A rapidly evolving secretome builds and patterns a sea shell

Jackson, Daniel J., McDougall, Carmel, Green, Kathryn, Simpson, Fiona, Worheide, Gert and Degnan, Bernard M. (2006) A rapidly evolving secretome builds and patterns a sea shell. BMC Biology, 4 40: 40-49.


Author Jackson, Daniel J.
McDougall, Carmel
Green, Kathryn
Simpson, Fiona
Worheide, Gert
Degnan, Bernard M.
Title A rapidly evolving secretome builds and patterns a sea shell
Journal name BMC Biology   Check publisher's open access policy
ISSN 1741-7007
Publication date 2006
Sub-type Article (original research)
DOI 10.1186/1741-7007-4-40
Volume 4
Issue 40
Start page 40
End page 49
Total pages 10
Place of publication United Kingdom
Publisher BioMed Central Ltd.
Collection year 2006
Language eng
Subject C1
270208 Molecular Evolution
630303 Aquaculture
Abstract Background: Instructions to fabricate mineralized structures with distinct nanoscale architectures, such as seashells and coral and vertebrate skeletons, are encoded in the genomes of a wide variety of animals. In mollusks, the mantle is responsible for the extracellular production of the shell, directing the ordered biomineralization of CaCO3 and the deposition of architectural and color patterns. The evolutionary origins of the ability to synthesize calcified structures across various metazoan taxa remain obscure, with only a small number of protein families identified from molluskan shells. The recent sequencing of a wide range of metazoan genomes coupled with the analysis of gene expression in non-model animals has allowed us to investigate the evolution and process of biomineralization in gastropod mollusks. Results: Here we show that over 25% of the genes expressed in the mantle of the vetigastropod Haliotis asinina encode secreted proteins, indicating that hundreds of proteins are likely to be contributing to shell fabrication and patterning. Almost 85% of the secretome encodes novel proteins; remarkably, only 19% of these have identifiable homologues in the full genome of the patellogastropod Lottia scutum. The spatial expression profiles of mantle genes that belong to the secretome is restricted to discrete mantle zones, with each zone responsible for the fabrication of one of the structural layers of the shell. Patterned expression of a subset of genes along the length of the mantle is indicative of roles in shell ornamentation. For example, Has-sometsuke maps precisely to pigmentation patterns in the shell, providing the first case of a gene product to be involved in molluskan shell pigmentation. We also describe the expression of two novel genes involved in nacre (mother of pearl) deposition. Conclusion: The unexpected complexity and evolvability of this secretome and the modular design of the molluskan mantle enables diversification of shell strength and design, and as such must contribute to the variety of adaptive architectures and colors found in mollusk shells. The composition of this novel mantle-specific secretome suggests that there are significant molecular differences in the ways in which gastropods synthesize their shells.
Keyword Elastomeric Biomineralization Protein
Oyster Pinctada-fucata
Lustrin-a
Haliotis-laevigata
Abalone Shell
Polyelectrolyte Sequence
Calcium-binding
Matrix Protein
Nacreous Layer
Expression
Q-Index Code C1

 
Versions
Version Filter Type
Citation counts: TR Web of Science Citation Count  Cited 59 times in Thomson Reuters Web of Science Article | Citations
Scopus Citation Count Cited 63 times in Scopus Article | Citations
Google Scholar Search Google Scholar
Access Statistics: 90 Abstract Views  -  Detailed Statistics
Created: Wed, 15 Aug 2007, 10:24:40 EST