Evidence that Hoxa expression domains are evolutionarily transposed in spinal ganglia, and are established by forward spreading in paraxial mesoderm

Abstract

Transposition of anatomical structures along the anteroposterior axis has been a commonly used mechanism for changing body proportions during the course of evolutionary time. Earlier work (Gaunt, S.J., 1994. Conservation in the Hox code during morphological evolution. Int. J. Dev. Biol. 38, 549–552; Burke, A.C., Nelson, C.E., Morgan, B.A., Tabin, C., 1995. Hox genes and the evolution of vertebrate axial morphology. Development 121, 333–346) showed how transposition in mesodermal derivatives (vertebrae) could be attributed to transposition in the expression of Hox genes along the axial series of somites. We now show how transposition in the segmental arrangement of the spinal nerves can also be correlated with shifts in the expression domains of Hox genes. Specifically, we show how the expression domains of Hoxa-7, a-9 and a-10 in spinal ganglia correspond similarly in both mouse and chick with the positions of the brachial and lumbosacral plexuses, and that this is true even though the brachial plexus of chick is shifted posteriorly, relative to mouse, by seven segmental units. In spite of these marked species differences in the boundaries of Hoxa-7 expression, cis regulatory elements located up to 5 kb upstream of the chick Hoxa-7 gene showed much functional and structural conservation with those described in the mouse (Puschel, A.W., Balling, R., Gruss, P., 1991. Separate elements cause lineage restriction and specify boundaries of Hox-1.1 expression. Development 112, 279–287; Knittel, T., Kessel, M., Kim, M.H., Gruss, P., 1995. A conserved enhancer of the human and murine Hoxa-7 gene specifies the anterior boundary of expression during embryonal development. Development 121, 1077–1088). We also show that chick Hoxa-7 and a-10 expression domains spread forward into regions of somites that are initially negative for the expression of these genes. We discuss this as evidence that Hox expression in paraxial mesoderm spreads forward, as earlier found for neurectoderm and lateral plate mesoderm, in a process that occurs independently of cell movement.