Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes

The conservation of orthologs of most subunits of the origin recognition complex (ORC) has served to propose that the whole complex is common to all eukaryotes. However, various uncertainties have arisen concerning ORC subunit composition in a variety of lineages. Also, it is unclear whether the anc...

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Autores: Ocaña-Pallarès, Eduard, Vergara, Zaida, Desvoyes, Bénédicte, Tejada-Jiménez, Manuel, Romero-Jurado, Ainhoa, Galván, Aurora, Fernández, Emilio, Ruiz-Trillo, Iñaki, Gutiérrez Armenta, Crisanto
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/220472
Acceso en línea:http://hdl.handle.net/10261/220472
Access Level:acceso abierto
Palabra clave:Origin recognition complex (ORC)
DNA replication
Eukaryotic evolution
Centriole
Gene loss
Parasitism
Whole genome duplication
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dc.title.none.fl_str_mv Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
title Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
spellingShingle Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
Ocaña-Pallarès, Eduard
Origin recognition complex (ORC)
DNA replication
Eukaryotic evolution
Centriole
Gene loss
Parasitism
Whole genome duplication
title_short Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
title_full Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
title_fullStr Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
title_full_unstemmed Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
title_sort Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes
dc.creator.none.fl_str_mv Ocaña-Pallarès, Eduard
Vergara, Zaida
Desvoyes, Bénédicte
Tejada-Jiménez, Manuel
Romero-Jurado, Ainhoa
Galván, Aurora
Fernández, Emilio
Ruiz-Trillo, Iñaki
Gutiérrez Armenta, Crisanto
author Ocaña-Pallarès, Eduard
author_facet Ocaña-Pallarès, Eduard
Vergara, Zaida
Desvoyes, Bénédicte
Tejada-Jiménez, Manuel
Romero-Jurado, Ainhoa
Galván, Aurora
Fernández, Emilio
Ruiz-Trillo, Iñaki
Gutiérrez Armenta, Crisanto
author_role author
author2 Vergara, Zaida
Desvoyes, Bénédicte
Tejada-Jiménez, Manuel
Romero-Jurado, Ainhoa
Galván, Aurora
Fernández, Emilio
Ruiz-Trillo, Iñaki
Gutiérrez Armenta, Crisanto
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
European Commission
European Research Council
Banco Santander
Fundación Ramón Areces
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Origin recognition complex (ORC)
DNA replication
Eukaryotic evolution
Centriole
Gene loss
Parasitism
Whole genome duplication
topic Origin recognition complex (ORC)
DNA replication
Eukaryotic evolution
Centriole
Gene loss
Parasitism
Whole genome duplication
description The conservation of orthologs of most subunits of the origin recognition complex (ORC) has served to propose that the whole complex is common to all eukaryotes. However, various uncertainties have arisen concerning ORC subunit composition in a variety of lineages. Also, it is unclear whether the ancestral diversification of ORC in eukaryotes was accompanied by the neofunctionalization of some subunits, for example, role of ORC1 in centriole homeostasis. We have addressed these questions by reconstructing the distribution and evolutionary history of ORC1-5/CDC6 in a taxon-rich eukaryotic data set. First, we identified ORC subunits previously undetected in divergent lineages, which allowed us to propose a series of parsimonious scenarios for the origin of this multiprotein complex. Contrary to previous expectations, we found a global tendency in eukaryotes to increase or decrease the number of subunits as a consequence of genome duplications or streamlining, respectively. Interestingly, parasites show significantly lower number of subunits than free-living eukaryotes, especially those with the lowest genome size and gene content metrics. We also investigated the evolutionary origin of the ORC1 role in centriole homeostasis mediated by the PACT region in human cells. In particular, we tested the consequences of reducing ORC1 levels in the centriole-containing green alga Chlamydomonas reinhardtii. We found that the proportion of centrioles to flagella and nuclei was not dramatically affected. This, together with the PACT region not being significantly more conserved in centriole-bearing eukaryotes, supports the notion that this neofunctionalization of ORC1 would be a recent acquisition rather than an ancestral eukaryotic feature.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
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dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/220472
url http://hdl.handle.net/10261/220472
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
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spelling Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic GenomesOcaña-Pallarès, EduardVergara, ZaidaDesvoyes, BénédicteTejada-Jiménez, ManuelRomero-Jurado, AinhoaGalván, AuroraFernández, EmilioRuiz-Trillo, IñakiGutiérrez Armenta, CrisantoOrigin recognition complex (ORC)DNA replicationEukaryotic evolutionCentrioleGene lossParasitismWhole genome duplicationThe conservation of orthologs of most subunits of the origin recognition complex (ORC) has served to propose that the whole complex is common to all eukaryotes. However, various uncertainties have arisen concerning ORC subunit composition in a variety of lineages. Also, it is unclear whether the ancestral diversification of ORC in eukaryotes was accompanied by the neofunctionalization of some subunits, for example, role of ORC1 in centriole homeostasis. We have addressed these questions by reconstructing the distribution and evolutionary history of ORC1-5/CDC6 in a taxon-rich eukaryotic data set. First, we identified ORC subunits previously undetected in divergent lineages, which allowed us to propose a series of parsimonious scenarios for the origin of this multiprotein complex. Contrary to previous expectations, we found a global tendency in eukaryotes to increase or decrease the number of subunits as a consequence of genome duplications or streamlining, respectively. Interestingly, parasites show significantly lower number of subunits than free-living eukaryotes, especially those with the lowest genome size and gene content metrics. We also investigated the evolutionary origin of the ORC1 role in centriole homeostasis mediated by the PACT region in human cells. In particular, we tested the consequences of reducing ORC1 levels in the centriole-containing green alga Chlamydomonas reinhardtii. We found that the proportion of centrioles to flagella and nuclei was not dramatically affected. This, together with the PACT region not being significantly more conserved in centriole-bearing eukaryotes, supports the notion that this neofunctionalization of ORC1 would be a recent acquisition rather than an ancestral eukaryotic feature.E.O.-P. was supported by a predoctoral FPI grant from Ministerio de Economía y Empresa (MINECO). Research in our laboratories was supported by grants BIO2017-92329-EXP, RTI2018-094793-B-I00 (MINECO, Ministerio de Ciencia e Innovación, Fondo Europeo de Desarrollo Regional [FEDER]), and ERC-2018-AdG_833617 (European Union [EU]) to C.G., grant BFU2017-90114-P (MINECO, FEDER) to I.R.-T., and grants BFU2015-70649-P (MINECO) and U.E.INTERREG VA POCTEP-055_ALGARED_PLUS5_E (EU) to E.F., and by institutional grants from Banco de Santander and Fundacion Ramon Areces to the CBMSO.Oxford University PressMinisterio de Economía y Competitividad (España)Ministerio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)European CommissionEuropean Research CouncilBanco SantanderFundación Ramón ArecesConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2020202020202020info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/220472reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BIO2017-92329-EXPBIO2017-92329-EXP/AEI/10.13039/501100011033info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-094793-B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BFU2017-90114-PBFU2017-90114-P/AEI/10.13039/501100011033info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2015-70649-Pinfo:eu-repo/grantAgreement/EC/H2020/833617RTI2018-094793-B-I00/AEI/10.13039/501100011033http://dx.doi.org/10.1093/gbe/evaa011Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2204722026-05-22T06:33:51Z
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