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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.


Related in: MedlinePlus

Evolution of the Lingula genome is revealed by comparative genomics of lophotrochozoan gene families.(a) Venn diagram of shared and unique gene families in four metazoans. Gene families were identified by clustering of orthologous groups using OrthoMCL. The number in parentheses shows unique gene families compared among 22 selected metazoan genomes. (b) Gene family history analyses with CAFE. Divergence times were estimated with PhyloBayes using calibration based on published fossil data. Gene families expanded or gained (red), contracted or lost (green). (c) Frequency of pair-wise genetic divergence calculated with synonymous substitution rate (Ks) among all possible paralogous pairs in the Lingula, Lottia and Capitella genomes.
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f2: Evolution of the Lingula genome is revealed by comparative genomics of lophotrochozoan gene families.(a) Venn diagram of shared and unique gene families in four metazoans. Gene families were identified by clustering of orthologous groups using OrthoMCL. The number in parentheses shows unique gene families compared among 22 selected metazoan genomes. (b) Gene family history analyses with CAFE. Divergence times were estimated with PhyloBayes using calibration based on published fossil data. Gene families expanded or gained (red), contracted or lost (green). (c) Frequency of pair-wise genetic divergence calculated with synonymous substitution rate (Ks) among all possible paralogous pairs in the Lingula, Lottia and Capitella genomes.

Mentions: An abundance of Lingula fossils from the Silurian, with morphology very similar to that of extant species, inspired Darwin with the idea of ‘living fossils.' Nevertheless, shells of fossilized and living lingulids show considerable diversity in chemical structure2021. Similarly, soft tissue fossils from the Chengjiang fauna reveal morphological changes among lingulid brachiopods22. Those findings suggest that lingulid brachiopods have been rapidly evolving. On the other hand, protein-coding genes of the coelacanth, another ‘living fossil,' are reported to be evolving significantly more slowly than those of other tetrapods23. Interestingly, we found that Lingula genes associated with basic metabolism, such as ribonucleoprotein complex biogenesis and RNA processing, show the slowest evolutionary rate among lophotrochozoans (Fig. 1j). However, we also found a high degree of changes in the genomic structure and gene families (Supplementary Note 3). The Lingula genome contains a disorganized Hox cluster. It is divided into two regions, and Lox2 and Lox4 are missing (Supplementary Fig. 12). Comparison of gene families shared by amphioxus Branchiostoma floridae24, Capitella and Lottia show that Lingula has 3,525 unique gene families (Fig. 2a). Further analyses show that the Lingula genome contains 7,263 gains and 8,441 losses of gene families. The turnover rate of gene families in Lingula is the highest among bilaterians (Fig. 2b).


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)

Evolution of the Lingula genome is revealed by comparative genomics of lophotrochozoan gene families.(a) Venn diagram of shared and unique gene families in four metazoans. Gene families were identified by clustering of orthologous groups using OrthoMCL. The number in parentheses shows unique gene families compared among 22 selected metazoan genomes. (b) Gene family history analyses with CAFE. Divergence times were estimated with PhyloBayes using calibration based on published fossil data. Gene families expanded or gained (red), contracted or lost (green). (c) Frequency of pair-wise genetic divergence calculated with synonymous substitution rate (Ks) among all possible paralogous pairs in the Lingula, Lottia and Capitella genomes.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Evolution of the Lingula genome is revealed by comparative genomics of lophotrochozoan gene families.(a) Venn diagram of shared and unique gene families in four metazoans. Gene families were identified by clustering of orthologous groups using OrthoMCL. The number in parentheses shows unique gene families compared among 22 selected metazoan genomes. (b) Gene family history analyses with CAFE. Divergence times were estimated with PhyloBayes using calibration based on published fossil data. Gene families expanded or gained (red), contracted or lost (green). (c) Frequency of pair-wise genetic divergence calculated with synonymous substitution rate (Ks) among all possible paralogous pairs in the Lingula, Lottia and Capitella genomes.
Mentions: An abundance of Lingula fossils from the Silurian, with morphology very similar to that of extant species, inspired Darwin with the idea of ‘living fossils.' Nevertheless, shells of fossilized and living lingulids show considerable diversity in chemical structure2021. Similarly, soft tissue fossils from the Chengjiang fauna reveal morphological changes among lingulid brachiopods22. Those findings suggest that lingulid brachiopods have been rapidly evolving. On the other hand, protein-coding genes of the coelacanth, another ‘living fossil,' are reported to be evolving significantly more slowly than those of other tetrapods23. Interestingly, we found that Lingula genes associated with basic metabolism, such as ribonucleoprotein complex biogenesis and RNA processing, show the slowest evolutionary rate among lophotrochozoans (Fig. 1j). However, we also found a high degree of changes in the genomic structure and gene families (Supplementary Note 3). The Lingula genome contains a disorganized Hox cluster. It is divided into two regions, and Lox2 and Lox4 are missing (Supplementary Fig. 12). Comparison of gene families shared by amphioxus Branchiostoma floridae24, Capitella and Lottia show that Lingula has 3,525 unique gene families (Fig. 2a). Further analyses show that the Lingula genome contains 7,263 gains and 8,441 losses of gene families. The turnover rate of gene families in Lingula is the highest among bilaterians (Fig. 2b).

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.


Related in: MedlinePlus