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Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle

INTRODUCTION: Bivalve molluscs have flourished in marine environments, and many species constitute important aquatic resources. Recently, whole genome sequences from two bivalves, the pearl oyster, Pinctada fucata, and the Pacific oyster, Crassostrea gigas, have been decoded, making it possible to c...

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Autores principales: Takeuchi, Takeshi, Koyanagi, Ryo, Gyoja, Fuki, Kanda, Miyuki, Hisata, Kanako, Fujie, Manabu, Goto, Hiroki, Yamasaki, Shinichi, Nagai, Kiyohito, Morino, Yoshiaki, Miyamoto, Hiroshi, Endo, Kazuyoshi, Endo, Hirotoshi, Nagasawa, Hiromichi, Kinoshita, Shigeharu, Asakawa, Shuichi, Watabe, Shugo, Satoh, Noriyuki, Kawashima, Takeshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4759782/
https://www.ncbi.nlm.nih.gov/pubmed/26900483
http://dx.doi.org/10.1186/s40851-016-0039-2
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author Takeuchi, Takeshi
Koyanagi, Ryo
Gyoja, Fuki
Kanda, Miyuki
Hisata, Kanako
Fujie, Manabu
Goto, Hiroki
Yamasaki, Shinichi
Nagai, Kiyohito
Morino, Yoshiaki
Miyamoto, Hiroshi
Endo, Kazuyoshi
Endo, Hirotoshi
Nagasawa, Hiromichi
Kinoshita, Shigeharu
Asakawa, Shuichi
Watabe, Shugo
Satoh, Noriyuki
Kawashima, Takeshi
author_facet Takeuchi, Takeshi
Koyanagi, Ryo
Gyoja, Fuki
Kanda, Miyuki
Hisata, Kanako
Fujie, Manabu
Goto, Hiroki
Yamasaki, Shinichi
Nagai, Kiyohito
Morino, Yoshiaki
Miyamoto, Hiroshi
Endo, Kazuyoshi
Endo, Hirotoshi
Nagasawa, Hiromichi
Kinoshita, Shigeharu
Asakawa, Shuichi
Watabe, Shugo
Satoh, Noriyuki
Kawashima, Takeshi
author_sort Takeuchi, Takeshi
collection PubMed
description INTRODUCTION: Bivalve molluscs have flourished in marine environments, and many species constitute important aquatic resources. Recently, whole genome sequences from two bivalves, the pearl oyster, Pinctada fucata, and the Pacific oyster, Crassostrea gigas, have been decoded, making it possible to compare genomic sequences among molluscs, and to explore general and lineage-specific genetic features and trends in bivalves. In order to improve the quality of sequence data for these purposes, we have updated the entire P. fucata genome assembly. RESULTS: We present a new genome assembly of the pearl oyster, Pinctada fucata (version 2.0). To update the assembly, we conducted additional sequencing, obtaining accumulated sequence data amounting to 193× the P. fucata genome. Sequence redundancy in contigs that was caused by heterozygosity was removed in silico, which significantly improved subsequent scaffolding. Gene model version 2.0 was generated with the aid of manual gene annotations supplied by the P. fucata research community. Comparison of mollusc and other bilaterian genomes shows that gene arrangements of Hox, ParaHox, and Wnt clusters in the P. fucata genome are similar to those of other molluscs. Like the Pacific oyster, P. fucata possesses many genes involved in environmental responses and in immune defense. Phylogenetic analyses of heat shock protein70 and C1q domain-containing protein families indicate that extensive expansion of genes occurred independently in each lineage. Several gene duplication events prior to the split between the pearl oyster and the Pacific oyster are also evident. In addition, a number of tandem duplications of genes that encode shell matrix proteins are also well characterized in the P. fucata genome. CONCLUSIONS: Both the Pinctada and Crassostrea lineages have expanded specific gene families in a lineage-specific manner. Frequent duplication of genes responsible for shell formation in the P. fucata genome explains the diversity of mollusc shell structures. These duplications reveal dynamic genome evolution to forge the complex physiology that enables bivalves to employ a sessile lifestyle in the intertidal zone. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-016-0039-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-47597822016-02-20 Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle Takeuchi, Takeshi Koyanagi, Ryo Gyoja, Fuki Kanda, Miyuki Hisata, Kanako Fujie, Manabu Goto, Hiroki Yamasaki, Shinichi Nagai, Kiyohito Morino, Yoshiaki Miyamoto, Hiroshi Endo, Kazuyoshi Endo, Hirotoshi Nagasawa, Hiromichi Kinoshita, Shigeharu Asakawa, Shuichi Watabe, Shugo Satoh, Noriyuki Kawashima, Takeshi Zoological Lett Research Article INTRODUCTION: Bivalve molluscs have flourished in marine environments, and many species constitute important aquatic resources. Recently, whole genome sequences from two bivalves, the pearl oyster, Pinctada fucata, and the Pacific oyster, Crassostrea gigas, have been decoded, making it possible to compare genomic sequences among molluscs, and to explore general and lineage-specific genetic features and trends in bivalves. In order to improve the quality of sequence data for these purposes, we have updated the entire P. fucata genome assembly. RESULTS: We present a new genome assembly of the pearl oyster, Pinctada fucata (version 2.0). To update the assembly, we conducted additional sequencing, obtaining accumulated sequence data amounting to 193× the P. fucata genome. Sequence redundancy in contigs that was caused by heterozygosity was removed in silico, which significantly improved subsequent scaffolding. Gene model version 2.0 was generated with the aid of manual gene annotations supplied by the P. fucata research community. Comparison of mollusc and other bilaterian genomes shows that gene arrangements of Hox, ParaHox, and Wnt clusters in the P. fucata genome are similar to those of other molluscs. Like the Pacific oyster, P. fucata possesses many genes involved in environmental responses and in immune defense. Phylogenetic analyses of heat shock protein70 and C1q domain-containing protein families indicate that extensive expansion of genes occurred independently in each lineage. Several gene duplication events prior to the split between the pearl oyster and the Pacific oyster are also evident. In addition, a number of tandem duplications of genes that encode shell matrix proteins are also well characterized in the P. fucata genome. CONCLUSIONS: Both the Pinctada and Crassostrea lineages have expanded specific gene families in a lineage-specific manner. Frequent duplication of genes responsible for shell formation in the P. fucata genome explains the diversity of mollusc shell structures. These duplications reveal dynamic genome evolution to forge the complex physiology that enables bivalves to employ a sessile lifestyle in the intertidal zone. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-016-0039-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-02-18 /pmc/articles/PMC4759782/ /pubmed/26900483 http://dx.doi.org/10.1186/s40851-016-0039-2 Text en © Takeuchi et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Takeuchi, Takeshi
Koyanagi, Ryo
Gyoja, Fuki
Kanda, Miyuki
Hisata, Kanako
Fujie, Manabu
Goto, Hiroki
Yamasaki, Shinichi
Nagai, Kiyohito
Morino, Yoshiaki
Miyamoto, Hiroshi
Endo, Kazuyoshi
Endo, Hirotoshi
Nagasawa, Hiromichi
Kinoshita, Shigeharu
Asakawa, Shuichi
Watabe, Shugo
Satoh, Noriyuki
Kawashima, Takeshi
Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle
title Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle
title_full Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle
title_fullStr Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle
title_full_unstemmed Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle
title_short Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle
title_sort bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4759782/
https://www.ncbi.nlm.nih.gov/pubmed/26900483
http://dx.doi.org/10.1186/s40851-016-0039-2
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