Burke AC et al. (1995), Hox genes and the evolution of vertebrate axial...

XB-ART-20140

Development 1995 Feb 01;1212:333-46.

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Hox genes and the evolution of vertebrate axial morphology.

Burke AC , Nelson CE , Morgan BA , Tabin C .

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A common form of evolutionary variation between vertebrate taxa is the different numbers of segments that contribute to various regions of the anterior-posterior axis; cervical vertebrae, thoracic vertebrae, etc. The term 'transposition' is used to describe this phenomenon. Genetic experiments with homeotic genes in mice have demonstrated that Hox genes are in part responsible for the specification of segmental identity along the anterior-posterior axis, and it has been proposed that an axial Hox code determines the morphology of individual vertebrae (Kessel, M. and Gruss, P. (1990) Science 249, 347-379). This paper presents a comparative study of the developmental patterns of homeobox gene expression and developmental morphology between animals that have homologous regulatory genes but different morphologies. The axial expression boundaries of 23 Hox genes were examined in the paraxial mesoderm of chick, and 16 in mouse embryos by in situ hybridization and immunolocalization techniques. Hox gene anterior expression boundaries were found to be transposed in concert with morphological boundaries. This data contributes a mechanistic level to the assumed homology of these regions in vertebrates. The recognition of mechanistic homology supports the historical homology of basic patterning mechanisms between all organisms that share these genes.

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Species referenced: Xenopus
Genes referenced: tbx2

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Fig. 5. Whole-mount in situ hybridizations with members of paralogue 6. Arrows indicate the anterior limit of gene expression in the paraxial mesoderm. (A) Chick (st. 25) Hoxc-6 expression boundary lies at somite level 19-20, aligned with the middle of the forelimb, at the first thoracic vertebra (T1). The paraxial mesoderm is labeled in an ‘arcade’ pattern along the flank: intersegmental labeling forms arches that meet dorsally in mid-segment, defining each somite. Somite labeling continues posteriorly into the tail. Laterally in the mid-flank there is a band of nearly continuous expression running anterior-posterior along the original boundary between somitic and lateral plate mesoderm. Lateral to this, in the body wall are streaks of inter segmental expression that trace the myosepta. (B) Mouse (E12) Hoxc-6 expression is aligned with the middle of the forelimb at somite level 12-13, the first thoracic vertebra, consistent with data reported by Jegalian et al. (1992). The mouse does not show an ‘arcade’ pattern of expression but the label is very strong in a near-continuous region of trunk mesoderm that covers approximately eight segments and extends laterally to the horizontal septum. Ventrally, the label is inter segmental, tracing the myosepta and rib positions in the body wall. (C) Goose at the morphological equivalent of a stage 25-26 chick embryo hybridized with chick the Hoxc-6 probe. Two different probes were used, both giving positive results with a variable degree of background that is comparable in chick and goose embryos. The labeling pattern is very similar to that of the chick including anterior-proximal limb labeling reported elsewhere (Sharp et al. 1988: Nelson et al. unpublished data), and a partial arcade pattern of somitic labeling. The paraxial mesoderm labeling starts at an axial level that aligns with the middle of the forelimb, at somite level 22-23, the first thoracic vertebra. (D) Whole-mount immunohistochemistry with XlhBox-1 antibody on stage 35 Xenopus embryos. Labeling begins at the border between somite 3 and somite 4, forming a continuous border across the neural tube and the mesoderm in agreement with labeling reported by Oliver et al. (1988).

Fig. 11. Schematic representation of the somite levels bridging the cervical-thoracic transition in mouse, chick, goose, Xenopus, zebrafish. Black bars represent the spinal nerves of the brachial plexus, and the level of the limb or fin bud is indicated with a curved line. The shaded somite levels indicate the level of Hoxc-6 expression as determined by whole-mount in situ hybridization, or immunohistochemistry. The level for the zebrafish is taken from Molven et al. (1990).