Functional redundancy of the three insulin receptors of cockroaches

Gene duplication is a fundamental evolutionary process which provides opportunities to acquire new gene functions. In the case of the insulin receptors (InRs) in cockroaches and close-related insects, two successive duplications determined the occurrence of three InR genes: InR2, InR1 and InR3, the...

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Authors: Pujal, David, Escudero Ruíz, Jorge, Cabrera, Pol, Bos, Laura, Vargas-Chávez, Carlos, Fernández García, Rosa María, Bellés, Xavier, Maestro, José L.
Format: article
Status:Published version
Publication Date:2024
Country:España
Institution:Consejo Superior de Investigaciones Científicas (CSIC)
Repository:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/373078
Online Access:http://hdl.handle.net/10261/373078
https://api.elsevier.com/content/abstract/scopus_id/85199344604
Access Level:Open access
Keyword:Subfunctionalization
Cockroach
Evolution
Gene duplication
Insulin receptor
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dc.title.none.fl_str_mv Functional redundancy of the three insulin receptors of cockroaches
title Functional redundancy of the three insulin receptors of cockroaches
spellingShingle Functional redundancy of the three insulin receptors of cockroaches
Pujal, David
Subfunctionalization
Cockroach
Evolution
Gene duplication
Insulin receptor
title_short Functional redundancy of the three insulin receptors of cockroaches
title_full Functional redundancy of the three insulin receptors of cockroaches
title_fullStr Functional redundancy of the three insulin receptors of cockroaches
title_full_unstemmed Functional redundancy of the three insulin receptors of cockroaches
title_sort Functional redundancy of the three insulin receptors of cockroaches
dc.creator.none.fl_str_mv Pujal, David
Escudero Ruíz, Jorge
Cabrera, Pol
Bos, Laura
Vargas-Chávez, Carlos
Fernández García, Rosa María
Bellés, Xavier
Maestro, José L.
author Pujal, David
author_facet Pujal, David
Escudero Ruíz, Jorge
Cabrera, Pol
Bos, Laura
Vargas-Chávez, Carlos
Fernández García, Rosa María
Bellés, Xavier
Maestro, José L.
author_role author
author2 Escudero Ruíz, Jorge
Cabrera, Pol
Bos, Laura
Vargas-Chávez, Carlos
Fernández García, Rosa María
Bellés, Xavier
Maestro, José L.
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
European Commission
Agència de Gestió d'Ajuts Universitaris i de Recerca
Generalitat de Catalunya
Ministerio de Ciencia e Innovación (España)
Maestro, José Luis [0000-0001-6117-0458]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Subfunctionalization
Cockroach
Evolution
Gene duplication
Insulin receptor
topic Subfunctionalization
Cockroach
Evolution
Gene duplication
Insulin receptor
description Gene duplication is a fundamental evolutionary process which provides opportunities to acquire new gene functions. In the case of the insulin receptors (InRs) in cockroaches and close-related insects, two successive duplications determined the occurrence of three InR genes: InR2, InR1 and InR3, the last two forming a sister cluster to InR2. The biological role of each of the gene duplicates and whether they resulted from neofunctionalization or subfunctionalization is still unclear. The analysis of the sequences from different lineages did not detect positive selection as driving the divergence of InR1 and InR3, discarding neofunctionalization, and suggesting that there is no functional divergence between both gene copies. Using the cockroach Blattella germanica as a model, we have determined that BgInR2 is the gene with the highest expression levels in all the tissues analyzed, both in adult females and males, as well as in nymphs and embryos. BgInR3 is second in expression levels while BgInR1 is expressed at lower levels and only in some tissues. The selective depletion by RNAi of each of the three InRs, analyzed in terms of phenotype and fat body transcriptomic profiles, resulted in essentially redundant effects, with a magnitude approximately proportional to the level of expression of the respective InR. Therefore, the results indicate that the InR duplicates likely experienced a subfunctionalization process, by which the three InRs maintained similar functions but contributing to those functions proportionally to their expression levels.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
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dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/373078
https://api.elsevier.com/content/abstract/scopus_id/85199344604
url http://hdl.handle.net/10261/373078
https://api.elsevier.com/content/abstract/scopus_id/85199344604
dc.language.none.fl_str_mv Inglés
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The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.ibmb.2024.104161
https://doi.org/10.1016/j.ibmb.2024.104161
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dc.publisher.none.fl_str_mv Elsevier
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spelling Functional redundancy of the three insulin receptors of cockroachesPujal, DavidEscudero Ruíz, JorgeCabrera, PolBos, LauraVargas-Chávez, CarlosFernández García, Rosa MaríaBellés, XavierMaestro, José L.SubfunctionalizationCockroachEvolutionGene duplicationInsulin receptorGene duplication is a fundamental evolutionary process which provides opportunities to acquire new gene functions. In the case of the insulin receptors (InRs) in cockroaches and close-related insects, two successive duplications determined the occurrence of three InR genes: InR2, InR1 and InR3, the last two forming a sister cluster to InR2. The biological role of each of the gene duplicates and whether they resulted from neofunctionalization or subfunctionalization is still unclear. The analysis of the sequences from different lineages did not detect positive selection as driving the divergence of InR1 and InR3, discarding neofunctionalization, and suggesting that there is no functional divergence between both gene copies. Using the cockroach Blattella germanica as a model, we have determined that BgInR2 is the gene with the highest expression levels in all the tissues analyzed, both in adult females and males, as well as in nymphs and embryos. BgInR3 is second in expression levels while BgInR1 is expressed at lower levels and only in some tissues. The selective depletion by RNAi of each of the three InRs, analyzed in terms of phenotype and fat body transcriptomic profiles, resulted in essentially redundant effects, with a magnitude approximately proportional to the level of expression of the respective InR. Therefore, the results indicate that the InR duplicates likely experienced a subfunctionalization process, by which the three InRs maintained similar functions but contributing to those functions proportionally to their expression levels.The work was supported by the grants TED2021-130489B–I00 funded by MICIU/AEI/10.13039/501100011033 and European Union NextGenerationEU/PRTR; PID2019-104483 GB-I00 funded by MCIN/AEI/10.13039/501100011033; and AGAUR 2021-SGR00419 funded by the Departament de Recerca i Universitats de la Generalitat de Catalunya to JLM and XB. RF acknowledges support from the following sources of funding: Ramón y Cajal fellowship (grant agreement no. RYC2017-22492 funded by MCIN/AEI/10.13039/501100011033 and ESF ‘Investing in your future’), the Agencia Estatal de Investigación (project PID2019-108824 GA-I00 funded by MCIN/AEI/10.13039/501100011033) and the Departament de Recerca i Universitats de la Generalitat de Catalunya (AGAUR 2021-SGR00420).Peer reviewedElsevierMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)European CommissionAgència de Gestió d'Ajuts Universitaris i de RecercaGeneralitat de CatalunyaMinisterio de Ciencia e Innovación (España)Maestro, José Luis [0000-0001-6117-0458]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/373078https://api.elsevier.com/content/abstract/scopus_id/85199344604reponame: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#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-108824GA-I00info:eu-repo/grantAgreement/AEI//TED2021-130489B–I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-104483GB-I00info:eu-repo/grantAgreement/AEI//RYC2017-22492The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.ibmb.2024.104161https://doi.org/10.1016/j.ibmb.2024.104161Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3730782026-05-22T06:33:51Z
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