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Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks

BACKGROUND: Mollusks display a striking morphological disparity, including, among others, worm-like animals (the aplacophorans), snails and slugs, bivalves, and cephalopods. This phenotypic diversity renders them ideal for studies into animal evolution. Despite being one of the most species-rich phy...

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Autores principales: De Oliveira, A. L., Wollesen, T., Kristof, A., Scherholz, M., Redl, E., Todt, C., Bleidorn, C., Wanninger, A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5103448/
https://www.ncbi.nlm.nih.gov/pubmed/27832738
http://dx.doi.org/10.1186/s12864-016-3080-9
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author De Oliveira, A. L.
Wollesen, T.
Kristof, A.
Scherholz, M.
Redl, E.
Todt, C.
Bleidorn, C.
Wanninger, A.
author_facet De Oliveira, A. L.
Wollesen, T.
Kristof, A.
Scherholz, M.
Redl, E.
Todt, C.
Bleidorn, C.
Wanninger, A.
author_sort De Oliveira, A. L.
collection PubMed
description BACKGROUND: Mollusks display a striking morphological disparity, including, among others, worm-like animals (the aplacophorans), snails and slugs, bivalves, and cephalopods. This phenotypic diversity renders them ideal for studies into animal evolution. Despite being one of the most species-rich phyla, molecular and in silico studies concerning specific key developmental gene families are still scarce, thus hampering deeper insights into the molecular machinery that governs the development and evolution of the various molluscan class-level taxa. RESULTS: Next-generation sequencing was used to retrieve transcriptomes of representatives of seven out of the eight recent class-level taxa of mollusks. Similarity searches, phylogenetic inferences, and a detailed manual curation were used to identify and confirm the orthology of numerous molluscan Hox and ParaHox genes, which resulted in a comprehensive catalog that highlights the evolution of these genes in Mollusca and other metazoans. The identification of a specific molluscan motif in the Hox paralog group 5 and a lophotrochozoan ParaHox motif in the Gsx gene is described. Functional analyses using KEGG and GO tools enabled a detailed description of key developmental genes expressed in important pathways such as Hedgehog, Wnt, and Notch during development of the respective species. The KEGG analysis revealed Wnt8, Wnt11, and Wnt16 as Wnt genes hitherto not reported for mollusks, thereby enlarging the known Wnt complement of the phylum. In addition, novel Hedgehog (Hh)-related genes were identified in the gastropod Lottia cf. kogamogai, demonstrating a more complex gene content in this species than in other mollusks. CONCLUSIONS: The use of de novo transcriptome assembly and well-designed in silico protocols proved to be a robust approach for surveying and mining large sequence data in a wide range of non-model mollusks. The data presented herein constitute only a small fraction of the information retrieved from the analysed molluscan transcriptomes, which can be promptly employed in the identification of novel genes and gene families, phylogenetic inferences, and other studies using molecular tools. As such, our study provides an important framework for understanding some of the underlying molecular mechanisms involved in molluscan body plan diversification and hints towards functions of key developmental genes in molluscan morphogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3080-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-51034482016-11-10 Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks De Oliveira, A. L. Wollesen, T. Kristof, A. Scherholz, M. Redl, E. Todt, C. Bleidorn, C. Wanninger, A. BMC Genomics Research Article BACKGROUND: Mollusks display a striking morphological disparity, including, among others, worm-like animals (the aplacophorans), snails and slugs, bivalves, and cephalopods. This phenotypic diversity renders them ideal for studies into animal evolution. Despite being one of the most species-rich phyla, molecular and in silico studies concerning specific key developmental gene families are still scarce, thus hampering deeper insights into the molecular machinery that governs the development and evolution of the various molluscan class-level taxa. RESULTS: Next-generation sequencing was used to retrieve transcriptomes of representatives of seven out of the eight recent class-level taxa of mollusks. Similarity searches, phylogenetic inferences, and a detailed manual curation were used to identify and confirm the orthology of numerous molluscan Hox and ParaHox genes, which resulted in a comprehensive catalog that highlights the evolution of these genes in Mollusca and other metazoans. The identification of a specific molluscan motif in the Hox paralog group 5 and a lophotrochozoan ParaHox motif in the Gsx gene is described. Functional analyses using KEGG and GO tools enabled a detailed description of key developmental genes expressed in important pathways such as Hedgehog, Wnt, and Notch during development of the respective species. The KEGG analysis revealed Wnt8, Wnt11, and Wnt16 as Wnt genes hitherto not reported for mollusks, thereby enlarging the known Wnt complement of the phylum. In addition, novel Hedgehog (Hh)-related genes were identified in the gastropod Lottia cf. kogamogai, demonstrating a more complex gene content in this species than in other mollusks. CONCLUSIONS: The use of de novo transcriptome assembly and well-designed in silico protocols proved to be a robust approach for surveying and mining large sequence data in a wide range of non-model mollusks. The data presented herein constitute only a small fraction of the information retrieved from the analysed molluscan transcriptomes, which can be promptly employed in the identification of novel genes and gene families, phylogenetic inferences, and other studies using molecular tools. As such, our study provides an important framework for understanding some of the underlying molecular mechanisms involved in molluscan body plan diversification and hints towards functions of key developmental genes in molluscan morphogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3080-9) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-10 /pmc/articles/PMC5103448/ /pubmed/27832738 http://dx.doi.org/10.1186/s12864-016-3080-9 Text en © The Author(s). 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
De Oliveira, A. L.
Wollesen, T.
Kristof, A.
Scherholz, M.
Redl, E.
Todt, C.
Bleidorn, C.
Wanninger, A.
Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks
title Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks
title_full Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks
title_fullStr Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks
title_full_unstemmed Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks
title_short Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks
title_sort comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5103448/
https://www.ncbi.nlm.nih.gov/pubmed/27832738
http://dx.doi.org/10.1186/s12864-016-3080-9
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