Expression Is an Ancestral Feature for Jawed Vertebrates
M elanie Debiais-Thibaud,* ,1 Paul Simion, 1 St ephanie Vent eo, 2 David Mu~ noz, 3 Sylvain Marcellini, 3 Sylvie Mazan, 4 and Tatjana Haitina* ,5
1
ISEM, Universit e de Montpellier, CNRS, IRD, EPHE, Montpellier, France
2
The Neuroscience Institute of Montpellier, Inserm UMR1051, University of Montpellier, Saint Eloi Hospital, Montpellier, France
3
Department of Cell Biology, Faculty of Biological Sciences, Universidad de Concepci on, Concepci on, Chile
4
Sorbonne Universit es, UPMC, CNRS UMR7232 Biologie Int egrative des Organismes Marins, Observatoire Oc eanologique, Banyuls-sur- Mer, France
5
Department of Organismal Biology, Uppsala University, Uppsala, Sweden
*Corresponding authors: E-mails: melanie.debiais-thibaud@umontpellier.fr; tatjana.haitina@ebc.uu.se.
Associate editor: Harmit Malik
Abstract
In order to characterize the molecular bases of mineralizing cell evolution, we targeted type X collagen, a nonfibrillar network forming collagen encoded by the Col10a1 gene. It is involved in the process of endochondral ossification in ray- finned fishes and tetrapods (Osteichthyes), but until now unknown in cartilaginous fishes (Chondrichthyes). We show that holocephalans and elasmobranchs have respectively five and six tandemly duplicated Col10a1 gene copies that display conserved genomic synteny with osteichthyan Col10a1 genes. All Col10a1 genes in the catshark Scyliorhinus canicula are expressed in ameloblasts and/or odontoblasts of teeth and scales, during the stages of extracellular matrix protein secretion and mineralization. Only one duplicate is expressed in the endoskeletal (vertebral) mineralizing tissues. We also show that the expression of type X collagen is present in teeth of two osteichthyans, the zebrafish Danio rerio and the western clawed frog Xenopus tropicalis, indicating an ancestral jawed vertebrate involvement of type X collagen in odontode formation. Our findings push the origin of Col10a1 gene prior to the divergence of osteichthyans and chondrichthyans, and demonstrate its ancestral association with mineralization of both the odontode skeleton and the endoskeleton.
Key words: type X collagen, chondrichthyan, mineralization, teeth, scales.
Introduction
Several factors make type X collagen an excellent candidate to study the evolution of the genetic mechanisms involved in skeletogenesis. First, although type X collagen was first iden- tified more than 30 years ago in chicken long bones (Schmid and Linsenmayer 1985), it has to date only been described in osteichthyans. An immunohistochemical analysis using rabbit anti-Col X antibodies labeled the shark skeleton (Seidel et al.
2017), but the elephant shark and whale shark genome se- quencing projects have failed to identify type X collagen genes (Venkatesh et al. 2014; Read et al. 2017). Second, type X col- lagen is a crucial factor of skeletal mineralization in amniotes, expressed in hypertrophic chondrocytes during endochon- dral ossification (Schmid and Linsenmayer 1985; Jacenko et al. 1993; Mcintosh et al. 1994; Kwan et al. 1997), and con- tributes to the initiation of calcium precipitation in the car- tilaginous extracellular matrix (Kirsch and Wuthier 1994).
Third, studies in nonamniote osteichthyans have revealed that Col10a1 is not limited to cartilage mineralization as it is expressed by osteoblasts in the amphibian Xenopus tropi- calis (Aldea et al. 2013) and the actinopterygians: the medaka Oryzias latipes (Renn and Winkler 2010), the spotted gar
Lepisosteus oculatus, and the zebrafish Danio rerio (Laue et al. 2008; Albertson et al. 2010; Eames et al. 2012). This suggests that in osteichthyans, type X collagen was originally involved in the mineralization of both the cartilage and bone matrix of the endoskeleton. Finally, Col10a1 originated through the two rounds of genome duplication that occurred early in vertebrate evolution, together with its paralogous Col8a1 and Col8a2 genes (Aldea et al. 2013). This suggests that Col10a1 should have been ancestrally present in chon- drichthyans, and raises the question of when it was recruited to the skeletal mineralization processes.
Chondrichthyans or cartilaginous fishes (Elasmobranchii and Holocephalii) have lost perichondral bone and all large dermal bones (Janvier 1996). Chondrichthyan skeletons, how- ever, are characterized by several types of mineralized tissues:
globular mineralized cartilage also found in fossil jawless ver- tebrates (Ørvig 1951; Dean and Summers 2006) and prismatic cartilage which is a chondrichthyan-derived feature (Seidel et al. 2016). A third type of mineralization is only found in elasmobranchs (sharks, rays, and skates), in the fibrous tissue surrounding their notochord, the site of areolar minera- lization (Arratia et al. 2001; Eames et al. 2007; Enault et al.
Article
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