Zahn N et al. (2022), Normal Table of Xenopus development: a new grap...

XB-ART-59204

Development 2022 Jul 15;14914:. doi: 10.1242/dev.200356.

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Normal Table of Xenopus development: a new graphical resource.

Zahn N , James-Zorn C , Ponferrada VG , Adams DS , Grzymkowski J , Buchholz DR , Nascone-Yoder NM , Horb M , Moody SA , Vize PD , Zorn AM .

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Normal tables of development are essential for studies of embryogenesis, serving as an important resource for model organisms, including the frog Xenopus laevis. Xenopus has long been used to study developmental and cell biology, and is an increasingly important model for human birth defects and disease, genomics, proteomics and toxicology. Scientists utilize Nieuwkoop and Faber's classic 'Normal Table of Xenopus laevis (Daudin)' and accompanying illustrations to enable experimental reproducibility and reuse the illustrations in new publications and teaching. However, it is no longer possible to obtain permission for these copyrighted illustrations. We present 133 new, high-quality illustrations of X. laevis development from fertilization to metamorphosis, with additional views that were not available in the original collection. All the images are available on Xenbase, the Xenopus knowledgebase (http://www.xenbase.org/entry/zahn.do), for download and reuse under an attributable, non-commercial creative commons license. Additionally, we have compiled a 'Landmarks Table' of key morphological features and marker gene expression that can be used to distinguish stages quickly and reliably (https://www.xenbase.org/entry/landmarks-table.do). This new open-access resource will facilitate Xenopus research and teaching in the decades to come.

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Species referenced: Xenopus laevis
Genes referenced: actc1 aplnr astl3a.1 atp1a1 atp4a bmp4 cfap161 chrd cndp1 cxcl14 en2 fgf2 fgf8 foxj1 gsx1 hand2 hba3 hhex lhx1 nanos1 nkx2-1 nkx2-5 nodal5 nog pax2 pax3 pax8 pdia2 pitx2 ptf1a sall4 shh slc4a4 sox17a sox2 tbxt tekt3 tnni3 vegt wt1
GO keywords: metamorphosis [+]

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	Fig. 1. Cleavage-stage X. laevis embryos. (A) The fertilized egg NF stage 1. (B) NF stage 2 (two-cell stage). (C) NF stage 3 (four-cell stage). (D) NF stage 4 (eight-cell stage). (E) NF stage 5 (16-cell stage). (F) NF stage 6 (32-cell stage). Vegetal/ventral views of NF stage 4-6 (D-F) are unshaded line drawings. See Table S1 for staging landmarks. Views as indicated. Scale bar: 1 mm.
	Fig. 2. Blastula-, gastrula- and early neurula-stage X. laevis embryos. (A) NF stage 6.5 (morula); unshaded line drawing. (B) NF stage 7 (large-cell blastula); unshaded line drawing. (C) NF stage 8 (medium-cell blastula); membrane removed. (D) NF stage 9 (fine-cell blastula); membrane removed. (E) Gastrula-stage embryos, NF stage 10, NF stage 10.5 and NF stage 11; membrane removed. (F) NF stage 11.5, NF stage 12 and NF stage 12.5; membrane removed. See Table S1 for staging landmarks. Views as indicated. Scale bar: 1 mm.
	Fig. 3. Neural-stage X. laevis embryos. (A) NF stage 13 (slit-blastopore). (B) NF stage 16 (mid-neural fold). (C) NF stage 17 (late neural fold). (D) NF stage 18 (neural groove). (E) NF stage 19 (initial neural tube). (F) NF stage 21 (suture of neural groove completely closed). Orientation for anterior views is dorsal up; dorsal views have anterior left; lateral views have dorsal up and anterior left. See Table S1 for staging landmarks. Membrane removed in all embryos. Views as indicated. Scale bar: 1 mm.
	Fig. 4. Early tailbud-stage X. laevis embryos. (A) NF stage 22. (B) NF stage 23. (C) NF stage 24. (D) NF stage 25. (E) NF stage 26. (F) NF stage 28. Orientation for dorsal and ventral views is anterior left; lateral views have dorsal up and anterior left. See Table S1 for staging landmarks. Membrane removed in all embryos. Views as indicated. Scale bar: 1 mm.
	Fig. 5. Late tailbud-stage and free-swimming tadpole X. laevis embryos. (A) NF stage 29-30. (B) NF stage 33-34. (C) NF stage 35-36. (D) NF stage 37-38. Orientation for dorsal and ventral views is anterior left; lateral views have dorsal up and anterior left. See Table S1 for staging landmarks. Membrane removed in all embryos. Views as indicated. Scale bar: 1 mm.
	Fig. 6. Free-swimming and gut-coiling stages of X. laevis tadpoles. (A) NF stage 40. (B) NF stage 43. (C) NF stage 45. Orientation for ventral views is anterior left; lateral views have dorsal up and anterior left. See Table S1 for staging landmarks. Membrane removed in all embryos. Views as indicated. Scale bars: 1 mm.
	Fig. 7. X. laevis embryos during gut-coiling stages, NF stages 41-46, in ventral view, alongside new gut coiling diagrams. The coiling digestive tract is depicted as three lines of varying thickness. The esophagus/stomach (thickest black line) begins anteriorly on the left side of the body at NF stage 41. As gut lengthening and coiling progresses, the stomach shifts to the right side of the body by NF stage 46. The midgut (dark-gray line) and hindgut (thin light-gray line) form a rudimentary ‘S’ shape curve by NF stage 41-42, and at NF stage 43 the midgut and hindgut have lengthened to form a ‘hairpin loop’, visible from the left side. This loop turns ventrally by NF stage 44, becoming the U-shaped apex of the future intestinal coils. Throughout NF stages 44 to 46, the midgut and hindgut continue to lengthen and loop, with the apex rotating inward to form a compact intestine with tightly wound, counterclockwise coils. Gut-coiling diagrams designed by J.G. Stages as indicated. Scale bar: 1 mm.
	Fig. 8. Limb development in X. laevis tadpoles. (A) NF stage 48 tadpole. (B) NF stage 54. (C) Limb bud development from NF stage 48 to 54, reproduced in the style of the drawing in the Nieuwkoop and Faber Normal Table (Nieuwkoop and Faber, 1956, 1994), but in left-to-right progression, with forelimbs (above) and hindlimbs (below), at the stages indicated. See Table S1 for staging landmarks. Views as indicated. Scale bars: 1 mm.
	Fig. 9. Premetamorphosis- and prometamorphosis-stage X. laevis tadpoles. (A) NF stage 52 (premetamorphosis). (B) NF stage 54 (premetamorphosis). (C) NF stage 56 (prometamorphosis). (D) NF stage 57, (prometamorphosis). Each stage is shown in lateral, dorsal and anterior views. Ventral views are available on Xenbase. See Table S1 for more staging landmarks. Membrane removed in all embryos. Views as indicated. Scale bars: 1 mm.
	Fig. 10. Prometamorphosis- and climax metamorphosis-stage X. laevis tadpoles. (A) NF stage 59. (B) NF stage 63. (C) NF stage 66. Each stage is shown in lateral, dorsal and anterior views. Ventral views are available on Xenbase. See Table S1 for more staging landmarks. Membrane removed in all embryos. Views as indicated. Scale bars: 1 mm.

	Fig. S3. Xenbase XAO anatomy terms pages. Anatomical entities (i.e., primary germ layers, cell types, tissues, organs, structures) are individual terms in the Xenopus anatomy ontology, the XAO. XAO terms used in the Landmarks Table link to the specific XAO page where information about that term is collated. A. XAO page (Summary tab) for heart (XAO:0000064), where the definition is based on Nieuwkoop and Faber’s (1956) Normal Table criteria, and a curated list of molecular markers from Xenbase gene expression data are given. B. Expression tab of XAO page for heart collates all curated gene expression data. Columns are sortable based on number of primary sources, predominantly images (curated gene expression data from published research articles) and papers (where gene and anatomy are co-referenced). Click ‘Images’ heading to sort genes with the most curated gene expression figures from primary sources (and therefore the best candidates for molecular markers) at the top of the list.

References [+] :

Almasoudi, Otic Neurogenesis in Xenopus laevis: Proliferation, Differentiation, and the Role of Eya1. 2021, Pubmed, Xenbase