Chalmers AD and Slack JM (2000), The Xenopus tadpole gut: fate maps and morphoge...

XB-ART-11771

Development 2000 Jan 01;1272:381-92. doi: 10.1242/dev.127.2.381.

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The Xenopus tadpole gut: fate maps and morphogenetic movements.

Chalmers AD , Slack JM .

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We have produced a comprehensive fate map showing where the organs of the gut and respiratory system are derived from in the early Xenopus laevis endoderm. We also show the origin of the associated smooth muscle layer on a separate fate map. Comparison of the two maps shows that for most organs of the gut the prospective epithelium and smooth muscle do not overlie each other in the early embryo but come together at a later stage. These fate maps should be useful for future studies into endoderm specification. It was not previously known how the elongation of the endoderm occurs, how the single-layered dorsal and many-layered ventral endoderm gives rise to the single layered epithelium, and whether or not the archenteron cavity actually gives rise to the gut lumen. Using a variety of labelling procedures we show firstly, that radial intercalation occurs in the gut transforming a short thick tube into a long thin tube; secondly, that the archenteron lining does not become the definitive gut lumen. Instead the archenteron cavity almost closes at tailbud stages before providing a nucleus for the definitive gut cavity, which opens up during elongation. Based on this work we present a model explaining the morphogenesis of the gut.

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Species referenced: Xenopus laevis
Genes referenced: fabp2 pdx1 sia1

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	Fig. 1. The stage 46 Xenopus tadpole gut. (A) Schematic diagram (ventral view/anterior at the top). (B) Whole-mount drawing (ventral and lateral views). The gut has been shaded dark grey and the liver and pancreas light grey. oe, oesophagus; lv, liver; gb, gall bladder; pa, pancreas; sia, proximal small intestine; sib, external coil of small intestine; sic, internal coil of small intestine; lic, internal coil of large intestine; lid, distal large intestine; st, stomach; pr, proctodaeum; ht, heart. Figure adapted from Chalmers and Slack (1998), with permission. Bar, 1 mm.
	Fig. 2. The 14 regions used for fate mapping. (A) Left view of a stage 14 whole mount. (B) Dorsal view of a stage 14 whole mount. (C) Parasagittal section of a stage 14 embryo. (D) Transverse section of a stage 14 embryo. The grafting regions are shown on the embryos using the following labels: 1, extreme anterior; 2, anterior dorsal; 3, anterior right; 4, anterior left; 5, anterior ventral; 6, middle dorsal; 7, middle right; 8, middle left; 9, middle ventral; 10, posterior dorsal; 11, posterior right; 12, posterior left, 13; posterior ventral; 14 extreme posterior.
	Fig. 3. Examples of FDA labelling. For each example a labelled drawing of a section (A,C,E,G,I) and a photograph of the labelled section (B,D,F,H,J) are shown. A whole-mount drawing is also included at the top of the figure to show the position of the sections in the tadpole. (A,B) Labelled pharynx. (C,D) Labelled pancreas and small intestine. (E,F) Labelled small intestine. (G,H) Labelled proctodaeum. (I,J) Labelled smooth muscle in the large intestine. (K) Smooth muscle layer in the tadpole gut. In B,D,F,H and J, arrowheads highlight labelled epithelia and arrows highlight smooth muscle. ph, pharynx; tn, tongue; sia, proximal small intestine; pa, pancreas; st, stomach; lid, distal large intestine; pr, proctodaeum. Bar, 200 mm (B); 120 mm (F,H); 95 mm (D,J); 30 mm (K).
	Fig. 4. Representative examples of the fate mapping. Drawings of sections from representative examples of eight of the 14 regions are shown. The position of the FDA label has been added to the drawings (green). A whole-mount drawing and drawings of standard sections are also shown to aid interpretation of the labelled sections (adapted from Chalmers and Slack, 1998). ph, pharynx; tn, tongue; ov, otic vesicle; no, notochord; ht, heart; lv, liver; tr, trachea; sia, proximal small intestine; sib, external coil of small intestine; sic, internal coil of small intestine; lic, internal coil of large intestine; lid, distal large intestine; pa, pancreas; bd, bile duct; lu, lungs; nd, nephritic ducts; pr, proctodaeum.
	Fig. 5. The endoderm and smooth muscle layer fate maps. (A) The endoderm fate map. The organ rudiments of the extreme anterior (1) (yellow), anterior dorsal (2) and ventral (5) (red), middle dorsal (6) and ventral (9) (blue), posterior dorsal (10) and ventral (13) (green) and extreme posterior (14) (black) endoderm are labelled at the position they form on a drawing of a stage 14 embryo. For the sake of clarity the lateral rudiments have not been included. (B) Projection of the early ventral endoderm onto the tadpole gut. The extreme anterior (1) (yellow), anterior ventral (5) (red), middle ventral (9) (blue), posterior ventral (13) (green) and extreme posterior regions (14) (black) are shaded in the embryo and in the regions they will give rise to in the tadpole gut. The drawings are viewed from the ventral side with anterior at the top. (C) Projection of the early dorsal endoderm. As in B but for the dorsal rather than ventral regions. (D) Location of the dorsal, lateral and ventral digestive tract rudiments for comparison with the smooth muscle layer fate map. The lateral rudiments are shown in the middle of the dorsal/ventral axis to represent their position on the side of the embryo. (E) Smooth muscle layer fate map. The position in the mesoderm of the lateral and ventral rudiments for the smooth muscle layer of the gut is shown on a drawing of a stage 14 embryo. None of the dorsal regions were fated to form smooth muscle. (F) Presumptive gene expression domains in the dorsal and ventral Xenopus endoderm. Regions of the endoderm that will give rise to tissues that express Xlhbox8 or IFABP in normal development are highlighted with coloured diagonal lines. ph, pharynx; tn, tongue; tr, trachea; lu, lungs; lv, liver; gb, gall bladder; pa, pancreas; bd, bile duct; oe, oesophagus; st, stomach; si, small intestine; sia, proximal small intestine; sib, external coil of small intestine; sic, internal coil of small intestine; li, large intestine; lic, internal coil of large intestine; lid, distal large intestine; pr, proctodaeum.
	Fig. 6. DiI labelling of the Xenopus endoderm. (A) Section of control stage 14 embryo. The four labelling positions are marked with arrows. (B) Section of control stage 40 embryo. (C) Whole-mount stage 45 control gut. (D) Section of floor DiI labelling at stage 14 (the archenteron is shrunk because of the replacement of the roof). Insert shows high magnification view. (E) Section of floor DiI labelling visualised at stage 39. (F) Floor DiI labelling visualised in a stage 45 whole mount. (G) Section of middle labelling at stage 14. (H) Section of middle DiI labelling visualised at stage 39. (I) Middle DiI labelling visualised in a stage 45 whole mount. (J) Section of ventral DiI labelling at stage 14. (K) Section of ventral DiI labelling visualised at stage 39. (L) Ventral DiI labelling visualised in a stage 45 whole mount. (M) Section of dorsal DiI labelling at stage 14. Insert shows high magnification view. (N) Section of dorsal DiI labelling visualised at stage 39. (O) Dorsal DiI labelling visualised in a stage 45 whole mount. Arrows highlight DiI label. no, notochord; ar-r, archenteron roof; ar-f, archenteron floor.
	Fig. 7. DiI/FDA double labelling of the Xenopus endoderm. (A) Section of stage 14 control embryo. The four labelling positions are marked with arrows. (B) Floor DiI and ventral FDA double labelling visualised in a stage 45 whole mount. (C) Floor DiI and dorsal FDA double labelling visualised in a stage 45 whole mount. (D) Middle DiI and ventral FDA double labelling visualised in a stage 45 whole mount.
	Fig. 8. The archenteron cavity during development. The superficial cell layer that gives rise to the cells lining the archenteron was labelled at stage 9/10. The labelled cells lining the archenteron could then be followed during development. (A) Unlabelled stage 14 embryo. (B) Biotin-labelled cells at stage 14 (arrow). (C) Unlabelled stage 38 embryo showing endogenous signal in the epidermis but not the gut. (D,E) Biotin-labelled cells (arrow) at stage 38 showing partial closure of archenteron. (F) Biotinlabelled cells (arrow) at stage 40 showing small persistent archenteron. The label is lost from the internalised cells. (G) Biotin-labelled cells in the posterior gut of a stage 40 embryo showing new cavity opening (arrow, biotin; arrowhead, unlabelled). (H) Biotin-labelled cells in the posterior gut at stage 42 showing cavity is only partially labelled (arrow, biotin; arrowhead, unlabelled). (I) Biotin-labelled cells (arrow) in stage 44 gut showing partial labelling of new cavity. Bar, 100 mm; 50 mm (E,G-I).
	Fig. 9. Morphogenesis of the gut epithelium. From stage 14 to stage 38 the embryonic archenteron narrows to a small cavity. During this time the dorsal (red), floor (blue), middle (black) and ventral (green) cell populations retain their relative positions. After stage 38 the gut cavity starts to open from the remains of the archenteron to split the ventral endoderm. This produces a cavity, part of which originated from the archenteron (solid line) and part is the new cavity (dashed line). By stage 45 the gut cavity is fully open. The splitting of the ventral endoderm places the cells of the archenteron (red + blue) on one side of the cavity and the middle (black) and ventral endoderm cells (green) on the other side. Radial intercalation may drive both the opening of the gut cavity and the elongation of the gut.