Transcriptional regulation of tocopherol biosynthesis in tomato

Tocopherols, compounds with vitamin E (VTE) activity, are potent lipid-soluble antioxidants synthesized only by photosynthetic organisms. Their biosynthesis requires the condensation of phytyl-diphosphate and homogentisate, derived from the methylerythritol phosphate (MEP) and shikimate pathways (SK), respectively. These metabolic pathways are central in plant chloroplast metabolism and are involved in the biosynthesis of important molecules such as chlorophyll, carotenoids, aromatic amino-acids and prenylquinones. In the last decade, few studies have provided insights into the regulation of VTE biosynthesis and its accumulation. However, the pathway regulatory mechanism/s at mRNA level remains unclear. We have recently identified a collection of tomato genes involved in tocopherol biosynthesis. In this work, by a dedicated qPCR array platform, the transcript levels of 47 genes, including paralogs, were determined in leaves and across fruit development. Expression data were analyzed for correlation with tocopherol profiles by coregulation network and neural clustering approaches. The results showed that tocopherol biosynthesis is controlled both temporally and spatially however total tocopherol content remains constant. These analyses exposed 18 key genes from MEP, SK, phytol recycling and VTE-core pathways highly associated with VTE content in leaves and fruits. Moreover, genomic analyses of promoter regions suggested that the expression of the tocopherol-core pathway genes is trancriptionally coregulated with specific genes of the upstream pathways. Whilst the transcriptional profiles of the precursor pathway genes would suggest an increase in VTE content across fruit development, the data indicate that in the M82 cultivar phytyl diphosphate supply limits tocopherol biosynthesis in later fruit stages. This is in part due to the decreasing transcript levels of geranylgeranyl reductase (GGDR) which restricts the isoprenoid precursor availability. As a proof of concept, by analyzing a collection of Andean landrace tomato genotypes, the role of the pinpointed genes in determining fruit tocopherol content was confirmed. The results uncovered a finely tuned regulation able to shift the precursor pathways controlling substrate influx for VTE biosynthesis and overcoming endogenous competition for intermediates. The whole set of data allowed to propose that 1-deoxy-D-xylulose-5-phosphate synthase and GGDR encoding genes, which determine phytyl-diphosphate availability, together with enzyme encoding genes involved in chlorophyll-derived phytol metabolism appear as the most plausible targets to be engineered aiming to improve tomato fruit nutritional value.

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Main Authors: Quadrana, Leandro Daniel, Almeida de Souza, Juliana Beatriz, Otaiza, Santiago N., Duffy, Tomas, Silva, Junia V. Corrêa da, Godoy, Fabiana de, Asís, Ramón, Bermúdez, Luisa, Fernie, Alisdair R., Carrari, Fernando, Rossi, Magdalena
Format: info:ar-repo/semantics/artículo biblioteca
Language:eng
Published: Springer 2013-02
Subjects:Tomate, Tocoferoles, Antioxidantes, Metabolismo, Vitamina E, Tomatoes, Tocopherols, Antioxidants, Metabolism, Vitamin E,
Online Access:https://link.springer.com/article/10.1007/s11103-012-0001-4
http://hdl.handle.net/20.500.12123/4271
https://doi.org/10.1007/s11103-012-0001-4
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country Argentina
countrycode AR
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access En linea
databasecode dig-inta-ar
tag biblioteca
region America del Sur
libraryname Biblioteca Central del INTA Argentina
language eng
topic Tomate
Tocoferoles
Antioxidantes
Metabolismo
Vitamina E
Tomatoes
Tocopherols
Antioxidants
Metabolism
Vitamin E
Tomate
Tocoferoles
Antioxidantes
Metabolismo
Vitamina E
Tomatoes
Tocopherols
Antioxidants
Metabolism
Vitamin E
spellingShingle Tomate
Tocoferoles
Antioxidantes
Metabolismo
Vitamina E
Tomatoes
Tocopherols
Antioxidants
Metabolism
Vitamin E
Tomate
Tocoferoles
Antioxidantes
Metabolismo
Vitamina E
Tomatoes
Tocopherols
Antioxidants
Metabolism
Vitamin E
Quadrana, Leandro Daniel
Almeida de Souza, Juliana Beatriz
Otaiza, Santiago N.
Duffy, Tomas
Silva, Junia V. Corrêa da
Godoy, Fabiana de
Asís, Ramón
Bermúdez, Luisa
Fernie, Alisdair R.
Carrari, Fernando
Rossi, Magdalena
Transcriptional regulation of tocopherol biosynthesis in tomato
description Tocopherols, compounds with vitamin E (VTE) activity, are potent lipid-soluble antioxidants synthesized only by photosynthetic organisms. Their biosynthesis requires the condensation of phytyl-diphosphate and homogentisate, derived from the methylerythritol phosphate (MEP) and shikimate pathways (SK), respectively. These metabolic pathways are central in plant chloroplast metabolism and are involved in the biosynthesis of important molecules such as chlorophyll, carotenoids, aromatic amino-acids and prenylquinones. In the last decade, few studies have provided insights into the regulation of VTE biosynthesis and its accumulation. However, the pathway regulatory mechanism/s at mRNA level remains unclear. We have recently identified a collection of tomato genes involved in tocopherol biosynthesis. In this work, by a dedicated qPCR array platform, the transcript levels of 47 genes, including paralogs, were determined in leaves and across fruit development. Expression data were analyzed for correlation with tocopherol profiles by coregulation network and neural clustering approaches. The results showed that tocopherol biosynthesis is controlled both temporally and spatially however total tocopherol content remains constant. These analyses exposed 18 key genes from MEP, SK, phytol recycling and VTE-core pathways highly associated with VTE content in leaves and fruits. Moreover, genomic analyses of promoter regions suggested that the expression of the tocopherol-core pathway genes is trancriptionally coregulated with specific genes of the upstream pathways. Whilst the transcriptional profiles of the precursor pathway genes would suggest an increase in VTE content across fruit development, the data indicate that in the M82 cultivar phytyl diphosphate supply limits tocopherol biosynthesis in later fruit stages. This is in part due to the decreasing transcript levels of geranylgeranyl reductase (GGDR) which restricts the isoprenoid precursor availability. As a proof of concept, by analyzing a collection of Andean landrace tomato genotypes, the role of the pinpointed genes in determining fruit tocopherol content was confirmed. The results uncovered a finely tuned regulation able to shift the precursor pathways controlling substrate influx for VTE biosynthesis and overcoming endogenous competition for intermediates. The whole set of data allowed to propose that 1-deoxy-D-xylulose-5-phosphate synthase and GGDR encoding genes, which determine phytyl-diphosphate availability, together with enzyme encoding genes involved in chlorophyll-derived phytol metabolism appear as the most plausible targets to be engineered aiming to improve tomato fruit nutritional value.
format info:ar-repo/semantics/artículo
topic_facet Tomate
Tocoferoles
Antioxidantes
Metabolismo
Vitamina E
Tomatoes
Tocopherols
Antioxidants
Metabolism
Vitamin E
author Quadrana, Leandro Daniel
Almeida de Souza, Juliana Beatriz
Otaiza, Santiago N.
Duffy, Tomas
Silva, Junia V. Corrêa da
Godoy, Fabiana de
Asís, Ramón
Bermúdez, Luisa
Fernie, Alisdair R.
Carrari, Fernando
Rossi, Magdalena
author_facet Quadrana, Leandro Daniel
Almeida de Souza, Juliana Beatriz
Otaiza, Santiago N.
Duffy, Tomas
Silva, Junia V. Corrêa da
Godoy, Fabiana de
Asís, Ramón
Bermúdez, Luisa
Fernie, Alisdair R.
Carrari, Fernando
Rossi, Magdalena
author_sort Quadrana, Leandro Daniel
title Transcriptional regulation of tocopherol biosynthesis in tomato
title_short Transcriptional regulation of tocopherol biosynthesis in tomato
title_full Transcriptional regulation of tocopherol biosynthesis in tomato
title_fullStr Transcriptional regulation of tocopherol biosynthesis in tomato
title_full_unstemmed Transcriptional regulation of tocopherol biosynthesis in tomato
title_sort transcriptional regulation of tocopherol biosynthesis in tomato
publisher Springer
publishDate 2013-02
url https://link.springer.com/article/10.1007/s11103-012-0001-4
http://hdl.handle.net/20.500.12123/4271
https://doi.org/10.1007/s11103-012-0001-4
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spelling oai:localhost:20.500.12123-42712019-06-05T16:56:06Z Transcriptional regulation of tocopherol biosynthesis in tomato Quadrana, Leandro Daniel Almeida de Souza, Juliana Beatriz Otaiza, Santiago N. Duffy, Tomas Silva, Junia V. Corrêa da Godoy, Fabiana de Asís, Ramón Bermúdez, Luisa Fernie, Alisdair R. Carrari, Fernando Rossi, Magdalena Tomate Tocoferoles Antioxidantes Metabolismo Vitamina E Tomatoes Tocopherols Antioxidants Metabolism Vitamin E Tocopherols, compounds with vitamin E (VTE) activity, are potent lipid-soluble antioxidants synthesized only by photosynthetic organisms. Their biosynthesis requires the condensation of phytyl-diphosphate and homogentisate, derived from the methylerythritol phosphate (MEP) and shikimate pathways (SK), respectively. These metabolic pathways are central in plant chloroplast metabolism and are involved in the biosynthesis of important molecules such as chlorophyll, carotenoids, aromatic amino-acids and prenylquinones. In the last decade, few studies have provided insights into the regulation of VTE biosynthesis and its accumulation. However, the pathway regulatory mechanism/s at mRNA level remains unclear. We have recently identified a collection of tomato genes involved in tocopherol biosynthesis. In this work, by a dedicated qPCR array platform, the transcript levels of 47 genes, including paralogs, were determined in leaves and across fruit development. Expression data were analyzed for correlation with tocopherol profiles by coregulation network and neural clustering approaches. The results showed that tocopherol biosynthesis is controlled both temporally and spatially however total tocopherol content remains constant. These analyses exposed 18 key genes from MEP, SK, phytol recycling and VTE-core pathways highly associated with VTE content in leaves and fruits. Moreover, genomic analyses of promoter regions suggested that the expression of the tocopherol-core pathway genes is trancriptionally coregulated with specific genes of the upstream pathways. Whilst the transcriptional profiles of the precursor pathway genes would suggest an increase in VTE content across fruit development, the data indicate that in the M82 cultivar phytyl diphosphate supply limits tocopherol biosynthesis in later fruit stages. This is in part due to the decreasing transcript levels of geranylgeranyl reductase (GGDR) which restricts the isoprenoid precursor availability. As a proof of concept, by analyzing a collection of Andean landrace tomato genotypes, the role of the pinpointed genes in determining fruit tocopherol content was confirmed. The results uncovered a finely tuned regulation able to shift the precursor pathways controlling substrate influx for VTE biosynthesis and overcoming endogenous competition for intermediates. The whole set of data allowed to propose that 1-deoxy-D-xylulose-5-phosphate synthase and GGDR encoding genes, which determine phytyl-diphosphate availability, together with enzyme encoding genes involved in chlorophyll-derived phytol metabolism appear as the most plausible targets to be engineered aiming to improve tomato fruit nutritional value. Instituto de Biotecnología Fil: Quadrana, Leandro Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Almeida de Souza, Juliana Beatriz. Universidade de Sao Paulo. Instituto de Biociências. Departamento de Botânica; Brasil Fil: Otaiza, Santiago N. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas; Argentina Fil: Duffy, Tomás. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Fil: Silva, Junia V. Corrêa da. Universidade de Sao Paulo. Instituto de Biociências. Departamento de Botânica; Brasil Fil: Godoy, Fabiana de. Universidade de Sao Paulo. Instituto de Biociências. Departamento de Botânica; Brasil Fil: Asis, Ramón. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Córdoba. Centro de Investigaciones en Bioquímica Clínica e Inmunología; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas; Argentina Fil: Bermúdez, Luisa. Universidade de Sao Paulo. Instituto de Biociências. Departamento de Botânica; Brasil Fil: Fernie, Alisdair R. Max Planck Institute for Molecular Plant Physiology; Alemania Fil: Carrari, Fernando Oscar. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Fil: Rossi, Magdalena. Universidade de São Pablo. Instituto de Biociências. Departamento de Botânica; Brasil 2019-01-15T17:08:17Z 2019-01-15T17:08:17Z 2013-02 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion https://link.springer.com/article/10.1007/s11103-012-0001-4 http://hdl.handle.net/20.500.12123/4271 0167-4412 1573-5028 https://doi.org/10.1007/s11103-012-0001-4 eng info:eu-repo/semantics/restrictedAccess application/pdf Springer Plant Molecular Biology 81 (3) : 309–325 (February 2013)