Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation

Plant tissues can be enriched in phytonutrients not only by stimulating their biosynthesis but also by providing appropriate sink structures for their sequestering and storage. In the case of carotenoids, they accumulate at high levels in chromoplasts naturally found in flowers and fruit. Chromoplas...

Descripción completa

Detalles Bibliográficos
Autores: Morelli, Luca, Torres-Montilla, Salvador, Glauser, Gaétan, Shanmugabalaji, Venkatasalam, Kessler, Felix, Rodriguez-Concepcion, Manuel
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/335532
Acceso en línea:http://hdl.handle.net/10261/335532
https://api.elsevier.com/content/abstract/scopus_id/85143885583
Access Level:acceso abierto
Palabra clave:Carotenoid
Chloroplast
Chromoplast
Differentiation
Isoprenoid
Plastoglobules
Reactive oxygen species
Vitamins
id ES_47a555b4df8fdd45ffebdc50d2ab7166
oai_identifier_str oai:digital.csic.es:10261/335532
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
title Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
spellingShingle Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
Morelli, Luca
Carotenoid
Chloroplast
Chromoplast
Differentiation
Isoprenoid
Plastoglobules
Reactive oxygen species
Vitamins
title_short Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
title_full Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
title_fullStr Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
title_full_unstemmed Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
title_sort Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation
dc.creator.none.fl_str_mv Morelli, Luca
Torres-Montilla, Salvador
Glauser, Gaétan
Shanmugabalaji, Venkatasalam
Kessler, Felix
Rodriguez-Concepcion, Manuel
author Morelli, Luca
author_facet Morelli, Luca
Torres-Montilla, Salvador
Glauser, Gaétan
Shanmugabalaji, Venkatasalam
Kessler, Felix
Rodriguez-Concepcion, Manuel
author_role author
author2 Torres-Montilla, Salvador
Glauser, Gaétan
Shanmugabalaji, Venkatasalam
Kessler, Felix
Rodriguez-Concepcion, Manuel
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Consejo Superior de Investigaciones Científicas (España)
Generalitat Valenciana
Swiss National Science Foundation
Fundación la Caixa
Ministerio de Educación, Cultura y Deporte (España)
European Molecular Biology Laboratory
Morelli, Luca [0000-0002-9968-0012]
Torres-Montilla, Salvador [0000-0001-9691-0786]
Glauser, Gaétan [0000-0002-0983-8614]
Shanmugabalaji, Venkatasalam [0000-0002-3855-6958]
Kessler, Felix [0000-0001-6409-5043]
Rodríguez-Concepción, Manuel [0000-0002-1280-2305]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Carotenoid
Chloroplast
Chromoplast
Differentiation
Isoprenoid
Plastoglobules
Reactive oxygen species
Vitamins
topic Carotenoid
Chloroplast
Chromoplast
Differentiation
Isoprenoid
Plastoglobules
Reactive oxygen species
Vitamins
description Plant tissues can be enriched in phytonutrients not only by stimulating their biosynthesis but also by providing appropriate sink structures for their sequestering and storage. In the case of carotenoids, they accumulate at high levels in chromoplasts naturally found in flowers and fruit. Chromoplasts can also be artificially differentiated from leaf chloroplasts by boosting carotenoid production with the bacterial protein crtB. Here we used electron and confocal microscopy together with subplastidial fractionation and transcript, protein and metabolite analyses to analyze the structural and biochemical changes occurring in crtB-induced artificial chromoplasts and their impact on the accumulation of health-related isoprenoids. We show that leaf chromoplasts develop plastoglobules (PG) harboring high levels of carotenoids (mainly phytoene and pro-vitamin A β-carotene) but also other nutritionally relevant isoprenoids, such as tocopherols (vitamin E) and phylloquinone (vitamin K1). Further promoting PG proliferation by exposure to intense (high) light resulted in a higher accumulation of these health-related metabolites but also an acceleration of the chloroplast-to-chromoplast conversion. We further show that the production of reactive oxygen species (ROS) stimulates chromoplastogenesis. Our data suggest that carotenoid accumulation and ROS production are not just consequences but promoters of the chromoplast differentiation process.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
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
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/335532
https://api.elsevier.com/content/abstract/scopus_id/85143885583
url http://hdl.handle.net/10261/335532
https://api.elsevier.com/content/abstract/scopus_id/85143885583
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #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/PID2020-115810GB-I00
info:eu-repo/grantAgreement/MECD//FPU16%2F04054
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PCI2021-121941
Morelli, Luca; Torres-Montilla, Salvador; Glauser, Gaétan; Shanmugabalaji, Venkatasalam; Kessler, Felix; Rodríguez-Concepción, Manuel; 2023; Novel insights on the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation [Dataset]; New Phytologist Trust; John Wiley & Sons; https://doi.org/10.1111/nph.18585
https://doi.org/10.1111/nph.18585
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv New Phytologist Trust
John Wiley & Sons
publisher.none.fl_str_mv New Phytologist Trust
John Wiley & Sons
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869407307875483648
spelling Novel insights into the contribution of plastoglobules and reactive oxygen species to chromoplast differentiationMorelli, LucaTorres-Montilla, SalvadorGlauser, GaétanShanmugabalaji, VenkatasalamKessler, FelixRodriguez-Concepcion, ManuelCarotenoidChloroplastChromoplastDifferentiationIsoprenoidPlastoglobulesReactive oxygen speciesVitaminsPlant tissues can be enriched in phytonutrients not only by stimulating their biosynthesis but also by providing appropriate sink structures for their sequestering and storage. In the case of carotenoids, they accumulate at high levels in chromoplasts naturally found in flowers and fruit. Chromoplasts can also be artificially differentiated from leaf chloroplasts by boosting carotenoid production with the bacterial protein crtB. Here we used electron and confocal microscopy together with subplastidial fractionation and transcript, protein and metabolite analyses to analyze the structural and biochemical changes occurring in crtB-induced artificial chromoplasts and their impact on the accumulation of health-related isoprenoids. We show that leaf chromoplasts develop plastoglobules (PG) harboring high levels of carotenoids (mainly phytoene and pro-vitamin A β-carotene) but also other nutritionally relevant isoprenoids, such as tocopherols (vitamin E) and phylloquinone (vitamin K1). Further promoting PG proliferation by exposure to intense (high) light resulted in a higher accumulation of these health-related metabolites but also an acceleration of the chloroplast-to-chromoplast conversion. We further show that the production of reactive oxygen species (ROS) stimulates chromoplastogenesis. Our data suggest that carotenoid accumulation and ROS production are not just consequences but promoters of the chromoplast differentiation process.This work was funded by grants from Spanish MCIN/AEI/10.13039/501100011033 and European NextGeneration EU/PRTR and PRIMA programs to MR-C (PID2020-115810GB-I00 and UToPIQ-PCI2021-121941). MR-C is also supported by CSIC (202040E299) and Generalitat Valenciana (PROMETEU/2021/056). Work at University of Neuchatel was supported by the Swiss National Science Foundation (SNSF) grant 31003A_176191. LM and ST-M received predoctoral fellowships from La Caixa Foundation (INPhINIT program LCF/BQ/IN18/11660004) and MEC (FPU program, FPU16/04054), respectively. LM was also funded by an EMBO short-term fellowship (ASTF 8907) to do part of the work at the University of Neuchatel (Switzerland).Peer reviewedNew Phytologist TrustJohn Wiley & SonsMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Consejo Superior de Investigaciones Científicas (España)Generalitat ValencianaSwiss National Science FoundationFundación la CaixaMinisterio de Educación, Cultura y Deporte (España)European Molecular Biology LaboratoryMorelli, Luca [0000-0002-9968-0012]Torres-Montilla, Salvador [0000-0001-9691-0786]Glauser, Gaétan [0000-0002-0983-8614]Shanmugabalaji, Venkatasalam [0000-0002-3855-6958]Kessler, Felix [0000-0001-6409-5043]Rodríguez-Concepción, Manuel [0000-0002-1280-2305]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/335532https://api.elsevier.com/content/abstract/scopus_id/85143885583reponame: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#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-115810GB-I00info:eu-repo/grantAgreement/MECD//FPU16%2F04054info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PCI2021-121941Morelli, Luca; Torres-Montilla, Salvador; Glauser, Gaétan; Shanmugabalaji, Venkatasalam; Kessler, Felix; Rodríguez-Concepción, Manuel; 2023; Novel insights on the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation [Dataset]; New Phytologist Trust; John Wiley & Sons; https://doi.org/10.1111/nph.18585https://doi.org/10.1111/nph.18585Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3355322026-05-22T06:33:51Z
score 15.81155

Similares en LA Referencia