Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner

Autores
Almeida, Juliana; da Silva Azevedo, Mariana; Spicher, Livia; Glauser, Gaetán; vom Dorp, Katharina; Guyer, Luzia; Carranza, Andrea del Valle; Asis, Ramón; Pereira de Souza, Amanda; Buckeridge, Marcos; Demarco, Diego; Bres, Cécil; Rothan, Christophe; Pereira Peres, Lazaro Eustáquio; Hörtensteiner, Stephan; Kessler, Felix; Dörmann, Peter; Carrari, Fernando Oscar; Rossi, Magdalena
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Tocopherol, a compound with vitamin E (VTE) activity, is a conserved constituent of the plastidial antioxidant network in photosynthetic organisms. The synthesis of tocopherol involves the condensation of an aromatic head group with an isoprenoid prenyl side chain. The latter, phytyl diphosphate, can be derived from chlorophyll phytol tail recycling, which depends on phytol kinase (VTE5) activity. How plants co-ordinate isoprenoid precursor distribution for supplying biosynthesis of tocopherol and other prenyllipids in different organs is poorly understood. Here, Solanum lycopersicum plants impaired in the expression of two VTE5-like genes identified by phylogenetic analyses, named SlVTE5 and SlFOLK, were characterized. Our data show that while SlFOLK does not affect tocopherol content, the production of this metabolite is >80% dependent on SlVTE5 in tomato, in both leaves and fruits. VTE5 deficiency greatly impacted lipid metabolism, including prenylquinones, carotenoids, and fatty acid phytyl esters. However, the prenyllipid profile greatly differed between source and sink organs, revealing organ-specific metabolic adjustments in tomato. Additionally, VTE5-deficient plants displayed starch accumulation and lower CO2 assimilation in leaves associated with mild yield penalty. Taken together, our results provide valuable insights into the distinct regulation of isoprenoid metabolism in leaves and fruits and also expose the interaction between lipid and carbon metabolism, which results in carbohydrate export blockage in the VTE5-deficient plants, affecting tomato fruit quality.
Fil: Almeida, Juliana. Universidade de Sao Paulo; Brasil
Fil: da Silva Azevedo, Mariana. Universidade de Sao Paulo; Brasil
Fil: Spicher, Livia. Universite de Neuchatel; Suiza
Fil: Glauser, Gaetán. Universite de Neuchatel; Suiza
Fil: vom Dorp, Katharina. Universitat Bonn; Alemania
Fil: Guyer, Luzia. Universitat Zurich; Suiza
Fil: Carranza, Andrea del Valle. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; Argentina
Fil: Asis, Ramón. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; Argentina
Fil: Pereira de Souza, Amanda. Universidade de Sao Paulo; Brasil
Fil: Buckeridge, Marcos. Universidade de Sao Paulo; Brasil
Fil: Demarco, Diego. Universidade de Sao Paulo; Brasil
Fil: Bres, Cécil. Universite de Bordeaux; Francia
Fil: Rothan, Christophe. Universite de Bordeaux; Francia
Fil: Pereira Peres, Lazaro Eustáquio. Universidade de Sao Paulo; Brasil
Fil: Hörtensteiner, Stephan. Universitat Zurich; Suiza
Fil: Kessler, Felix. Universite de Neuchatel; Suiza
Fil: Dörmann, Peter. Universite de Neuchatel; Suiza
Fil: Carrari, Fernando Oscar. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas; Argentina
Fil: Rossi, Magdalena. Universidade de Sao Paulo; Brasil
Materia
Carotenoids
Chlorophyll
Phytol
Phytol Kinase
Prenyllipids
Solanum Lycopersicum
Tocopherol
Tomato
Vitamin E
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/46286
Acceder
id CONICETDig_a9dad64699a9cc6f8896fe2195009beb
oai_identifier_str oai:ri.conicet.gov.ar:11336/46286
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific mannerAlmeida, Julianada Silva Azevedo, MarianaSpicher, LiviaGlauser, Gaetánvom Dorp, KatharinaGuyer, LuziaCarranza, Andrea del ValleAsis, RamónPereira de Souza, AmandaBuckeridge, MarcosDemarco, DiegoBres, CécilRothan, ChristophePereira Peres, Lazaro EustáquioHörtensteiner, StephanKessler, FelixDörmann, PeterCarrari, Fernando OscarRossi, MagdalenaCarotenoidsChlorophyllPhytolPhytol KinasePrenyllipidsSolanum LycopersicumTocopherolTomatoVitamin Ehttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Tocopherol, a compound with vitamin E (VTE) activity, is a conserved constituent of the plastidial antioxidant network in photosynthetic organisms. The synthesis of tocopherol involves the condensation of an aromatic head group with an isoprenoid prenyl side chain. The latter, phytyl diphosphate, can be derived from chlorophyll phytol tail recycling, which depends on phytol kinase (VTE5) activity. How plants co-ordinate isoprenoid precursor distribution for supplying biosynthesis of tocopherol and other prenyllipids in different organs is poorly understood. Here, Solanum lycopersicum plants impaired in the expression of two VTE5-like genes identified by phylogenetic analyses, named SlVTE5 and SlFOLK, were characterized. Our data show that while SlFOLK does not affect tocopherol content, the production of this metabolite is >80% dependent on SlVTE5 in tomato, in both leaves and fruits. VTE5 deficiency greatly impacted lipid metabolism, including prenylquinones, carotenoids, and fatty acid phytyl esters. However, the prenyllipid profile greatly differed between source and sink organs, revealing organ-specific metabolic adjustments in tomato. Additionally, VTE5-deficient plants displayed starch accumulation and lower CO2 assimilation in leaves associated with mild yield penalty. Taken together, our results provide valuable insights into the distinct regulation of isoprenoid metabolism in leaves and fruits and also expose the interaction between lipid and carbon metabolism, which results in carbohydrate export blockage in the VTE5-deficient plants, affecting tomato fruit quality.Fil: Almeida, Juliana. Universidade de Sao Paulo; BrasilFil: da Silva Azevedo, Mariana. Universidade de Sao Paulo; BrasilFil: Spicher, Livia. Universite de Neuchatel; SuizaFil: Glauser, Gaetán. Universite de Neuchatel; SuizaFil: vom Dorp, Katharina. Universitat Bonn; AlemaniaFil: Guyer, Luzia. Universitat Zurich; SuizaFil: Carranza, Andrea del Valle. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; ArgentinaFil: Asis, Ramón. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; ArgentinaFil: Pereira de Souza, Amanda. Universidade de Sao Paulo; BrasilFil: Buckeridge, Marcos. Universidade de Sao Paulo; BrasilFil: Demarco, Diego. Universidade de Sao Paulo; BrasilFil: Bres, Cécil. Universite de Bordeaux; FranciaFil: Rothan, Christophe. Universite de Bordeaux; FranciaFil: Pereira Peres, Lazaro Eustáquio. Universidade de Sao Paulo; BrasilFil: Hörtensteiner, Stephan. Universitat Zurich; SuizaFil: Kessler, Felix. Universite de Neuchatel; SuizaFil: Dörmann, Peter. Universite de Neuchatel; SuizaFil: Carrari, Fernando Oscar. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas; ArgentinaFil: Rossi, Magdalena. Universidade de Sao Paulo; BrasilOxford University Press2015-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/46286Almeida, Juliana; da Silva Azevedo, Mariana; Spicher, Livia; Glauser, Gaetán; vom Dorp, Katharina; et al.; Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner; Oxford University Press; Journal of Experimental Botany; 67; 3; 11-2015; 919-9340022-09571460-2431CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/jxb/article/67/3/919/2893353info:eu-repo/semantics/altIdentifier/doi/10.1093/jxb/erv504info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:08:47Zoai:ri.conicet.gov.ar:11336/46286instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 10:08:47.919CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
title Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
spellingShingle Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
Almeida, Juliana
Carotenoids
Chlorophyll
Phytol
Phytol Kinase
Prenyllipids
Solanum Lycopersicum
Tocopherol
Tomato
Vitamin E
title_short Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
title_full Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
title_fullStr Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
title_full_unstemmed Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
title_sort Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner
dc.creator.none.fl_str_mv Almeida, Juliana
da Silva Azevedo, Mariana
Spicher, Livia
Glauser, Gaetán
vom Dorp, Katharina
Guyer, Luzia
Carranza, Andrea del Valle
Asis, Ramón
Pereira de Souza, Amanda
Buckeridge, Marcos
Demarco, Diego
Bres, Cécil
Rothan, Christophe
Pereira Peres, Lazaro Eustáquio
Hörtensteiner, Stephan
Kessler, Felix
Dörmann, Peter
Carrari, Fernando Oscar
Rossi, Magdalena
author Almeida, Juliana
author_facet Almeida, Juliana
da Silva Azevedo, Mariana
Spicher, Livia
Glauser, Gaetán
vom Dorp, Katharina
Guyer, Luzia
Carranza, Andrea del Valle
Asis, Ramón
Pereira de Souza, Amanda
Buckeridge, Marcos
Demarco, Diego
Bres, Cécil
Rothan, Christophe
Pereira Peres, Lazaro Eustáquio
Hörtensteiner, Stephan
Kessler, Felix
Dörmann, Peter
Carrari, Fernando Oscar
Rossi, Magdalena
author_role author
author2 da Silva Azevedo, Mariana
Spicher, Livia
Glauser, Gaetán
vom Dorp, Katharina
Guyer, Luzia
Carranza, Andrea del Valle
Asis, Ramón
Pereira de Souza, Amanda
Buckeridge, Marcos
Demarco, Diego
Bres, Cécil
Rothan, Christophe
Pereira Peres, Lazaro Eustáquio
Hörtensteiner, Stephan
Kessler, Felix
Dörmann, Peter
Carrari, Fernando Oscar
Rossi, Magdalena
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Carotenoids
Chlorophyll
Phytol
Phytol Kinase
Prenyllipids
Solanum Lycopersicum
Tocopherol
Tomato
Vitamin E
topic Carotenoids
Chlorophyll
Phytol
Phytol Kinase
Prenyllipids
Solanum Lycopersicum
Tocopherol
Tomato
Vitamin E
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Tocopherol, a compound with vitamin E (VTE) activity, is a conserved constituent of the plastidial antioxidant network in photosynthetic organisms. The synthesis of tocopherol involves the condensation of an aromatic head group with an isoprenoid prenyl side chain. The latter, phytyl diphosphate, can be derived from chlorophyll phytol tail recycling, which depends on phytol kinase (VTE5) activity. How plants co-ordinate isoprenoid precursor distribution for supplying biosynthesis of tocopherol and other prenyllipids in different organs is poorly understood. Here, Solanum lycopersicum plants impaired in the expression of two VTE5-like genes identified by phylogenetic analyses, named SlVTE5 and SlFOLK, were characterized. Our data show that while SlFOLK does not affect tocopherol content, the production of this metabolite is >80% dependent on SlVTE5 in tomato, in both leaves and fruits. VTE5 deficiency greatly impacted lipid metabolism, including prenylquinones, carotenoids, and fatty acid phytyl esters. However, the prenyllipid profile greatly differed between source and sink organs, revealing organ-specific metabolic adjustments in tomato. Additionally, VTE5-deficient plants displayed starch accumulation and lower CO2 assimilation in leaves associated with mild yield penalty. Taken together, our results provide valuable insights into the distinct regulation of isoprenoid metabolism in leaves and fruits and also expose the interaction between lipid and carbon metabolism, which results in carbohydrate export blockage in the VTE5-deficient plants, affecting tomato fruit quality.
Fil: Almeida, Juliana. Universidade de Sao Paulo; Brasil
Fil: da Silva Azevedo, Mariana. Universidade de Sao Paulo; Brasil
Fil: Spicher, Livia. Universite de Neuchatel; Suiza
Fil: Glauser, Gaetán. Universite de Neuchatel; Suiza
Fil: vom Dorp, Katharina. Universitat Bonn; Alemania
Fil: Guyer, Luzia. Universitat Zurich; Suiza
Fil: Carranza, Andrea del Valle. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; Argentina
Fil: Asis, Ramón. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; Argentina
Fil: Pereira de Souza, Amanda. Universidade de Sao Paulo; Brasil
Fil: Buckeridge, Marcos. Universidade de Sao Paulo; Brasil
Fil: Demarco, Diego. Universidade de Sao Paulo; Brasil
Fil: Bres, Cécil. Universite de Bordeaux; Francia
Fil: Rothan, Christophe. Universite de Bordeaux; Francia
Fil: Pereira Peres, Lazaro Eustáquio. Universidade de Sao Paulo; Brasil
Fil: Hörtensteiner, Stephan. Universitat Zurich; Suiza
Fil: Kessler, Felix. Universite de Neuchatel; Suiza
Fil: Dörmann, Peter. Universite de Neuchatel; Suiza
Fil: Carrari, Fernando Oscar. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas; Argentina
Fil: Rossi, Magdalena. Universidade de Sao Paulo; Brasil
description Tocopherol, a compound with vitamin E (VTE) activity, is a conserved constituent of the plastidial antioxidant network in photosynthetic organisms. The synthesis of tocopherol involves the condensation of an aromatic head group with an isoprenoid prenyl side chain. The latter, phytyl diphosphate, can be derived from chlorophyll phytol tail recycling, which depends on phytol kinase (VTE5) activity. How plants co-ordinate isoprenoid precursor distribution for supplying biosynthesis of tocopherol and other prenyllipids in different organs is poorly understood. Here, Solanum lycopersicum plants impaired in the expression of two VTE5-like genes identified by phylogenetic analyses, named SlVTE5 and SlFOLK, were characterized. Our data show that while SlFOLK does not affect tocopherol content, the production of this metabolite is >80% dependent on SlVTE5 in tomato, in both leaves and fruits. VTE5 deficiency greatly impacted lipid metabolism, including prenylquinones, carotenoids, and fatty acid phytyl esters. However, the prenyllipid profile greatly differed between source and sink organs, revealing organ-specific metabolic adjustments in tomato. Additionally, VTE5-deficient plants displayed starch accumulation and lower CO2 assimilation in leaves associated with mild yield penalty. Taken together, our results provide valuable insights into the distinct regulation of isoprenoid metabolism in leaves and fruits and also expose the interaction between lipid and carbon metabolism, which results in carbohydrate export blockage in the VTE5-deficient plants, affecting tomato fruit quality.
publishDate 2015
dc.date.none.fl_str_mv 2015-11
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/46286
Almeida, Juliana; da Silva Azevedo, Mariana; Spicher, Livia; Glauser, Gaetán; vom Dorp, Katharina; et al.; Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner; Oxford University Press; Journal of Experimental Botany; 67; 3; 11-2015; 919-934
0022-0957
1460-2431
CONICET Digital
CONICET
url http://hdl.handle.net/11336/46286
identifier_str_mv Almeida, Juliana; da Silva Azevedo, Mariana; Spicher, Livia; Glauser, Gaetán; vom Dorp, Katharina; et al.; Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner; Oxford University Press; Journal of Experimental Botany; 67; 3; 11-2015; 919-934
0022-0957
1460-2431
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/jxb/article/67/3/919/2893353
info:eu-repo/semantics/altIdentifier/doi/10.1093/jxb/erv504
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.13397

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