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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.
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).
