Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening

Autores
Centeno, Danilo C.; Osorio, Sonia; Nunes Nesi, Adriano; Bertolo, Ana L. F.; Carneiro, Raphael T.; Araújo, Wagner L.; Steinhauser, Marie Caroline; Michalska, Justyna; Rohrmann, Johannes; Geigenberger, Peter; Oliver, Sandra N.; Stitt, Mark; Carrari, Fernando Oscar; Rose, Jocelyn K. C.; Fernie, Alisdair R.
Año de publicación
2011
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Despite the fact that the organic acid content of a fruit is regarded as one of its most commercially important quality traits when assessed by the consumer, relatively little is known concerning the physiological importance of organic acid metabolism for the fruit itself. Here, we evaluate the effect of modifying malate metabolism in a fruit-specific manner, by reduction of the activities of either mitochondrial malate dehydrogenase or fumarase, via targeted antisense approaches in tomato (Solanum lycopersicum). While these genetic perturbations had relatively little effect on the total fruit yield, they had dramatic consequences for fruit metabolism, as well as unanticipated changes in postharvest shelf life and susceptibility to bacterial infection. Detailed characterization suggested that the rate of ripening was essentially unaltered but that lines containing higher malate were characterized by lower levels of transitory starch and a lower soluble sugars content at harvest, whereas those with lower malate contained higher levels of these carbohydrates. Analysis of the activation state of ADP-glucose pyrophosphorylase revealed that it correlated with the accumulation of transitory starch. Taken together with the altered activation state of the plastidial malate dehydrogenase and the modified pigment biosynthesis of the transgenic lines, these results suggest that the phenotypes are due to an altered cellular redox status. The combined data reveal the importance of malate metabolism in tomato fruit metabolism and development and confirm the importance of transitory starch in the determination of agronomic yield in this species.
Fil: Centeno, Danilo C.. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Osorio, Sonia. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Nunes Nesi, Adriano. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Bertolo, Ana L. F.. Cornell University; Estados Unidos
Fil: Carneiro, Raphael T.. Cornell University; Estados Unidos
Fil: Araújo, Wagner L.. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Steinhauser, Marie Caroline. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Michalska, Justyna. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Rohrmann, Johannes. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Geigenberger, Peter. Technische Universitat München; Alemania
Fil: Oliver, Sandra N.. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Stitt, Mark. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Carrari, Fernando Oscar. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rose, Jocelyn K. C.. Cornell University; Estados Unidos
Fil: Fernie, Alisdair R.. Max Planck Institute Of Molecular Plant Physiology; Alemania
Materia
tomato
Solanum
post-harvest
metabolism
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:11336/192404

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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softeningCenteno, Danilo C.Osorio, SoniaNunes Nesi, AdrianoBertolo, Ana L. F.Carneiro, Raphael T.Araújo, Wagner L.Steinhauser, Marie CarolineMichalska, JustynaRohrmann, JohannesGeigenberger, PeterOliver, Sandra N.Stitt, MarkCarrari, Fernando OscarRose, Jocelyn K. C.Fernie, Alisdair R.tomatoSolanumpost-harvestmetabolismhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Despite the fact that the organic acid content of a fruit is regarded as one of its most commercially important quality traits when assessed by the consumer, relatively little is known concerning the physiological importance of organic acid metabolism for the fruit itself. Here, we evaluate the effect of modifying malate metabolism in a fruit-specific manner, by reduction of the activities of either mitochondrial malate dehydrogenase or fumarase, via targeted antisense approaches in tomato (Solanum lycopersicum). While these genetic perturbations had relatively little effect on the total fruit yield, they had dramatic consequences for fruit metabolism, as well as unanticipated changes in postharvest shelf life and susceptibility to bacterial infection. Detailed characterization suggested that the rate of ripening was essentially unaltered but that lines containing higher malate were characterized by lower levels of transitory starch and a lower soluble sugars content at harvest, whereas those with lower malate contained higher levels of these carbohydrates. Analysis of the activation state of ADP-glucose pyrophosphorylase revealed that it correlated with the accumulation of transitory starch. Taken together with the altered activation state of the plastidial malate dehydrogenase and the modified pigment biosynthesis of the transgenic lines, these results suggest that the phenotypes are due to an altered cellular redox status. The combined data reveal the importance of malate metabolism in tomato fruit metabolism and development and confirm the importance of transitory starch in the determination of agronomic yield in this species.Fil: Centeno, Danilo C.. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Osorio, Sonia. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Nunes Nesi, Adriano. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Bertolo, Ana L. F.. Cornell University; Estados UnidosFil: Carneiro, Raphael T.. Cornell University; Estados UnidosFil: Araújo, Wagner L.. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Steinhauser, Marie Caroline. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Michalska, Justyna. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Rohrmann, Johannes. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Geigenberger, Peter. Technische Universitat München; AlemaniaFil: Oliver, Sandra N.. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Stitt, Mark. Max Planck Institute Of Molecular Plant Physiology; AlemaniaFil: Carrari, Fernando Oscar. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Rose, Jocelyn K. C.. Cornell University; Estados UnidosFil: Fernie, Alisdair R.. Max Planck Institute Of Molecular Plant Physiology; AlemaniaAmerican Society of Plant Biologist2011-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/192404Centeno, Danilo C.; Osorio, Sonia; Nunes Nesi, Adriano; Bertolo, Ana L. F.; Carneiro, Raphael T.; et al.; Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening; American Society of Plant Biologist; Plant Cell; 23; 1; 3-2011; 162-1841040-4651CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/plcell/article/23/1/162/6094982info:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.109.072231info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:04:21Zoai:ri.conicet.gov.ar:11336/192404instacron: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 10:04:21.536CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
title Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
spellingShingle Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
Centeno, Danilo C.
tomato
Solanum
post-harvest
metabolism
title_short Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
title_full Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
title_fullStr Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
title_full_unstemmed Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
title_sort Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening
dc.creator.none.fl_str_mv Centeno, Danilo C.
Osorio, Sonia
Nunes Nesi, Adriano
Bertolo, Ana L. F.
Carneiro, Raphael T.
Araújo, Wagner L.
Steinhauser, Marie Caroline
Michalska, Justyna
Rohrmann, Johannes
Geigenberger, Peter
Oliver, Sandra N.
Stitt, Mark
Carrari, Fernando Oscar
Rose, Jocelyn K. C.
Fernie, Alisdair R.
author Centeno, Danilo C.
author_facet Centeno, Danilo C.
Osorio, Sonia
Nunes Nesi, Adriano
Bertolo, Ana L. F.
Carneiro, Raphael T.
Araújo, Wagner L.
Steinhauser, Marie Caroline
Michalska, Justyna
Rohrmann, Johannes
Geigenberger, Peter
Oliver, Sandra N.
Stitt, Mark
Carrari, Fernando Oscar
Rose, Jocelyn K. C.
Fernie, Alisdair R.
author_role author
author2 Osorio, Sonia
Nunes Nesi, Adriano
Bertolo, Ana L. F.
Carneiro, Raphael T.
Araújo, Wagner L.
Steinhauser, Marie Caroline
Michalska, Justyna
Rohrmann, Johannes
Geigenberger, Peter
Oliver, Sandra N.
Stitt, Mark
Carrari, Fernando Oscar
Rose, Jocelyn K. C.
Fernie, Alisdair R.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv tomato
Solanum
post-harvest
metabolism
topic tomato
Solanum
post-harvest
metabolism
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Despite the fact that the organic acid content of a fruit is regarded as one of its most commercially important quality traits when assessed by the consumer, relatively little is known concerning the physiological importance of organic acid metabolism for the fruit itself. Here, we evaluate the effect of modifying malate metabolism in a fruit-specific manner, by reduction of the activities of either mitochondrial malate dehydrogenase or fumarase, via targeted antisense approaches in tomato (Solanum lycopersicum). While these genetic perturbations had relatively little effect on the total fruit yield, they had dramatic consequences for fruit metabolism, as well as unanticipated changes in postharvest shelf life and susceptibility to bacterial infection. Detailed characterization suggested that the rate of ripening was essentially unaltered but that lines containing higher malate were characterized by lower levels of transitory starch and a lower soluble sugars content at harvest, whereas those with lower malate contained higher levels of these carbohydrates. Analysis of the activation state of ADP-glucose pyrophosphorylase revealed that it correlated with the accumulation of transitory starch. Taken together with the altered activation state of the plastidial malate dehydrogenase and the modified pigment biosynthesis of the transgenic lines, these results suggest that the phenotypes are due to an altered cellular redox status. The combined data reveal the importance of malate metabolism in tomato fruit metabolism and development and confirm the importance of transitory starch in the determination of agronomic yield in this species.
Fil: Centeno, Danilo C.. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Osorio, Sonia. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Nunes Nesi, Adriano. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Bertolo, Ana L. F.. Cornell University; Estados Unidos
Fil: Carneiro, Raphael T.. Cornell University; Estados Unidos
Fil: Araújo, Wagner L.. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Steinhauser, Marie Caroline. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Michalska, Justyna. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Rohrmann, Johannes. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Geigenberger, Peter. Technische Universitat München; Alemania
Fil: Oliver, Sandra N.. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Stitt, Mark. Max Planck Institute Of Molecular Plant Physiology; Alemania
Fil: Carrari, Fernando Oscar. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rose, Jocelyn K. C.. Cornell University; Estados Unidos
Fil: Fernie, Alisdair R.. Max Planck Institute Of Molecular Plant Physiology; Alemania
description Despite the fact that the organic acid content of a fruit is regarded as one of its most commercially important quality traits when assessed by the consumer, relatively little is known concerning the physiological importance of organic acid metabolism for the fruit itself. Here, we evaluate the effect of modifying malate metabolism in a fruit-specific manner, by reduction of the activities of either mitochondrial malate dehydrogenase or fumarase, via targeted antisense approaches in tomato (Solanum lycopersicum). While these genetic perturbations had relatively little effect on the total fruit yield, they had dramatic consequences for fruit metabolism, as well as unanticipated changes in postharvest shelf life and susceptibility to bacterial infection. Detailed characterization suggested that the rate of ripening was essentially unaltered but that lines containing higher malate were characterized by lower levels of transitory starch and a lower soluble sugars content at harvest, whereas those with lower malate contained higher levels of these carbohydrates. Analysis of the activation state of ADP-glucose pyrophosphorylase revealed that it correlated with the accumulation of transitory starch. Taken together with the altered activation state of the plastidial malate dehydrogenase and the modified pigment biosynthesis of the transgenic lines, these results suggest that the phenotypes are due to an altered cellular redox status. The combined data reveal the importance of malate metabolism in tomato fruit metabolism and development and confirm the importance of transitory starch in the determination of agronomic yield in this species.
publishDate 2011
dc.date.none.fl_str_mv 2011-03
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/11336/192404
Centeno, Danilo C.; Osorio, Sonia; Nunes Nesi, Adriano; Bertolo, Ana L. F.; Carneiro, Raphael T.; et al.; Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening; American Society of Plant Biologist; Plant Cell; 23; 1; 3-2011; 162-184
1040-4651
CONICET Digital
CONICET
url http://hdl.handle.net/11336/192404
identifier_str_mv Centeno, Danilo C.; Osorio, Sonia; Nunes Nesi, Adriano; Bertolo, Ana L. F.; Carneiro, Raphael T.; et al.; Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening; American Society of Plant Biologist; Plant Cell; 23; 1; 3-2011; 162-184
1040-4651
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/plcell/article/23/1/162/6094982
info:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.109.072231
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
application/pdf
dc.publisher.none.fl_str_mv American Society of Plant Biologist
publisher.none.fl_str_mv American Society of Plant Biologist
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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