Regeneration of amphioxus oral cirri and its skeletal rods: implications for the origin of the vertebrate skeleton

Abstract

The oral cirri of amphioxus function as the first filter during feeding by eliminating unwanted large or noxious particulates. In this study, we were able to regenerate cirri following artificial amputation. This is the first firm observation of regeneration in amphioxus. Using this regeneration system, we studied skeletogenesis of the cellular skeleton of amphioxus oral cirri. During regeneration, the skeletal cells showed expression of fibrillar collagen and SoxE genes. These observations suggest that an evolutionarily conserved genetic regulatory system is involved in amphioxus cirrus and vertebrate cartilage skeletogenesis. In addition, Runx and SPARC/osteonectin expression were observed in regenerating cirral skeletal cells, indicating that cirral skeletogenesis is similar to vertebrate osteogenesis. We propose that the common ancestors of chordates possessed a genetic regulatory system that was the prototype of chondrogenesis and osteogenesis in vertebrates. Genome duplications caused divergence of this genetic regulatory system resulting in the emergence of cartilage and mineralized bone. The development of the vertebrate skeleton is an example of the functional segregation and subsequent recruitment of unique genetic materials that may account for the evolutionary diversification of novel cell types.