Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum
Ecology of insects is as wide as their diversity, which reflects their high capacity of adaptation in most of the environments of our planet. Aphids, with over 4,000 species, have developed a series of adaptations including a high phenotypic plasticity and the ability to feed on the phloem-sap of pl...
| Autores: | ; ; ; ; ; ; ; ; |
|---|---|
| Tipo de documento: | Artículo |
| Fecha de publicación: | 2020 |
| País: | España |
| Institución: | Universitat Politècnica de Catalunya (UPC) |
| Repositorio: | UPCommons. Portal del coneixement obert de la UPC |
| Lenguaje: | Inglés |
| OAI Identifier: | oai:upcommons.upc.edu:2117/189307 |
| Acceso en línea: | https://hdl.handle.net/2117/189307 https://dx.doi.org/10.1093/molbev/msaa110 |
| Nivel de acceso: | Acceso abierto |
| Palabra clave: | Genetics Data sets. Gene duplicates FAIRE-Seq Insect Neofunctionalization Positive selection Phylogenomics Genètica ADN Insectes Gens -- Mapatge Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica |
| _version_ | 1878732585640656896 |
|---|---|
| author | Fernández, Rosa |
| author2 | Marcet Houben, Marina Legeai, Fabrice Richard, Gautier Robin, Stéfanie Wucher, Valentin Pegueroles, Cinta Gabaldon, Toni Tagu, Denis |
| author2_role | author author author author author author author author |
| author_browse | Fernández, Rosa Gabaldon, Toni Legeai, Fabrice Marcet Houben, Marina Pegueroles, Cinta Richard, Gautier Robin, Stéfanie Tagu, Denis Wucher, Valentin |
| author_facet | Fernández, Rosa Marcet Houben, Marina Legeai, Fabrice Richard, Gautier Robin, Stéfanie Wucher, Valentin Pegueroles, Cinta Gabaldon, Toni Tagu, Denis |
| author_role | author |
| collection | UPCommons. Portal del coneixement obert de la UPC |
| description | Ecology of insects is as wide as their diversity, which reflects their high capacity of adaptation in most of the environments of our planet. Aphids, with over 4,000 species, have developed a series of adaptations including a high phenotypic plasticity and the ability to feed on the phloem-sap of plants, which is enriched in sugars derived from photosynthesis. Recent analyses of aphid genomes have indicated a high level of shared ancestral gene duplications that might represent a basis for genetic innovation and broad adaptations. In addition, there is a large number of recent, species-specific gene duplications whose role in adaptation remains poorly understood. Here, we tested whether duplicates specific to the pea aphid Acyrthosiphon pisum are related to genomic innovation by combining comparative genomics, transcriptomics, and chromatin accessibility analyses. Consistent with large levels of neofunctionalization, we found that most of the recent pairs of gene duplicates evolved asymmetrically, showing divergent patterns of positive selection and gene expression. Genes under selection involved a plethora of biological functions, suggesting that neofunctionalization and tissue specificity, among other evolutionary mechanisms, have orchestrated the evolution of recent paralogs in the pea aphid and may have facilitated host-symbiont cooperation. Our comprehensive phylogenomics analysis allowed us to tackle the history of duplicated genes to pave the road towards understanding the role of gene duplication in ecological adaptation. |
| eu_rights_str_mv | openAccess |
| format | article |
| id | ES_45d5f9c1c63b592c0eb4e1e0610a503d |
| institution | Universitat Politècnica de Catalunya (UPC) |
| instname_str | Universitat Politècnica de Catalunya (UPC) |
| language | eng |
| network_acronym_str | ES |
| network_name_str | España |
| oai_identifier_str | oai:upcommons.upc.edu:2117/189307 |
| publishDate | 2020 |
| publishDateSort | 2020 |
| publisher | Oxford University Press (OUP) |
| publisherStr | Oxford University Press (OUP) |
| reponame_str | UPCommons. Portal del coneixement obert de la UPC |
| spelling | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum Fernández, Rosa Marcet Houben, Marina Legeai, Fabrice Richard, Gautier Robin, Stéfanie Wucher, Valentin Pegueroles, Cinta Gabaldon, Toni Tagu, Denis Genetics Data sets. Gene duplicates FAIRE-Seq Insect Neofunctionalization Positive selection Phylogenomics Genètica ADN Insectes Gens -- Mapatge Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica Ecology of insects is as wide as their diversity, which reflects their high capacity of adaptation in most of the environments of our planet. Aphids, with over 4,000 species, have developed a series of adaptations including a high phenotypic plasticity and the ability to feed on the phloem-sap of plants, which is enriched in sugars derived from photosynthesis. Recent analyses of aphid genomes have indicated a high level of shared ancestral gene duplications that might represent a basis for genetic innovation and broad adaptations. In addition, there is a large number of recent, species-specific gene duplications whose role in adaptation remains poorly understood. Here, we tested whether duplicates specific to the pea aphid Acyrthosiphon pisum are related to genomic innovation by combining comparative genomics, transcriptomics, and chromatin accessibility analyses. Consistent with large levels of neofunctionalization, we found that most of the recent pairs of gene duplicates evolved asymmetrically, showing divergent patterns of positive selection and gene expression. Genes under selection involved a plethora of biological functions, suggesting that neofunctionalization and tissue specificity, among other evolutionary mechanisms, have orchestrated the evolution of recent paralogs in the pea aphid and may have facilitated host-symbiont cooperation. Our comprehensive phylogenomics analysis allowed us to tackle the history of duplicated genes to pave the road towards understanding the role of gene duplication in ecological adaptation. RF was funded by a Juan de la Cierva-Incorporación Fellowship (Government of Spain, IJCI-2015-26627) and a Marie Skłodowska-Curie Fellowship (747607). TG acknowledges support from the Spanish Ministry of Economy, Industry, and Competitiveness (MEIC) for the EMBL partnership, and grants ‘Centro de Excelencia Severo Ochoa 2013-2017’ SEV-2012-0208, and BFU2015-67107 co-funded by European Regional Development Fund (ERDF); from the CERCA Programme / Generalitat de Catalunya; from the Catalan Research Agency (AGAUR) SGR857, and grant from the European Union’s Horizon 2020 research and innovation programme under the grant agreement ERC-2016-724173 the Marie Sklodowska-Curie grant agreement No H2020-MSCA-ITN-2014-642095. DT was funded by “Severo Ochoa visiting scientific programme” for a 6 months stay at the Center for Genomic Regulation - Barcelona - to start the project, supported as well by INRA SPE. Dr Roderic Guigo (CRG, Barcelona) is warmly acknowledged for his welcome in his lab.Drs. Akiko Sugio, Julie Jaquiéry, Gaël Le Trionnaire and Jean-Christophe Simon (INRAE, UMR 1349 Igepp, Rennes, France) are acknowledged for access to unpublished data of RNA-Seq.Daktulosphaira vitifoliaedata were provided by the Phylloxera Genome Project (https://bipaa.genouest.org/is/aphidbase/): funding for D. vitifoliaeclone Pcf genomic sequencing was provided by INRA (AIP Bioressources) and BGI Biotech in the frame of i5k initiative. Parts of the transcriptomic resources were obtained within the 1KITE projects (Bernhard Misof, Bonn, Germany). The Acyrthosiphon pisum phylome can be accessed at PhylomeDB 4.0 under phylome number 441. RNA-Seq data are accessible at NCBI, see Table S2 Peer Reviewed Oxford University Press (OUP) https://hdl.handle.net/2117/189307 https://dx.doi.org/10.1093/molbev/msaa110 |
| spellingShingle | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum Fernández, Rosa Genetics Data sets. Gene duplicates FAIRE-Seq Insect Neofunctionalization Positive selection Phylogenomics Genètica ADN Insectes Gens -- Mapatge Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica |
| title | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum |
| title_full | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum |
| title_fullStr | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum |
| title_full_unstemmed | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum |
| title_short | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum |
| title_sort | Selection following gene duplication shapes recent genome evolution in the pea aphid Acyrthosiphon pisum |
| topic | Genetics Data sets. Gene duplicates FAIRE-Seq Insect Neofunctionalization Positive selection Phylogenomics Genètica ADN Insectes Gens -- Mapatge Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica |
| topic_facet | Genetics Data sets. Gene duplicates FAIRE-Seq Insect Neofunctionalization Positive selection Phylogenomics Genètica ADN Insectes Gens -- Mapatge Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica |
| url | https://hdl.handle.net/2117/189307 https://dx.doi.org/10.1093/molbev/msaa110 |