Possible rules for the ancestral origin of Hox gene collinearity

Abstract

The Hox gene cluster is believed to have formed from a single ProtoHox gene by repeated cycles of the following events: tandem gene duplication, mutation to generate a new expression boundary along the embryonic axis, and acquisition of a new Hox patterning function. The Hox cluster in Bilateria evolved in compliance with the so-called collinearity rule. That is, the order of the genes along the chromosome corresponds with the order of their embryonic expression domains along the head-tail axis. Gaunt (2015) suggested that collinearity may have arisen as a mechanism to minimise the incidence of boundaries between active and inactive genes within the Hox cluster. We now attempt to clarify the model by presenting it in the form of three rules: 1) no two Hox genes may persist in the same cluster with the same anterior boundary of activity in the same tissue; 2) an inactive Hox gene must not be flanked by two active Hox genes; 3) an active Hox gene must not be flanked by two inactive genes. We provide evidence and illustrative computer simulations to show that these rules, which can apply only to partially overlapping patterns of Hox activity, may account for the ancestral origin of Hox gene collinearity.

Keywords: Bilateria; Embryo; Evolution; Modelling.