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Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi

BACKGROUND: Helitrons are class-II eukaryotic transposons that transpose via a rolling circle mechanism. Due to their ability to capture and mobilize gene fragments, they play an important role in the evolution of their host genomes. We have used a bioinformatics approach for the identification of h...

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Autores principales: Castanera, Raúl, Pérez, Gúmer, López, Leticia, Sancho, Rubén, Santoyo, Francisco, Alfaro, Manuel, Gabaldón, Toni, Pisabarro, Antonio G, Oguiza, José A, Ramírez, Lucía
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4289320/
https://www.ncbi.nlm.nih.gov/pubmed/25480150
http://dx.doi.org/10.1186/1471-2164-15-1071
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author Castanera, Raúl
Pérez, Gúmer
López, Leticia
Sancho, Rubén
Santoyo, Francisco
Alfaro, Manuel
Gabaldón, Toni
Pisabarro, Antonio G
Oguiza, José A
Ramírez, Lucía
author_facet Castanera, Raúl
Pérez, Gúmer
López, Leticia
Sancho, Rubén
Santoyo, Francisco
Alfaro, Manuel
Gabaldón, Toni
Pisabarro, Antonio G
Oguiza, José A
Ramírez, Lucía
author_sort Castanera, Raúl
collection PubMed
description BACKGROUND: Helitrons are class-II eukaryotic transposons that transpose via a rolling circle mechanism. Due to their ability to capture and mobilize gene fragments, they play an important role in the evolution of their host genomes. We have used a bioinformatics approach for the identification of helitrons in two Pleurotus ostreatus genomes using de novo detection and homology-based searching. We have analyzed the presence of helitron-captured genes as well as the expansion of helitron-specific helicases in fungi and performed a phylogenetic analysis of their conserved domains with other representative eukaryotic species. RESULTS: Our results show the presence of two helitron families in P. ostreatus that disrupt gene colinearity and cause a lack of synteny between their genomes. Both putative autonomous and non-autonomous helitrons were transcriptionally active, and some of them carried highly expressed captured genes of unknown origin and function. In addition, both families contained eukaryotic, bacterial and viral domains within the helitron’s boundaries. A phylogenetic reconstruction of RepHel helicases using the Helitron-like and PIF1-like helicase conserved domains revealed a polyphyletic origin for eukaryotic helitrons. CONCLUSION: P. ostreatus helitrons display features similar to other eukaryotic helitrons and do not tend to capture host genes or gene fragments. The occurrence of genes probably captured from other hosts inside the helitrons boundaries pose the hypothesis that an ancient horizontal transfer mechanism could have taken place. The viral domains found in some of these genes and the polyphyletic origin of RepHel helicases in the eukaryotic kingdom suggests that virus could have played a role in a putative lateral transfer of helitrons within the eukaryotic kingdom. The high similarity of some helitrons, along with the transcriptional activity of its RepHel helicases indicates that these elements are still active in the genome of P. ostreatus. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1071) contains supplementary material, which is available to authorized users.
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spelling pubmed-42893202015-01-11 Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi Castanera, Raúl Pérez, Gúmer López, Leticia Sancho, Rubén Santoyo, Francisco Alfaro, Manuel Gabaldón, Toni Pisabarro, Antonio G Oguiza, José A Ramírez, Lucía BMC Genomics Research Article BACKGROUND: Helitrons are class-II eukaryotic transposons that transpose via a rolling circle mechanism. Due to their ability to capture and mobilize gene fragments, they play an important role in the evolution of their host genomes. We have used a bioinformatics approach for the identification of helitrons in two Pleurotus ostreatus genomes using de novo detection and homology-based searching. We have analyzed the presence of helitron-captured genes as well as the expansion of helitron-specific helicases in fungi and performed a phylogenetic analysis of their conserved domains with other representative eukaryotic species. RESULTS: Our results show the presence of two helitron families in P. ostreatus that disrupt gene colinearity and cause a lack of synteny between their genomes. Both putative autonomous and non-autonomous helitrons were transcriptionally active, and some of them carried highly expressed captured genes of unknown origin and function. In addition, both families contained eukaryotic, bacterial and viral domains within the helitron’s boundaries. A phylogenetic reconstruction of RepHel helicases using the Helitron-like and PIF1-like helicase conserved domains revealed a polyphyletic origin for eukaryotic helitrons. CONCLUSION: P. ostreatus helitrons display features similar to other eukaryotic helitrons and do not tend to capture host genes or gene fragments. The occurrence of genes probably captured from other hosts inside the helitrons boundaries pose the hypothesis that an ancient horizontal transfer mechanism could have taken place. The viral domains found in some of these genes and the polyphyletic origin of RepHel helicases in the eukaryotic kingdom suggests that virus could have played a role in a putative lateral transfer of helitrons within the eukaryotic kingdom. The high similarity of some helitrons, along with the transcriptional activity of its RepHel helicases indicates that these elements are still active in the genome of P. ostreatus. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1071) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-05 /pmc/articles/PMC4289320/ /pubmed/25480150 http://dx.doi.org/10.1186/1471-2164-15-1071 Text en © Castanera et al.; licensee BioMed Central. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Castanera, Raúl
Pérez, Gúmer
López, Leticia
Sancho, Rubén
Santoyo, Francisco
Alfaro, Manuel
Gabaldón, Toni
Pisabarro, Antonio G
Oguiza, José A
Ramírez, Lucía
Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi
title Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi
title_full Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi
title_fullStr Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi
title_full_unstemmed Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi
title_short Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi
title_sort highly expressed captured genes and cross-kingdom domains present in helitrons create novel diversity in pleurotus ostreatus and other fungi
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4289320/
https://www.ncbi.nlm.nih.gov/pubmed/25480150
http://dx.doi.org/10.1186/1471-2164-15-1071
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