Endochondral bone in an Early Devonian ‘placoderm’ from Mongolia

Brazeau, Martin D.; Giles, Sam; Dearden, Richard P.; Jerve, Anna; Ariunchimeg, Ya.; Zorig, Enkhtaivan; Sansom, Robert S.; Guillerme, Thomas; Castiello, Marco

doi:10.1038/s41559-020-01290-2

Cited by 40 publications

(22 citation statements)

References 41 publications

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“…During ontogeny, most vertebrate skeletons are initially composed predominantly of hyaline cartilage and largely replaced by bone via endochondral ossification (Hall, 1975(Hall, , 2005. In contrast, chondrichthyans, including elasmobranchs (sharks, skates, rays, and relatives) and holocephalans (chimaeroids) do not develop osseous skeletons, having secondarily lost the ability to produce endoskeletal bone (Coates et al, 1998;Dean and Summers, 2006;Ryll et al, 2014;Debiais-Thibaud, 2019;Brazeau et al, 2020). Instead, the chondrichthyan endoskeleton remains primarily composed of hyaline-like cartilage, with elasmobranchs developing a comparatively thin outer layer of cortical mineralization over most of their skeleton during ontogeny (Hall, 2005;Egerbacher et al, 2006;Dean et al, 2009Dean et al, , 2015Seidel et al, 2016Seidel et al, , 2019bAtake et al, 2019;Debiais-Thibaud, 2019).…”

Section: Introductionmentioning

confidence: 99%

Mineralization of the Callorhinchus Vertebral Column (Holocephali; Chondrichthyes)

et al. 2020

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Members of the Chondrichthyes (Elasmobranchii and Holocephali) are distinguished by their largely cartilaginous endoskeletons, which comprise an uncalcified core overlain by a mineralized layer; in the Elasmobranchii (sharks, skates, rays) most of this mineralization takes the form of calcified polygonal tiles known as tesserae. In recent years, these skeletal tissues have been described in ever increasing detail in sharks and rays, but those of Holocephali (chimaeroids) have been less well-studied, with conflicting accounts as to whether or not tesserae are present. During embryonic ontogeny in holocephalans, cervical vertebrae fuse to form a structure called the synarcual. The synarcual mineralizes early and progressively, anteroposteriorly and dorsoventrally, and therefore presents a good skeletal structure in which to observe mineralized tissues in this group. Here, we describe the development and mineralization of the synarcual in an adult and stage 36 elephant shark embryo (Callorhinchus milii). Small, discrete, but irregular blocks of cortical mineralization are present in stage 36, similar to what has been described recently in embryos of other chimaeroid taxa such as Hydrolagus, while in Callorhinchus adults, the blocks of mineralization are more irregular, but remain small. This differs from fossil members of the holocephalan crown group (Edaphodon), as well as from stem group holocephalans (e.g., Symmorida, Helodus, Iniopterygiformes), where tesserae are notably larger than in Callorhinchus and show similarities to elasmobranch tesserae, for example with respect to polygonal shape.

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Section: Introductionmentioning

confidence: 99%

Mineralization of the Callorhinchus Vertebral Column (Holocephali; Chondrichthyes)

et al. 2020

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“…Although previously reported expression of Mgp and Bgp1 in tetrapods was found involved in the regulation of mineralization in skeletal tissues, only Mgp1 displays association with skeletal tissue differentiation in the small-spotted catshark embryo, and its expression pattern is congruent with an ability to inhibit mineralization in the step preceding precipitation of calcium in the cartilaginous matrix. The ability to activate mineralization in skeletal tissues may finally be a specificity of the Bgp1 bony fish copy: either because it evolved after the divergence with cartilaginous fishes or because cartilaginous fishes have secondarily lost bone-associated genetic toolkits as they lost bone tissues (Donoghue et al, 2006;Brazeau et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates

Leurs

Martinand‐Mari²,

Ventéo³

et al. 2021

Front. Genet.

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Matrix Gla protein (Mgp) and bone Gla protein (Bgp) are vitamin-K dependent proteins that bind calcium in their γ-carboxylated versions in mammals. They are recognized as positive (Bgp) or negative (Mgp and Bgp) regulators of biomineralization in a number of tissues, including skeletal tissues of bony vertebrates. The Mgp/Bgp gene family is poorly known in cartilaginous fishes, which precludes the understanding of the evolution of the biomineralization toolkit at the emergence of jawed vertebrates. Here we took advantage of recently released genomic and transcriptomic data in cartilaginous fishes and described the genomic loci and gene expression patterns of the Mgp/Bgp gene family. We identified three genes, Mgp1, Mgp2, and Bgp, in cartilaginous fishes instead of the single previously reported Mgp gene. We describe their genomic loci, resulting in a dynamic evolutionary scenario for this gene family including several events of local (tandem) duplications, but also of translocation events, along jawed vertebrate evolution. We describe the expression patterns of Mgp1, Mgp2, and Bgp in embryonic stages covering organogenesis in the small-spotted catshark Scyliorhinus canicula and present a comparative analysis with Mgp/Bgp family members previously described in bony vertebrates, highlighting ancestral features such as early embryonic, soft tissues, and neuronal expressions, but also derived features of cartilaginous fishes such as expression in fin supporting fibers. Our results support an ancestral function of Mgp in skeletal mineralization and a later derived function of Bgp in skeletal development that may be related to the divergence of bony vertebrates.

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“…The trabecular mineralization pattern in the vertebrate endoskeleton is commonly illustrated by endochondral bone (i.e., bone deposited within a degrading cartilage template), which was long argued to appear first in osteichthyans ( Donoghue and Sansom, 2002 ; Donoghue et al, 2006 ). New fossil data describe endochondral bone with a trabecular mineralization pattern also in placoderm-like fish ( Brazeau et al, 2020 ), suggesting that the trabecular mineralization pattern is present in the endoskeleton of ancestral vertebrates ( Figure 3 ). Given that ostracoderms and placoderms also had mineralized cartilage in their endoskeletons, further work should clarify whether a trabecular mineralization pattern in cartilage was pervasive in these ancestral vertebrates.…”

Section: Developmental Studies Of Chondrichthyan Tesserae Can Shed Light On Mineralization Pattern Evolutionmentioning

confidence: 99%

Mineralized Cartilage and Bone-Like Tissues in Chondrichthyans Offer Potential Insights Into the Evolution and Development of Mineralized Tissues in the Vertebrate Endoskeleton

Atake

Eames

2021

Front. Genet.

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The impregnation of biominerals into the extracellular matrix of living organisms, a process termed biomineralization, gives rise to diverse mineralized (or calcified) tissues in vertebrates. Preservation of mineralized tissues in the fossil record has provided insights into the evolutionary history of vertebrates and their skeletons. However, current understanding of the vertebrate skeleton and of the processes underlying its formation is biased towards biomedical models such as the tetrapods mouse and chick. Chondrichthyans (sharks, skates, rays, and chimaeras) and osteichthyans are the only vertebrate groups with extant (living) representatives that have a mineralized skeleton, but the basal phylogenetic position of chondrichthyans could potentially offer unique insights into skeletal evolution. For example, bone is a vertebrate novelty, but the internal supporting skeleton (endoskeleton) of extant chondrichthyans is commonly described as lacking bone. The molecular and developmental basis for this assertion is yet to be tested. Subperichondral tissues in the endoskeleton of some chondrichthyans display mineralization patterns and histological and molecular features of bone, thereby challenging the notion that extant chondrichthyans lack endoskeletal bone. Additionally, the chondrichthyan endoskeleton demonstrates some unique features and others that are potentially homologous with other vertebrates, including a polygonal mineralization pattern, a trabecular mineralization pattern, and an unconstricted perichordal sheath. Because of the basal phylogenetic position of chondrichthyans among all other extant vertebrates with a mineralized skeleton, developmental and molecular studies of chondrichthyans are critical to flesh out the evolution of vertebrate skeletal tissues, but only a handful of such studies have been carried out to date. This review discusses morphological and molecular features of chondrichthyan endoskeletal tissues and cell types, ultimately emphasizing how comparative embryology and transcriptomics can reveal homology of mineralized skeletal tissues (and their cell types) between chondrichthyans and other vertebrates.

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Endochondral bone in an Early Devonian ‘placoderm’ from Mongolia

Cited by 40 publications

References 41 publications

Mineralization of the Callorhinchus Vertebral Column (Holocephali; Chondrichthyes)

Mineralization of the Callorhinchus Vertebral Column (Holocephali; Chondrichthyes)

Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates

Mineralized Cartilage and Bone-Like Tissues in Chondrichthyans Offer Potential Insights Into the Evolution and Development of Mineralized Tissues in the Vertebrate Endoskeleton

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