A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids

Background: Light, the driving force of photosynthesis, can be harmful when present in excess; therefore, any light harvesting system requires photoprotection. Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection an...

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Autores: Sturm, Sabine, Engelken, Johannes, Gruber, Ansgar, Vugrinec, Sascha, Kroth, Peter G, Adamska, Iwona, Lavaud, Johann
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2013
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/23211
Acceso en línea:http://hdl.handle.net/10230/23211
http://dx.doi.org/10.1186/1471-2148-13-159
Access Level:acceso abierto
Palabra clave:Seqüència d&apos
aminoàcids
Proteïnes -- Metabolisme
Complex plastids
Diatoms
Chloroplast
Gene transfer
Light-harvesting antenna proteins
Red lineage chlorophyll a/b-binding-like proteins
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spelling A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastidsSturm, SabineEngelken, JohannesGruber, AnsgarVugrinec, SaschaKroth, Peter GAdamska, IwonaLavaud, JohannSeqüència d&aposaminoàcidsProteïnes -- MetabolismeComplex plastidsDiatomsChloroplastGene transferLight-harvesting antenna proteinsRed lineage chlorophyll a/b-binding-like proteinsBackground: Light, the driving force of photosynthesis, can be harmful when present in excess; therefore, any light harvesting system requires photoprotection. Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages. Results: Here, we demonstrate that the recently discovered “red lineage chlorophyll a/b-binding-like proteins” (RedCAPs) form a monophyletic family within this protein superfamily. The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin). Expression of a full-length RedCAP:GFP fusion construct in the diatom Phaeodactylum tricornutum confirmed the predicted plastid localisation of RedCAPs. Furthermore, we observed that similarly to the fucoxanthin chlorophyll a/c-binding light-harvesting antenna proteins also RedCAP transcripts in diatoms were regulated in a diurnal way at standard light conditions and strongly repressed at high light intensities./nConclusions: The absence of RedCAPs from the green lineage implies that RedCAPs evolved in the red lineage after separation from the the green lineage. During the evolution of secondary plastids, RedCAP genes therefore must have been transferred from the nucleus of the endocytobiotic alga to the nucleus of the host cell, a process that involved complementation with pre-sequences allowing import of the gene product into the secondary plastid bound by four membranes. Based on light-dependent transcription and on localisation data, we propose that RedCAPs might participate in the light (intensity and quality)-dependent structural or functional reorganisation of the light-harvesting antennae of the photosystems upon dark to light shifts as regularly experienced by diatoms in nature. Remarkably, in plastids of the red lineage as well as in green lineage plastids, the phycobilisome based cyanobacterial light harvesting system has been replaced by light harvesting systems that are based on members of the extended LHC protein superfamily, either for one of the photosystems (PS I of red algae) or for both (diatoms). In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.This work was supported by the Universität Konstanz and by grants of the Deutsche Forschungsgemeinschaft (KR 1661/3 to PGK, AD 92/7-2 to IA, LA 2368/2-1 to JL). JE was supported by a grant (I/82 750) from the Volkswagenstiftung (“Förderungsinitiative Evolutionsbiologie”)BioMed Central201520152013info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/23211http://dx.doi.org/10.1186/1471-2148-13-159reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésBMC Evolutionary Biology. 2013; 13: 159© 2013 Sturm et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.http://creativecommons.org/licenses/by/2.0info:eu-repo/semantics/openAccessoai:recercat.cat:10230/232112026-05-29T05:05:01Z
dc.title.none.fl_str_mv A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
title A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
spellingShingle A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
Sturm, Sabine
Seqüència d&apos
aminoàcids
Proteïnes -- Metabolisme
Complex plastids
Diatoms
Chloroplast
Gene transfer
Light-harvesting antenna proteins
Red lineage chlorophyll a/b-binding-like proteins
title_short A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
title_full A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
title_fullStr A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
title_full_unstemmed A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
title_sort A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
dc.creator.none.fl_str_mv Sturm, Sabine
Engelken, Johannes
Gruber, Ansgar
Vugrinec, Sascha
Kroth, Peter G
Adamska, Iwona
Lavaud, Johann
author Sturm, Sabine
author_facet Sturm, Sabine
Engelken, Johannes
Gruber, Ansgar
Vugrinec, Sascha
Kroth, Peter G
Adamska, Iwona
Lavaud, Johann
author_role author
author2 Engelken, Johannes
Gruber, Ansgar
Vugrinec, Sascha
Kroth, Peter G
Adamska, Iwona
Lavaud, Johann
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Seqüència d&apos
aminoàcids
Proteïnes -- Metabolisme
Complex plastids
Diatoms
Chloroplast
Gene transfer
Light-harvesting antenna proteins
Red lineage chlorophyll a/b-binding-like proteins
topic Seqüència d&apos
aminoàcids
Proteïnes -- Metabolisme
Complex plastids
Diatoms
Chloroplast
Gene transfer
Light-harvesting antenna proteins
Red lineage chlorophyll a/b-binding-like proteins
description Background: Light, the driving force of photosynthesis, can be harmful when present in excess; therefore, any light harvesting system requires photoprotection. Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages. Results: Here, we demonstrate that the recently discovered “red lineage chlorophyll a/b-binding-like proteins” (RedCAPs) form a monophyletic family within this protein superfamily. The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin). Expression of a full-length RedCAP:GFP fusion construct in the diatom Phaeodactylum tricornutum confirmed the predicted plastid localisation of RedCAPs. Furthermore, we observed that similarly to the fucoxanthin chlorophyll a/c-binding light-harvesting antenna proteins also RedCAP transcripts in diatoms were regulated in a diurnal way at standard light conditions and strongly repressed at high light intensities./nConclusions: The absence of RedCAPs from the green lineage implies that RedCAPs evolved in the red lineage after separation from the the green lineage. During the evolution of secondary plastids, RedCAP genes therefore must have been transferred from the nucleus of the endocytobiotic alga to the nucleus of the host cell, a process that involved complementation with pre-sequences allowing import of the gene product into the secondary plastid bound by four membranes. Based on light-dependent transcription and on localisation data, we propose that RedCAPs might participate in the light (intensity and quality)-dependent structural or functional reorganisation of the light-harvesting antennae of the photosystems upon dark to light shifts as regularly experienced by diatoms in nature. Remarkably, in plastids of the red lineage as well as in green lineage plastids, the phycobilisome based cyanobacterial light harvesting system has been replaced by light harvesting systems that are based on members of the extended LHC protein superfamily, either for one of the photosystems (PS I of red algae) or for both (diatoms). In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.
publishDate 2013
dc.date.none.fl_str_mv 2013
2015
2015
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/23211
http://dx.doi.org/10.1186/1471-2148-13-159
url http://hdl.handle.net/10230/23211
http://dx.doi.org/10.1186/1471-2148-13-159
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv BMC Evolutionary Biology. 2013; 13: 159
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/2.0
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/2.0
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
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