Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny

Vertebrates have seven types of fibrillar collagens that are encoded by 11 genes. Types I, V, and XXIV collagens are components of mineralized bone, whereas types II, XI, and XXVII collagens are components of cartilage. In this study, we traced the molecular evolutionary history of chordate collagen genes and examined how gene duplications gave rise to the collagen genes used for skeletons. Our analyses of deuterostome collagen genes, including one amphioxus gene that we identified in this study, suggest that the common ancestors of deuterostomes possessed three fibrillar collagen genes. Expression analyses of chordate fibrillar collagen genes suggest that in the ancestors of chordates, fibrillar collagen was co-opted to the formation of the notochord sheath independently in three clades. Our results also imply that co-option of collagen genes to cartilage occurred in clade A (col2A1), clade B (col11A1, 11A2), and clade C (COL27A1). Similarly, some fibrillar collagen genes have been co-opted for mineralized bone independently from clade A genes (col1A1, 1A2, 5A2), clade B genes (col5A1), and clade C genes (COL24A1). These frequent co-options for notochord, cartilage, and mineralized bone must have been accompanied by the rapid evolution of cis-regulatory elements for transcription. In addition, we found that one of the ascidian fibrillar collagen genes possesses an amino acid insertion at the identical site of the C-terminal noncollagenous domain in vertebrate fibrillar collagen genes. This observation raises a suspicion about the relatively well-accepted phylogeny of the close relationship between amphioxus and vertebrates.