Della Gaspera B et al. (2021), Evolution of Somite Compartmentalization: A Vie...

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Front Cell Dev Biol 2021 Jan 01;9:790847. doi: 10.3389/fcell.2021.790847.

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Evolution of Somite Compartmentalization: A View From Xenopus.

Della Gaspera B , Weill L , Chanoine C .

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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.

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Species referenced: Xenopus laevis
Genes referenced: bmp4 cdknx cxcl12 ebf2 ebf3 fgf4 fgf8 fxyd1 hes6 itk mef2c mef2d meox2 myf5 myf6 myod1 myog myrf nodal pax1 pax3 pax7 pitx2 rbm24 scx shh sim1 sox5 tbx6 tbxt tcf15 twist1 wnt11
GO keywords: gastrulation [+]

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	FIGURE 1. Main characteristics of somite compartmentalization in vertebrates. (A) Comparison of somite organization between amniotes and anamniotes. Schematic view of somites slightly after the phylotypic stage. In anamniotes, the somite organization is adapted to the ondulatory swimming of the larvae and harbors a chevron shape with the myotome occupying the majority of the somite. The thin layer of dermomyotome cells is in dorso-lateral position and the sclerotome layer is ventro-medially stranded between the myotome and the midline structures (neural tube and notochord). The syndetome at the origin of the dorsal tendons arises from the sclerotome. The tenocytes project cytoplasmic extensions between muscle cells of adjacent somites. In amniotes, the spatial organization is the same, but the myotome compartment is reduced and the sclerotome is larger. (B) Somite compartmentalization in amphioxus. The anterior and intermediate somites are formed by enterocoely from the endoderm at the early neurula stage. The somites are subdivided into a medial myotome and a lateral domain at late neurula stage. The sclerotome-like cells seem to migrate from the lateral domain to position themselves medially between the myotome and the axial structures. 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. (C) Somite compartmentalization in Xenopus. The somite is initially medio-laterally organized with the myotome in medial position and multipotent somitic cells (MSCs) in lateral one. The myotome forms first and is initially made up of a medial- and a lateral-population of muscle cells. The MSCs appear at lateral somitic Frontier (LSF) at the beginning of neurulation and envelop next dorsally and ventrally the myotome to give rise to both dermomyotome and sclerotome.
	FIGURE 2. The myogenic waves and the myotome formation in amniotes and Xenopus. (A) The myotome is essentially derived from the dermomyotome in amniotes. The primary myotome is made of mononucleated cells arising from the four borders of the dermomyotome. Next cells coming from the central dermomyotome invade the primary myotome and contribute to the myotome growth. Hence, two myogenic waves are at the origin of myotome formation. Modified from Lagha et al. (2008a). (B) Myotome is the main somite compartment in Xenopus and is formed by at least three myogenic waves. The first myogenic wave is made up of two subpopulations, a medial and a lateral one, constitutes the primitive myotome and arises directly from paraxial mesoderm. The second myogenic wave arises from epaxial and hypaxial border of the dermomyotome at stage 28–30. The third myogenic wave has been visualized by myf5 mRNA staining that marked isolated round cells inside the myotome at stage 37–38. The myotome is initially made up of mononucleated fibers until stage 45 when the first multinucleated muscle fibers were observed. Hence, it can be considered that both the first wave of primitive myotome and the second wave of hypaxial and epaxial dermomyotome contribute to the formation of primary myotome. The third could participate to plurinucleated fibers formation and myotome growth. St., stage.
	FIGURE 3. Comparison of compartmentalization modes between amphioxus, zebrafish, Xenopus, chick and mouse. (A) The lateral domain of amphioxus somite is already compartmentalized at mid neurula stage and possesses progenitors that give rise to the external cells layer, the sclerotome-like compartment but also the lateral plate mesoderm and the fin box mesothelium at stage G9. The lateral domain can be subdivided into three subdomains which express different set of genes. 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. In zebrafish, an apparent movement of somite rotation relocated the different cell populations during the segmentation period. The posterior cells elongate toward the anterior region of the somites (straight black arrows) and give rise to fast fibers, the anterior cells were relocated in the surface outside of the somites (curved black arrows) and give rise to the dermomyotome. In addition, the medially adaxial cells migrate laterally toward the myotome periphery (grey arrows) and differentiate both into pioneer cells and superficial slow fibers. The endotome cells migrate toward the midline aorta (light blue hollow arrows). The appearance and location of MSCs are unknown and difficult to infer in zebrafish. Somites at 12 and 24 hpf (hour post fertilization). In Xenopus, lateral MSCs envelop the myotome ventrally and dorsally to give rise to the dermomyotome and the sclerotome (bended black arrows). Both in Xenopus and zebrafish, the lateral fast fibers are in dorsal and ventral position around the medial ones which are located close to the notochord. Somites at mid-neurulation (stage 18) and at tailbud stage (stage 28). In amniotes, chick, and mouse, the newly formed somites are naïve structures, made up of MSCs which subdivide into a dorso-lateral dermomyotome and a ventro-medial sclerotome. The dermomyotome cells remain epithelial whereas the sclerotome cells undergo EMT (epithelial mesenchymal transition). In chick, the pioneer cells begin to express Myf5 and Myod1 medially at epithelial somite stage, and become the first myocytes used as a scaffold for the construction of primary myotome. For zebrafish modified from Buckingham and Vincent, (2009) and Keenan and Currie, (2019). For chick and mouse, modified from Buckingham, (2001). (C) Comparison of muscle cell movements during somitogenesis between zebrafish, Xenopus, and axolotl. Zebrafish: Cell movements during apparent somite rotation. Lineage tracing of cells inside a somite makes it possible to follow their movements. Myogenic cells (curved arrow), Dermomyotome precursors (straight arrow). Explained in (A). Xenopus: Myogenic cells are first oriented perpendicular to the antero-posterior axis, before becoming parallel to it during apparent somite rotation (black arrows). Axolotl: Differentiation of myogenic cells inside somites is characterized by cell elongation in antero-posterior direction progressing medio‐laterally (hollow arrows). Adaxial cells have been described in axolotl but are not represented here (Banfi et al., 2012). For zebrafish, modified from Stellabotte et al. (2007). For Xenopus, modified from Keller, (2000). For axolotl summarized from Neff et al. (1989), Radice et al. (1989), and Keller, (2000).
	FIGURE 4. Summary of myogenic regulatory factor (MRF) functions in mouse and zebrafish models. (A) Timing of myofibers formation during embryonic and fetal myogenesis in mice. (B) Summary of the main phenotypes of single KO mice for Myod1, Myf5, or Myogenin, double KO mice for Myod and Myf5, and triple KO mice for Myod1, Myf5, and Myf6. Myoblasts formation requires either Myod1 or Myf5. Myog is necessary for muscle differentiation and Myf6 can compensate the absence of Myod1 and Myf5 only during embryonic myogenesis. Myf6 KO mice did not show muscle development defects. Modified from Hernández-Hernández et al. (2017). (C) Genetic hierarchy during embryonic myogenesis in epaxial and hypaxial domain of the somite. Mice invalidated for the three genes Pax3, Myf5, and Myf6 show an absence of all skeletal muscles in the trunk indicating that these factors act upstream of Myod1. While the myogenesis in the hypaxial domain is Pax3 dependent, a program initiated by Myf5, Pax3 independent exists in the epaxial domain. Dashed lines indicate that the regulation of Myod1 expression by Pax3 is probably indirect through Pitx2 and Six transcription factors. Head mouse myogenesis is not presented here. For a more detailed analysis of MRF KO mice, see Bismuth and Relaix (2010), Comai et al. (2014), and Buckingham (2017). (D) Main phenotypes of zebrafish single mutants for Myod1, Myf5, or Myog and double mutant for Myod1 and Myf5. The zebrafish mutant for Myf6 did not show abnormal muscle development. In zebrafish, Myod1 is necessary for normal cranial muscle development whereas Myf6 does not compensate the absence of Myod1 and Myf5. (E) Summary of the MRF phylogeny in bilaterians. Aase-Remedios et al. (2020) propose that the four vertebrate genes coding for MRFs do not result from two rounds of whole genome duplication (2R WGD) of a single ancestral gene, that would have taken place between ancestral chordates and vertebrates. Instead, a cluster of two MRF genes generated by tandem duplication predates the 2R WGD. One gene of this cluster generates via 2R WGD and gene losses the early vertebrate MRFs (Myf5 and Myod1), and the other generates the late vertebrate MRFs (Myf6 and Myogenin). The first vertical dashed line indicates that tunicate MRFs could be the orthologs of either the early or the late ancestral MRF gene preceding the 2R WGD. The two MRF genes present in cyclostome species could be the orthologs of the early MRF gene. Cyclostomes would have diverged from gnathostomes after the first R WGD and before the second R WGD (Nakatani et al., 2021). Horizontal dashed lines indicate that the next duplication events in the branch are not shown here. Modified from Aase-Remedios et al. (2020).
	FIGURE 5. Comparison of the somitic Mef2c mRNA expression between zebrafish, Xenopus, chick, and mouse. The Mef2c expression is conserved in vertebrate somites. The staining is intense in intersomitic region corresponding to the syndetome where the tenocytes differentiate (schematic on the top right corner). In chick, the staining is reduced to muscle-associated tissue. The Mef2c expression is compared with both Scleraxis (syndetome marker) and Myod1, Myf6, or Myogenin (myotome markers). The somitic blocks are indicated by curved lines and the intersomitic regions by short lines. For zebrafish, the Mef2ca expression at 24 and 48 hpf (hours post fertilization). The probe is indicated in each image. All images are lateral views except the second row for Xenopus where the first three images at the left are dorsal views and the forth image at the right is a front view. Figure is composed of images from ISH database of ZFIN for zebrafish (zfin.org), Geisha for chick (geisha.arizona.edu) and Embrys for mouse (embrys.jp).
	FIGURE 6. Comparison of aorta and posterior cardinal vein formation and their somitic contributions between zebrafish, Xenopus, and chick. The ECs and vSMCs that make up the blood vessels throughout the body have various origins. While ECs are exclusively from the splanchnic or the somitic mesoderm, vSMCs are derived from the neural crest and, from the splanchnic or the somitic mesoderm (Pardanaud et al., 1996; Pouget et al., 2006 and, 2008; Etchevers et al., 2001). The aorta formation has also been the focus of intense research in vertebrates as the adult hematopoietic stem cells are generated from the ventral aortic hemangioblasts. This bipotent progenitors can also differentiate into endothelial cells (Pardanaud et al., 1996; Pardanaud and Dieterlen-Lièvre, 1999; Ciau-Uitz et al., 2010; Ciau-Uitz and Patient, 2016). In zebrafish, the aorta hemangioblasts are the first to migrate from the PLM to the midline, coalesce, and form the single aorta. A distinct population of endothelial cells migrates later from the PLM to the midline to form the posterior cardinal vein. ECs and vSMCs from the somites contribute to the aorta and probably to the posterior cardinal vein maturation. Modified from Kohli et al. (2013) and Hogan and Schulte-Merker (2017). In Xenopus, a single aorta is also made up of migrating hemangioblasts from DLP, whereas a pair of bilateral cardinal veins appears at trunk level. Until now, the somitic contributions to the aorta and bilateral cardinal veins are unknown. Modified from Cleaver and Krieg, (1998), Ciau-Uitz et al. (2000), and Charpentier et al. (2015). In chick, a pair of bilateral aorta is first formed from the lateral plate mesoderm before fusing at the midline and receiving ECs and vSMCs from the somites. The bilateral posterior cardinal veins are formed of ECs from the somites. The endotome remains difficult to characterize in amniotes since it seems that ECs derive from several somitic regions (Wilting et al., 1995; Nimmagadda et al., 2005). Modified from Sato, (2013) and Jaffredo et al. (2013). In red, lateral plate mesoderm derived cells. In blue, somite-derived cells. In purple, unknown origin. DLP, dorsal lateral plate mesoderm; DM, dermomyotome; ECs endothelial cells; HSCs, hematopoietic stem cells; LMP, lateral plate mesoderm; PLM, posterior lateral plate mesoderm; vSMCs, vascular smooth muscle cells.
	FIGURE 7. Main functions of BMP, FGF, Wnt, and Shh signalings during somite compartmentalization in anamniotes (A) and amniotes (B). Somite compartmentalization depends on signals expressed by surrounding tissues. Shh is expressed by notochord (NC) and floor plate, Wnt by surface ectoderm (SE) and dorsal neural tube (NT) and BMP4 by lateral plate mesoderm (LPM). Most of the functions fulfilled by the signaling molecules seem to be conserved between anamniotes (A) and amniotes (B). However, it seems that Fgf and to a lesser extent Wnt may play an early role in the formation of primitive myotome only in anamniotes (A). Arrows, promoting effect; T-shaped line, inhibitory effect.
	FIGURE 8. (A) Summary of the main changes during the evolutionary history of somites compartmentalization. The last common ancestor of bilaterians, Urbilateria, possesses neither somites nor notochord, but probably transverse muscles and a medial mesodermal tissue according to the axochord hypothesis (Brunnet al, 2015; Yasuoka, 2020). Satellite-like cells and cartilage-like cells are also probably already present in Urbilateria. Regarding the transcription factors expressed in vertebrate somites, results from Drosophila and Xenopus suggest that Mef2 and Twist could act upstream of muscle identity genes in Urbilateria. The notochord and the somites appear in chordates. The somite is made up of the primitive myotome and probably multipotent progenitors which give rise to satellite cells and muscle-associated tissues ventrally and dorsally. The existence of sclerotome-like cells in cephalochordates suggests that the somitic progenitors can already give rise to specialized connective tissue cells. In vertebrate, the somites compartmentalize mainly into the myotome, the dermomyotome, and the sclerotome. In gnathostome vertebrates, the three populations of slow, lateral fast, and medial fast muscle fibers has been characterized. The genome possesses both Scleraxis and Tcf15 genes, but also four MRFs and four Mef2 genes. The non-conservation of Mef2 function in the paraxial mesoderm and the changes in compartmentalization mode between zebrafish and Xenopus raise the question of the origin of these variations. (B) Evolution of somite compartmentalization based on axochord hypothesis (Brunet et al., 2015; Yasuoka, 2020). The axochord hypothesis (the axochord in annelids and the notochord in chordate are homologs) proposes that the notochord evolves from a medial mesodermal tissue present in Urbilateria, the last common ancestor of all bilaterians, and suggests that transverse muscles attached to it, could give rise to the primitive myotome in ancestral chordates. The origin of MSCs in Urbilateria is unknown. Proto-MSCs probably already exist in last chordate ancestor. The transition from ancestral chordates to vertebrates allowed MSCs to give rise to all new somite structures, i.e., the dermomyotome, its hypaxial region, and the sclerotome. The transition from anamniote to amniote vertebrates is characterized by expansion of the MSCs domain at the expense of the primitive myotome. The chordate dorso-ventral axis is inverted compared with Urbilateria. Anamniote vertebrate is used in Figure 8B as the somite organization of the extant anamniote vertebrates are considered to be closed to the primitive one. VM, ventro-medial mesodermal tissue; TM, transverse muscle; M, medial somite region; L, lateral somite region.
	FIGURE 9. The signaling pathways involved in MSCs and primitive myotome formation in Xenopus. In anamniotes and particularly in Xenopus, the somite development is characterized by the early and massive myotome formation, and the delayed sclerotome development. The construction of primitive myotome is so early specified that it is interconnected to the dorso-mesoderm induction and the paraxial mesoderm specification. The signaling pathways like Fgf, Wnt and Nodal, involved in the dorso-mesoderm induction and in the paraxial mesoderm specification, also quickly trigger myogenic program leading to the primitive myotome formation (Jones et al., 1995; Wylie et al., 1996; Joseph and Melton, 1997; Fisher et al., 2002; Dorey and Amaya, 2010). In contrary, the amniote myotome formation takes place later after somitogenesis and the same signaling pathways involved earlier in the mesoderm induction and in the paraxial mesoderm specification did not induced myogenic program at the same time (Alev et al., 2013; Kiecker et al., 2016). In Xenopus, Fgf and Wnt play a key role in gene expression of the dorso-lateral marginal zone. This region can be considered as the presumptive paraxial mesoderm since it will give rise to somites later. Both Fgf and Wnt also contribute to the expression of Myf5 and Myod1 during the medial myogenic wave in Xenopus. Fgf has also been identified as the main inducer of the lateral myogenic wave which occurs later. In the beginning of neurulation, while the MSCs appear at the LSF, sonic hedgehog (Shh) secreted from notochord favors the myotome formation. BMP4 acts during neurulation to favor satellite cells lineage. Since the satellite cells are not already present at this stage, BMP4 would rather promote the MSCs and/or dermomyotome formation (Daughters et al., 2011).

References [+] :

Aase-Remedios, More Than One-to-Four via 2R: Evidence of an Independent Amphioxus Expansion and Two-Gene Ancestral Vertebrate State for MyoD-Related Myogenic Regulatory Factors (MRFs). 2020, Pubmed