Normal Table of Xenopus development: a new graphical resource

Abstract

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.

Keywords: Xenopus laevis; AMA; Amphibian development; EAMA; Embryo; FETAX; Metamorphosis; Normal table.

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, , 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.