A dynamic history of gene duplications and losses characterizes the evolution of the SPARC family in eumetazoans

Abstract

The vertebrates share the ability to produce a skeleton made of mineralized extracellular matrix. However, our understanding of the molecular changes that accompanied their emergence remains scarce. Here, we describe the evolutionary history of the SPARC (secreted protein acidic and rich in cysteine) family, because its vertebrate orthologues are expressed in cartilage, bones and teeth where they have been proposed to bind calcium and act as extracellular collagen chaperones, and because further duplications of specific SPARC members produced the small calcium-binding phosphoproteins (SCPP) family that is crucial for skeletal mineralization to occur. Both phylogeny and synteny conservation analyses reveal that, in the eumetazoan ancestor, a unique ancestral gene duplicated to give rise to SPARC and SPARCB described here for the first time. Independent losses have eliminated one of the two paralogues in cnidarians, protostomes and tetrapods. Hence, only non-tetrapod deuterostomes have conserved both genes. Remarkably, SPARC and SPARCB paralogues are still linked in the amphioxus genome. To shed light on the evolution of the SPARC family members in chordates, we performed a comprehensive analysis of their embryonic expression patterns in amphioxus, tunicates, teleosts, amphibians and mammals. Our results show that in the chordate lineage SPARC and SPARCB family members were recurrently recruited in a variety of unrelated tissues expressing collagen genes. We propose that one of the earliest steps of skeletal evolution involved the co-expression of SPARC paralogues with collagenous proteins.

Molecular cloning and characterization of the matricellular protein Sparc/osteonectin in flatfish, Scophthalmus maximus, and its developmental stage-dependent transcriptional regulation during metamorphosis

“…Therefore, the comparative analysis of turbot Sparc primary sequence with other SPARC proteins from diverse vertebrate species and specifically with its teleost orthologs suggests a strong evolutionary conservation pressure for this protein and also indicates that conservation in function should exist. Although, we did not find any other sparc paralogous in turbot, we have to mention the possibility that turbot genoma might contain two additional sparc paralogues, sparcl1 and sparcb as discovered in other teleost like zebrafish or trout (Bertrand et al, 2013).…”

“…Furthermore, phylogenetic analysis indicated that SPARC/SPARCL1 has been roughly identified in both protostomes and deuterostomes, and a related gene (sparcb) has also been found in tunicates, amphioxus and zebrafish (Bertrand et al, 2013). In Turbot, Sparc clusters together with its vertebrate orthologues and teleost Sparcs were arranged into a single clade.…”

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

“…The classical evolutionary scenario posits that the SPARC-L1 and SPARC paralogues arose from two rounds of vertebrate-specific genome duplications [34, 35]. The gar and coelacanth SPARC-L1 genomic loci were recently shown to contain a SPARC-L2 gene of unknown evolutionary history [5, 36].…”

Amphioxus regeneration: evolutionary and biomedical implications

“…Markers for a number of genes implicated in vertebrate chondrogenesis and osteogenesis including collagens FCol1 and FCol2, SPARC, soxE and runx were expressed specifically in the tips of the regenerating skeletal rods. Amphioxus in fact possesses two SPARC genes, conserved since the eumetazoan ancestor, both of which are expressed in the notochord during embryonic development (Bertrand et al, 2013). Combined with expression data in other chordates, this leads the authors to suggest that co-expression of SPARC-like and Collagen proteins in mesenchymal cells was one of the key steps to skeletal evolution (Bertrand et al, 2013).…”

“…Amphioxus in fact possesses two SPARC genes, conserved since the eumetazoan ancestor, both of which are expressed in the notochord during embryonic development (Bertrand et al, 2013). Combined with expression data in other chordates, this leads the authors to suggest that co-expression of SPARC-like and Collagen proteins in mesenchymal cells was one of the key steps to skeletal evolution (Bertrand et al, 2013). Indeed, a SPARC gene and runx2 are expressed in prospective scleroblast progenitors during scale regeneration in the goldfish, a collagenous dermal skeleton component (Iimura et al, 2012).…”