An axial domain of HOM/Hox gene expression is formed by morphogenetic alignment of independently specified cell lineages in the leech Helobdella

Abstract

The homeobox gene Lox2, a member of the HOM/Hox gene class, is expressed in a restricted domain along the anteroposterior (A-P) body axis of the leech Helobdella. The segmental tissues of the leech embryo arise from the parallel merger of five distinct and bilaterally paired cell lineages generated by embryonic stem cells or teloblasts. Injection of cell lineage tracers coupled with anti-LOX2 immunochemistry reveals that all five teloblast lineages generate central nervous system neurons that express the LOX2 protein, and that each lineage expresses LOX2 within a similar domain of body segments. Some lineally identified neurons display anti-LOX2 immunoreactivity over the entire expression domain, but the OM7 neuron has a distinctively high level of LOX2 expression, which is restricted to the seventh midbody ganglion. To ascertain the role of positional information in the axial patterning of LOX2 expression, we performed focal cell ablations that displaced one or another of the teloblast lineages out of segmental register with the other axial tissues. Such displacements brought about a corresponding shift in the LOX2 expression of the perturbed lineage, and had little or no effect on the LOX2 expression of the other, unperturbed lineages. This result indicates that the axial domain of LOX2 expression is not specified by positional cues acting coordinately across the various teloblast lineages, nor would it seem that the expression domain is imprinted from one lineage to the others. Rather, the different teloblast lineages acquire their axial patterns independently, and secondarily bring these patterns into alignment along the A-P axis through a process of morphogenetic assembly.