MacKenzie EM et al. (2022), Normal development in Xenopus laevis: A complem...

XB-ART-58857

Dev Dyn 2022 Aug 01;2518:1340-1356. doi: 10.1002/dvdy.465.

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Normal development in Xenopus laevis: A complementary staging table for the skull based on cartilage and bone.

MacKenzie EM , Atkins JB , Korneisel DE , Cantelon AS , McKinnell IW , Maddin HC .

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BACKGROUND: Xenopus laevis is a widely used model organism in the fields of genetics and development, and more recently evolution. At present, the most widely used staging table for X. laevis is based primarily on external features and does not describe the corresponding skull development in detail. Here, we describe skull development in X. laevis, complete with labeled figures, for each relevant stage in the most widely used staging table. RESULTS: We find skull development in X. laevis is, for the most part, distinct at each of the previously established stages based on external anatomy. However, variation does exist in the timing of onset of ossification of certain bones in the skull, which results in a range of stages where a skull element first ossifies. The overall sequence of ossification is less variable than the timing of ossification onset. CONCLUSIONS: While events in skull development vary somewhat between specimens, and in comparison, to external events, this staging table is useful in showing both when bones first appear and for documenting the range of temporal variance in X. laevis skull development more accurately than previously done. Furthermore, when only skull data are available, the approximate stage of a specimen can now be determined.

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Species referenced: Xenopus laevis
Genes referenced: asl cnr1 phb1 smpd1
GO keywords: ossification [+]

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	Figure 1. Development of the chondrocranium, NF stages 41–48, in X. laevis. From left to right, each row consists of a photograph in dorsal (left) and ventral view (right), with an illustration highlighting the dorsal (left) and ventral (right) views with structures drawn as if they were opaque. Cartilage is stained with Alcian blue. (A–C) NF stages 41–42; (D–F), NF stages 43–44; (G–I), NF stages 45–46; (J–L), NF stages 47–48. Lines that end with filled circles indicate small foramina and lines that end with open circles indicate larger foramina. Scale bars equal 1 mm. bf, basicranial fenestra; bhb, basihyobranchial; cb1-4, ceratobranchials one through four; cf, carotid foramen; ch, ceratohyal; ct, commisura terminalis; ef, exoccipital foramen; ir, infrarostral; mc, Meckel's cartilage; nf, nasal foramen; oa, occipital arch; oc, otic capsule; phb, planum hyobranchiale; pk, parachordal cartilage; pq, palatoquadrate; pqap, ascending process of the palatoquadrate; pqpa, pars articularis of the palatoquadrate; pqvp, ventrolateral process of the palatoquadrate; qe, quadratoethmoidal; so, subocular cartilage; sof, subocular fenestra; sr, suprarostral plate; tc, trabecular cartilage; tt, tenticular cartilage
	Figure 2. Development of the chondrocranium, NF stages 49–53, in X. laevis. From left to right, each row consists of a photograph in dorsal (left) and ventral view (right), with an illustration highlighting the dorsal (left) and ventral (right) views with structures drawn as if they were opaque. Cartilage is stained with Alcian blue. (A–C), NF stage 49; (D–F), NF stages 50–51; (G–I), NF stages 52–53. Lines that end with filled circles indicate small foramina and lines that end with open circles indicate larger foramina. Scale bars equal 1 mm. bf, basicranial fenestra; bhb, basihyobranchial; cb1-4, ceratobranchials one through four; cf, carotid foramen; ch, ceratohyal; ct, commisura terminalis; ef, exoccipital foramen; ir, infrarostral; mc, Meckel's cartilage; na, neural arches; nf, nasal foramen; oa, occipital arch; oc, otic capsule; phb, planum hyobranchiale; pk, parachordal cartilage; pq, palatoquadrate; pqap, ascending process of the palatoquadrate; pqpa, pars articularis of the palatoquadrate; pqvp, ventrolateral process of the palatoquadrate; qe, quadratoethmoidal; so, subocular cartilage; sof, subocular fenestra; sr, suprarostral plate; tc, trabecular cartilage; tt, tenticular cartilage
	Figure 3. Development of the skull, NF stages 54–59, in X. laevis. From left to right, each row consists of a photograph in dorsal (left) and ventral view (right), with an illustration in dorsal (left) and ventral (right) view. Bone is stained with Alizarin red S. (A–C) NF stages 54–55; (D–F), NF stage 56; (G–I), NF stage 57; (J–L), NF stages 58–59. Lines that end with filled circles indicate small foramina and lines that end with open circles indicate larger foramina. Scale bars equal 1 mm. a, atlas; asm, medial angulosplenial; ef, exoccipital foramen; ex, exoccipital; fp, frontoparietal; po, prootic; oc, otic capsule portion of the prootic; ps, parasphenoid.
	Figure 4. Development of the skull, NF stages 60–63, in X. laevis. From left to right, each row consists of a photograph in dorsal (left) and ventral view (right), with an illustration in dorsal (left) and ventral (right) view. Bone is stained with Alizarin red S. (A–C), NF stage 60; (D–F), NF stage 61, upper and lower jaw elements were digitally rearticulated with the skull in panels (D) and (E), the composite photos were used as the basis of the line drawings in (F); (G–I), NF stage 62, upper and lower jaw elements were digitally rearticulated with the skull in panels G and H, the composite photos were used as the basis of the line drawings in I; (J–L), NF stage 63. Lines that end with filled circles indicate small foramina and lines that end with open circles indicate larger foramina. Scale bars equal 1 mm. a, atlas; asm, medial angulosplenial; asl, lateral angulosplenial; d, dentary; ef, exoccipital foramen; ex, exoccipital; fo, foramen ovalis; fp, frontoparietal; m, maxilla; n, nasal; pf, pineal foramen; pm, premaxilla; po, prootic; oc, otic capsule portion of the prootic; ps, parasphenoid; s, squamosal; sm, septomaxilla.
	Figure 5. Development of the skull, NF stages 64–66, in X. laevis. From left to right, each row consists of a photograph in dorsal (left) and ventral view (right), with an illustration in dorsal (left) and ventral (right) view. Bone is stained with Alizarin red S. (A–C), NF stage 64; (D–F), NF stage 65; (G–I), NF stage 66. Lines that end with filled circles indicate small foramina and lines that end with open circles indicate larger foramina. Scale bars equal 1 mm. a, atlas; as, angulosplenial with fused medial and lateral ossifications; asm, medial angulosplenial; asl, lateral angulosplenial; co, columella; d, dentary; ef, exoccipital foramen; ex, exoccipital; fo, foramen ovalis; fp, frontoparietal; m, maxilla; n, nasal; pf, pineal foramen; pm, premaxilla; po, prootic; oc, otic capsule portion of the prootic; ps, parasphenoid; pt, pterygoid; s, squamosal; sm, septomaxilla; v, vomer.