 1–3 represent vertebral positions. ac, acoustic capsule; ex, cartilaginous primordium of exoccipital. Scale bar in a is common among a, d, and e. Scale bar in b is common among b, c, and f.
Figure 5
Xenopus laevis, formation and midline fusion of centrumprimordia in the ventral view. Note that these centra are formed only dorsal to the notochord and photographed through the transparent notochord. (a–d) Larvae with one, two, three, and four pairs of centra, respectively. (e, f) Larvae with five pairs of distinct centra. Small ossification centers are already formed at the sixth and seventh positions in e. (g) Larva with seven pairs of centra. (h) Larva with nine pairs of centra, which are mostly fused. Midline fusion starts from the third, fourth, and fifth centra. Scale bar in a is common among a–c. Scale bar in d is common among d–h. Black arrowheads, anteroposteriorly short centrum; white arrowheads, porous centrum.
Figure 6
Xenopus laevis, completion of centrum formation in the trunk during metamorphosis. Timing of midline fusion of the first (atlas) and ninth (sacral) centrum varies among individuals (a, b). At Stage (St.) 65, the intervertebral cartilage appears at the fifth, sixth, seventh, and eighth centra (d). At St. 66 (froglet), the intervertebral cartilage is more developed and visible at the third to ninth centra (e). Arrowheads, intervertebral cartilage. Scale bar is common among a–e.
Figure 7
Xenopus laevis, regression of the notochord from Stage (St.) 62–66 (a–d). Arrowheads indicate the ventral margin of the notochord. Scale bar is common among a–d.
Figure 8
Xenopus laevis, process of urostyle formation from Stage (St.) 62–66. Lateral (a, c, e, g) and ventral (b, d, f, h) views of the postsacral region at St. 62 (a, b), St. 63 (c, d), St. 65 (e, f), and St. 66 (g, h). The postsacral vertebrae are represented by 10, 11, and 12. hypo, hypochord.
