Abstract
Somites are transitory metameric structures at the basis of the axial organization of vertebrate musculoskeletal system. During evolution, somites appear in the chordate phylum and compartmentalize mainly into the dermomyotome, the myotome, and the sclerotome in vertebrates. In this review, we summarized the existing literature about somite compartmentalization in Xenopus and compared it with other anamniote and amniote vertebrates. We also present and discuss a model that describes the evolutionary history of somite compartmentalization from ancestral chordates to amniote vertebrates. We propose that the ancestral organization of chordate somite, subdivided into a lateral compartment of multipotent somitic cells (MSCs) and a medial primitive myotome, evolves through two major transitions. From ancestral chordates to vertebrates, the cell potency of MSCs may have evolved and gave rise to all new vertebrate compartments, i.e., the dermomyome, its hypaxial region, and the sclerotome. From anamniote to amniote vertebrates, the lateral MSC territory may expand to the whole somite at the expense of primitive myotome and may probably facilitate sclerotome formation. We propose that successive modifications of the cell potency of some type of embryonic progenitors could be one of major processes of the vertebrate evolution.
Highlights
In amniote vertebrates, somite development has been the subject of intense research over many decades, giving insight into the morphological and molecular processes leading to their formation, compartmentalization, and differentiation (Brand-Saberi and Christ, 2000; Buckingham, 2001; Christ et al, 2007; Applebaum and Kalcheim, 2015; Hirst and Marcelle et al, 2015; Chal and Pourquié, 2017; Tani et al, 2020)
We recently identified Twist1 as a marker of migrating sclerotome progenitors in two amphibians, Xenopus and axolotl, and showed that both sclerotome and dermomyotome cells originate from a cell population located at lateral somitic frontier (LSF) revealing the ancestral location of multipotent somitic cells (MSCs) (Della Gaspera et al, 2012b; Della Gaspera et al, 2019)
4.2.1 Which Cell Type Could be at the Evolutionary Origin of Multipotent Somitic Cells? In Xenopus, MSCs give rise to all the new structures that emerged in vertebrates, the dermomyotome as such, its hypaxial region, and the sclerotome
Summary
Somite development has been the subject of intense research over many decades, giving insight into the morphological and molecular processes leading to their formation, compartmentalization, and differentiation (Brand-Saberi and Christ, 2000; Buckingham, 2001; Christ et al, 2007; Applebaum and Kalcheim, 2015; Hirst and Marcelle et al, 2015; Chal and Pourquié, 2017; Tani et al, 2020). We recently proposed a model of somite organization that describes the evolutionary history of their compartmentalization from the last common ancestor of chordates to amniote vertebrates and explains the common lateral origin of the sclerotome and the dermomyotome (Della Gaspera et al, 2019). We discuss the arguments in favor of the present model tracing the evolutionary history of the somite, and its potential implication on the formation of muscleassociated tissues
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