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  Parallel evolution of nacre building gene sets in molluscs

Jackson, D. J., McDougall, C., Woodcroft, B., Moase, P., Rose, R. A., Kube, M., et al. (2010). Parallel evolution of nacre building gene sets in molluscs. Molecular Biology and Evolution, 27(3), 591-608. doi:10.1093/molbev/msp278.

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Item Permalink: http://hdl.handle.net/11858/00-001M-0000-0010-7BC5-B Version Permalink: http://hdl.handle.net/11858/00-001M-0000-0010-7BC6-9
Genre: Journal Article
Alternative Title : Mol Bio Evol

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 Creators:
Jackson, Daniel J., Author
McDougall, Carmel, Author
Woodcroft, Ben, Author
Moase, Patrick, Author
Rose, Robert A., Author
Kube, Michael1, Author              
Reinhardt, Richard1, Author              
Rokhsar, Daniel S., Author
Montagnani, Caroline, Author
Joubert, Caroline, Author
Piquemal, David, Author
Degnan, Bernard M., Author
Affiliations:
1High Throughput Technologies, Max Planck Institute for Molecular Genetics, Max Planck Society, ou_1433552              

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Free keywords: Biomineralization; Nacre; EST; Evolution; Mollusc; Pearl
 Abstract: The capacity to biomineralize is closely linked to the rapid expansion of animal life during the early Cambrian, with many skeletonized phyla first appearing in the fossil record at this time. The appearance of disparate molluscan forms during this period leaves open the possibility that shells evolved independently and in parallel in at least some groups. To test this proposition and gain insight into the evolution of structural genes that contribute to shell fabrication, we compared genes expressed in nacre (mother-of-pearl) forming cells in the mantle of the bivalve Pinctada maxima and the gastropod Haliotis asinina. Despite both species having highly lustrous nacre, we find extensive differences in these expressed gene sets. Following the removal of housekeeping genes, less than 10% of all gene clusters are shared between these molluscs, with some being conserved biomineralization genes that are also found in deuterostomes. These differences extend to secreted proteins that may localize to the organic shell matrix, with less than 15% of this secretome being shared. Despite these differences, H. asinina and P. maxima both secrete proteins with repetitive low-complexity domains (RLCDs). Pinctada maxima RLCD proteins—for example, the shematrins—are predominated by silk/fibroin-like domains, which are absent from the H. asinina data set. Comparisons of shematrin genes across three species of Pinctada indicate that this gene family has undergone extensive divergent evolution within pearl oysters. We also detect fundamental bivalve–gastropod differences in extracellular matrix proteins involved in mollusc-shell formation. Pinctada maxima expresses a chitin synthase at high levels and several chitin deacetylation genes, whereas only one protein involved in chitin interactions is present in the H. asinina data set, suggesting that the organic matrix on which calcification proceeds differs fundamentally between these species. Large-scale differences in genes expressed in nacre-forming cells of Pinctada and Haliotis are compatible with the hypothesis that gastropod and bivalve nacre is the result of convergent evolution. The expression of novel biomineralizing RLCD proteins in each of these two molluscs and, interestingly, sea urchins suggests that the evolution of such structural proteins has occurred independently multiple times in the Metazoa.

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Language(s): eng - English
 Dates: 2010-03
 Publication Status: Published in print
 Pages: -
 Publishing info: -
 Table of Contents: -
 Rev. Type: -
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Title: Molecular Biology and Evolution
  Alternative Title : Mol Bio Evol
Source Genre: Journal
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Publ. Info: -
Pages: - Volume / Issue: 27 (3) Sequence Number: - Start / End Page: 591 - 608 Identifier: ISSN: 0737-4038