Somite Compartments in Amphioxus and Its Implications on the Evolution of the Vertebrate Skeletal Tissues

Abstract

Mineralized skeletal tissues of vertebrates are an evolutionary novelty within the chordate lineage. While the progenitor cells that contribute to vertebrate skeletal tissues are known to have two embryonic origins, the mesoderm and neural crest, the evolutionary origin of their developmental process remains unclear. Using cephalochordate amphioxus as our model, we found that cells at the lateral wall of the amphioxus somite express SPARC (a crucial gene for tissue mineralization) and various collagen genes. During development, some of these cells expand medially to surround the axial structures, including the neural tube, notochord and gut, while others expand laterally and ventrally to underlie the epidermis. Eventually these cell populations are found closely associated with the collagenous matrix around the neural tube, notochord, and dorsal aorta, and also with the dense collagen sheets underneath the epidermis. Using known genetic markers for distinct vertebrate somite compartments, we showed that the lateral wall of amphioxus somite likely corresponds to the vertebrate dermomyotome and lateral plate mesoderm. Furthermore, we demonstrated a conserved role for BMP signaling pathway in somite patterning of both amphioxus and vertebrates. These results suggest that compartmentalized somites and their contribution to primitive skeletal tissues are ancient traits that date back to the chordate common ancestor. The finding of SPARC-expressing skeletal scaffold in amphioxus further supports previous hypothesis regarding SPARC gene family expansion in the elaboration of the vertebrate mineralized skeleton.

Evolution of Somite Compartmentalization: A View From Xenopus

“…Following metamorphosis, embryonic muscles degenerate and AMPs give rise to both adult muscle fibers and muscle satellite cells ( Chaturvedi et al, 2017 ; Boukhatmi and Bray, 2018 ). Satellite cells have also been described in another protostome, the crustacean species Parhyale hawaiensis ( Konstantinides and Averof, 2014 ) and in the mesothelium of amphioxus somites, a muscle-associated tissue, which potentially derived from lateral somitic domain ( Somorjai et al, 2012 ; Mansfield et al, 2015 ; Yong et al, 2021 ). Hence, AMP-like cells are probably already present in Urbilateria ( Figure 8A ).…”

“…One possible scenario is that the lineage of AMP-like cells could have evolved and increased their cell potency capacities to also give rise to cartilage-like cells and become MSCs. Yong et al (2021) suggested that the lateral somitic domain in amphioxus could be first a connective tissue probably associated with muscle and then co-opted genes involved in cartilage and bone development during vertebrate evolution. Alternatively, it has been proposed that sclerotome cells could have evolutionarily derived from the cartilage-like cells of the medial and ventral mesentery that expressed SoxD, SoxE, and Collagen A.…”

“…In cephalochordates, histological analyses show that the somitic dorso-lateral external cells are not equivalent to the vertebrate dermomyotome ( Holland, 1996 ; Holland et al, 1999 ; Mansfield et al, 2015 ). However, pax3/7 has been detected in the dorso-lateral region of amphioxus somites indicating that these external cells possess some features of vertebrate dermomyotome ( Yong et al, 2021 ). Moreover, the lateral somitic domain of amphioxus can be subdivided at mid/late neurula stage into three subdomains with specific expression of Pax3/7, Pax1/9, and Hand genes suggesting that somitic compartmentalization already exists in the ancestral chordates ( Figure 3A ).…”

“…For example, Pax3/7 is expressed in the central domain (CD), Pax1/9 in the dorsal domain (DD) and Hand in the ventral domain (VD). Adapted from Yong et al (2021) . (B) The first phases of compartmentalization are both medio-lateral and antero-posterior in zebrafish, mainly medio-lateral in Xenopus and mainly dorso-ventral in chick and mouse.…”

“…The lateral domain also gives rise to the dorsal external cells, the medial fin box mesothelium (FBM) and the latero-ventral perivisceral mesothelium (PVM). Modified from Mansfield et al (2015) and Yong et al (2021) . ES, epithelial somite; NC, notochord; NP, neural plate; END, endoderm; ECT, ectoderm.…”