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The Lingula genome provides insights into brachiopod evolution and the origin of phosphate biomineralization.

Luo YJ, Takeuchi T, Koyanagi R, Yamada L, Kanda M, Khalturina M, Fujie M, Yamasaki S, Endo K, Satoh N - Nat Commun (2015)

Bottom Line: However, Lingula has independently undergone domain combinations to produce shell matrix collagens with EGF domains and carries lineage-specific shell matrix proteins.Gene family expansion, domain shuffling and co-option of genes appear to be the genomic background of Lingula's unique biomineralization.This Lingula genome provides resources for further studies of lophotrochozoan evolution.

View Article: PubMed Central - PubMed

Affiliation: Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.

ABSTRACT
The evolutionary origins of lingulid brachiopods and their calcium phosphate shells have been obscure. Here we decode the 425-Mb genome of Lingula anatina to gain insights into brachiopod evolution. Comprehensive phylogenomic analyses place Lingula close to molluscs, but distant from annelids. The Lingula gene number has increased to ∼34,000 by extensive expansion of gene families. Although Lingula and vertebrates have superficially similar hard tissue components, our genomic, transcriptomic and proteomic analyses show that Lingula lacks genes involved in bone formation, indicating an independent origin of their phosphate biominerals. Several genes involved in Lingula shell formation are shared by molluscs. However, Lingula has independently undergone domain combinations to produce shell matrix collagens with EGF domains and carries lineage-specific shell matrix proteins. Gene family expansion, domain shuffling and co-option of genes appear to be the genomic background of Lingula's unique biomineralization. This Lingula genome provides resources for further studies of lophotrochozoan evolution.

No MeSH data available.


Genes related to biomineralization expressed during Lingula shell formation.A schematic illustration of genes involved in Lingula biomineralization identified in the present study. Genes are coloured by their known functions in shell or bone formation in molluscs and vertebrates, respectively. Dashed outlines indicate gene families expanded specifically in Lingula. BMPR, bone morphogenetic protein receptor; ECM, extracellular matrix; GAG, glucosaminoglycan; SEVP1, Sushi von Willebrand factor type A, EGF and pentraxin domain-containing protein 1; WVA, von Willebrand factor type A domain containing protein. Proteins with ion-binding domains are labelled with Ca2+, Fe2+ or Cu2+. P and S in white circles indicate phosphate and sulfate groups.
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f7: Genes related to biomineralization expressed during Lingula shell formation.A schematic illustration of genes involved in Lingula biomineralization identified in the present study. Genes are coloured by their known functions in shell or bone formation in molluscs and vertebrates, respectively. Dashed outlines indicate gene families expanded specifically in Lingula. BMPR, bone morphogenetic protein receptor; ECM, extracellular matrix; GAG, glucosaminoglycan; SEVP1, Sushi von Willebrand factor type A, EGF and pentraxin domain-containing protein 1; WVA, von Willebrand factor type A domain containing protein. Proteins with ion-binding domains are labelled with Ca2+, Fe2+ or Cu2+. P and S in white circles indicate phosphate and sulfate groups.

Mentions: In light of the close phylogenetic relationship between Lingula and molluscs, we hypothesized evolutionary scenarios for the primitive mode of biomineralization in common ancestors of brachiopods and molluscs. By comparing chemical and molecular features, we present three possible primitive modes (that is, Ca-phosphate primitive, Ca-carbonate primitive and chitin scaffold hypotheses; Supplementary Fig. 28). Given different chemistry and genetic components of their shells, we argue that the calcification process might be a derived feature in brachiopods and molluscs. Instead, chitin localized in epithelial cells may be the primitive character, predating biomineralization. A chitinous scaffold may provide the organic framework for interactions between extracellular matrix and mineral ions28. In summary, we propose a possible mechanism for Lingula shell formation (Fig. 7). First, the interaction of myosin head-containing CHSs and actin filaments may translate the cytoskeleton organization into an extracellular chitin scaffold. Chitinase in the shell matrix then possibly remodels the chitin scaffold to facilitate the interaction of chitin and chitin-binding proteins. Calcium-binding proteins probably regulate the calcium concentration in the shell matrix and initiate calcium phosphate deposition, together with other structural proteins, such as EGF domain-containing fibrillar collagens and alanine-rich proteins.


The Lingula genome provides insights into brachiopod evolution and the origin of phosphate biomineralization.

Luo YJ, Takeuchi T, Koyanagi R, Yamada L, Kanda M, Khalturina M, Fujie M, Yamasaki S, Endo K, Satoh N - Nat Commun (2015)

Genes related to biomineralization expressed during Lingula shell formation.A schematic illustration of genes involved in Lingula biomineralization identified in the present study. Genes are coloured by their known functions in shell or bone formation in molluscs and vertebrates, respectively. Dashed outlines indicate gene families expanded specifically in Lingula. BMPR, bone morphogenetic protein receptor; ECM, extracellular matrix; GAG, glucosaminoglycan; SEVP1, Sushi von Willebrand factor type A, EGF and pentraxin domain-containing protein 1; WVA, von Willebrand factor type A domain containing protein. Proteins with ion-binding domains are labelled with Ca2+, Fe2+ or Cu2+. P and S in white circles indicate phosphate and sulfate groups.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4595640&req=5

f7: Genes related to biomineralization expressed during Lingula shell formation.A schematic illustration of genes involved in Lingula biomineralization identified in the present study. Genes are coloured by their known functions in shell or bone formation in molluscs and vertebrates, respectively. Dashed outlines indicate gene families expanded specifically in Lingula. BMPR, bone morphogenetic protein receptor; ECM, extracellular matrix; GAG, glucosaminoglycan; SEVP1, Sushi von Willebrand factor type A, EGF and pentraxin domain-containing protein 1; WVA, von Willebrand factor type A domain containing protein. Proteins with ion-binding domains are labelled with Ca2+, Fe2+ or Cu2+. P and S in white circles indicate phosphate and sulfate groups.
Mentions: In light of the close phylogenetic relationship between Lingula and molluscs, we hypothesized evolutionary scenarios for the primitive mode of biomineralization in common ancestors of brachiopods and molluscs. By comparing chemical and molecular features, we present three possible primitive modes (that is, Ca-phosphate primitive, Ca-carbonate primitive and chitin scaffold hypotheses; Supplementary Fig. 28). Given different chemistry and genetic components of their shells, we argue that the calcification process might be a derived feature in brachiopods and molluscs. Instead, chitin localized in epithelial cells may be the primitive character, predating biomineralization. A chitinous scaffold may provide the organic framework for interactions between extracellular matrix and mineral ions28. In summary, we propose a possible mechanism for Lingula shell formation (Fig. 7). First, the interaction of myosin head-containing CHSs and actin filaments may translate the cytoskeleton organization into an extracellular chitin scaffold. Chitinase in the shell matrix then possibly remodels the chitin scaffold to facilitate the interaction of chitin and chitin-binding proteins. Calcium-binding proteins probably regulate the calcium concentration in the shell matrix and initiate calcium phosphate deposition, together with other structural proteins, such as EGF domain-containing fibrillar collagens and alanine-rich proteins.

Bottom Line: However, Lingula has independently undergone domain combinations to produce shell matrix collagens with EGF domains and carries lineage-specific shell matrix proteins.Gene family expansion, domain shuffling and co-option of genes appear to be the genomic background of Lingula's unique biomineralization.This Lingula genome provides resources for further studies of lophotrochozoan evolution.

View Article: PubMed Central - PubMed

Affiliation: Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.

ABSTRACT
The evolutionary origins of lingulid brachiopods and their calcium phosphate shells have been obscure. Here we decode the 425-Mb genome of Lingula anatina to gain insights into brachiopod evolution. Comprehensive phylogenomic analyses place Lingula close to molluscs, but distant from annelids. The Lingula gene number has increased to ∼34,000 by extensive expansion of gene families. Although Lingula and vertebrates have superficially similar hard tissue components, our genomic, transcriptomic and proteomic analyses show that Lingula lacks genes involved in bone formation, indicating an independent origin of their phosphate biominerals. Several genes involved in Lingula shell formation are shared by molluscs. However, Lingula has independently undergone domain combinations to produce shell matrix collagens with EGF domains and carries lineage-specific shell matrix proteins. Gene family expansion, domain shuffling and co-option of genes appear to be the genomic background of Lingula's unique biomineralization. This Lingula genome provides resources for further studies of lophotrochozoan evolution.

No MeSH data available.