Lamprey type II collagen and Sox9 reveal an ancient origin of the vertebrate collagenous skeleton.
Type II collagen is the major cartilage matrix protein in the jawed vertebrate skeleton. Lampreys and hagfishes, by contrast, are thought to have noncollagenous cartilage. This difference in skeletal structure has led to the hypothesis that the vertebrate common ancestor had a noncollagenous skeleton, with type II collagen becoming the predominant cartilage matrix protein after the divergence of jawless fish from the jawed vertebrates approximately 500 million years ago. Here we report that lampreys have two type II collagen (Col2alpha1) genes that are expressed during development of the cartilaginous skeleton. We also demonstrate that the adult lamprey skeleton is rich in Col2alpha1 protein. Furthermore, we have isolated a lamprey orthologue of Sox9, a direct transcriptional regulator of Col2alpha1 in jawed vertebrates, and show that it is coexpressed with both Col2alpha1 genes during skeletal development. These results reveal that the genetic pathway for chondrogenesis in lampreys and gnathostomes is conserved through the activation of cartilage matrix molecules and suggest that a collagenous skeleton evolved surprisingly early in vertebrate evolution.
Zhang
Guangjun
G
Department of Zoology, University of Florida, 223 Bartram Hall, Gainesville, 32611, USA.
Miyamoto
Michael M
MM
Cohn
Martin J
MJ
D000375:Aging / Q000502:physiology; D000818:Animals; D020219:Chondrogenesis; D024043:Collagen Type II / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D006609:High Mobility Group Proteins / Q000235:genetics / Q000378:metabolism*; D006801:Humans; D007798:Lampreys / Q000196:embryology / Q000254:growth & development / Q000378:metabolism*; D008969:Molecular Sequence Data; D010802:Phylogeny; D055758:SOX9 Transcription Factor; D012863:Skeleton; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
D024043:Collagen Type II; D006609:High Mobility Group Proteins; D055758:SOX9 Transcription Factor; C527932:SOX9 protein, human; D014157:Transcription Factors