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The left-right body axis is coordinately aligned with the orthogonal dorsoventral and anterioposterior body axes. The developmental mechanisms that regulate axis coordination are unknown. Here it is shown that the cardiac left-right orientation in zebrafish (Danio rerio) is randomized in notochord-defective no tail and floating head mutants. no tail (Brachyury) and floating head (Xnot) encode putative transcription factors that are expressed in the organizer and notochord, structures which regulate dorsoventral and anterioposterior development in vertebrate embryos. Results from dorsal tissue extirpation and cardiac primordia explantation indicate that cardiac left-right orientation is dependent on dorsoanterior structures including the notochord and is specified during neural fold stages in Xenopus laevis. Thus, the notochord coordinates the development of all three body axes in the vertebrate body plan.
FIG. 1. Zebrafish mutants with defective notochords have randomized
cardiac orientation. Ventral view of embryos stained with
MF20 (Gonzalez-Sanchez and Bader, 1984) to view the cardiac ventricle
and outflow tract, indicated by arrow. Atrium is lightly
stained and out of the focal plane. Anterior is at the top. (A) Phenotypically
wild-type embryo from no tail cross, displaying normal
cardiac left–right orientation. (B) Floating head (flh) mutant with
cardiac left –right reversal and smaller area of staining. (C) ntl mutant
with a normal heart. (D) ntl mutant with a left–right reversed
heart. Scale bar represents 100 mm.
FIG. 2. Specification of cardiac left –right orientation. (A) Sample X. laevis embryo depicting region of explanted precardiac mesoderm at stage 18. Explants from stage 18 embryos in which the left– right orientation was (B) normal or (C) reversed. The darkly stained conus (c) and ventricle (v) and the lightly stained atrium (a) were morphologically distinct. The open extremity of the atrium appeared flared and attached by unstained mesoderm to the enclosing surface of the explant. The left–right orientation was assessed with bifocal microscopy as previously described. Scale bar represents (A) 2 mm and (B, C) 50 mm.
FIG. 3. Extirpation of dorsal tissue disrupts notochord development. Equivalent amounts of dorsal tissues, including notochord, were
deleted in X. laevis embryos by extirpations at different stages. (A) Diagram of tissue extirpation on a neural fold stage embryo (stage 15).
(B) Diagram of tissue extirpation on tailbud stage embryo. (C) Notochord labeled by in situ hybridization in stage 36 embryo from which
dorsal tissue was extirpated at stage 18. (D) Notochord labeled by in situ hybridization in stage 36 embryo from which dorsal tissue was
extirpated at tailbud (stage 28). Arrows mark the boundaries of notochord deficiency. Scale bar represents 2 mm.
FIG. 4. Extirpation of dorsal tissue during early neurula stages randomizes cardiac left– right orientation. Graph of results from extirpation experiments diagrammed in Fig. 3. Solid bars represent the percentage of left –right cardiac reversals in embryos from which dorsal tissue was extirpated at the indicated stages; hatched bars represent mock-dissected controls. Vertical numbers above each bar indicate the number of embryos examined. * indicates P 0.005 by x2 analysis, comparing extirpations and control dissections at the same stage. nd indicates not determined.
