Tracking the origins of the bilaterian Hox patterning system: insights from the acoel flatworm Symsagittifera roscoffensis

Abstract

Genes of the Hox cluster encode for transcriptional regulators that show collinear expression along the anteroposterior (AP) body axis in all bilateral animals. However, it is still unclear when in the evolutionary history of bilaterians the Hox system first conferred positional identity along the AP-axis. Recent molecular phylogenies have convincingly shown that the acoel flatworms, traditionally classified within the Platyhelminthes, are the sister group of the remaining Bilateria, branching out before the common ancestor of protostomes, and deuterostomes (the so-called PDA). This key phylogenetic position offers the opportunity to search for the presence and early role of Hox cluster genes to pattern the AP axis in acoels. Here, we report on the cloning, genomic arrangement, and expression domains of Hox genes in Symsagittifera roscoffensis. Three Hox genes were detected: one from each of the major groups of Hox genes, which are anterior, central, and posterior. In bacterial artificial chromosome cloning, sequencing, and chromosomal fluorescence in situ hybridization, Hox genes were not observed as being clustered in a unique genomic region. Nevertheless, despite its dispersion within the genome, Hox genes are expressed in nested domains along the AP axis in the juvenile worm. The basic set of Hox genes in acoels and their coarse nested spatial deployment might be the first indicators of the role of Hox genes in the evolution of bilateral symmetry and AP positional identity from a hypothetical radial ancestor.