Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen Limitation
Anthocyanin biosynthesis is regulated by environmental factors (such as light, temperature, and water availability) and nutrient status (such as carbon, nitrogen, and phosphate nutrition). Previous reports show that low nitrogen availability strongly enhances anthocyanin accumulation in non carbon-l...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-05-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2018.00421/full |
| _version_ | 1818247068905373696 |
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| author | Eric Soubeyrand Sophie Colombié Bertrand Beauvoit Zhanwu Dai Stéphanie Cluzet Ghislaine Hilbert Christel Renaud Lilly Maneta-Peyret Martine Dieuaide-Noubhani Jean-Michel Mérillon Yves Gibon Serge Delrot Eric Gomès |
| author_facet | Eric Soubeyrand Sophie Colombié Bertrand Beauvoit Zhanwu Dai Stéphanie Cluzet Ghislaine Hilbert Christel Renaud Lilly Maneta-Peyret Martine Dieuaide-Noubhani Jean-Michel Mérillon Yves Gibon Serge Delrot Eric Gomès |
| author_sort | Eric Soubeyrand |
| collection | DOAJ |
| description | Anthocyanin biosynthesis is regulated by environmental factors (such as light, temperature, and water availability) and nutrient status (such as carbon, nitrogen, and phosphate nutrition). Previous reports show that low nitrogen availability strongly enhances anthocyanin accumulation in non carbon-limited plant organs or cell suspensions. It has been hypothesized that high carbon-to-nitrogen ratio would lead to an energy excess in plant cells, and that an increase in flavonoid pathway metabolic fluxes would act as an “energy escape valve,” helping plant cells to cope with energy and carbon excess. However, this hypothesis has never been tested directly. To this end, we used the grapevine Vitis vinifera L. cultivar Gamay Teinturier (syn. Gamay Freaux or Freaux Tintorier, VIVC #4382) cell suspension line as a model system to study the regulation of anthocyanin accumulation in response to nitrogen supply. The cells were sub-cultured in the presence of either control (25 mM) or low (5 mM) nitrate concentration. Targeted metabolomics and enzyme activity determinations were used to parametrize a constraint-based model describing both the central carbon and nitrogen metabolisms and the flavonoid (phenylpropanoid) pathway connected by the energy (ATP) and reducing power equivalents (NADPH and NADH) cofactors. The flux analysis (2 flux maps generated, for control and low nitrogen in culture medium) clearly showed that in low nitrogen-fed cells all the metabolic fluxes of central metabolism were decreased, whereas fluxes that consume energy and reducing power, were either increased (upper part of glycolysis, shikimate, and flavonoid pathway) or maintained (pentose phosphate pathway). Also, fluxes of flavanone 3β-hydroxylase, flavonol synthase, and anthocyanidin synthase were strongly increased, advocating for a regulation of the flavonoid pathway by alpha-ketoglutarate levels. These results strongly support the hypothesis of anthocyanin biosynthesis acting as an energy escape valve in plant cells, and they open new possibilities to manipulate flavonoid production in plant cells. They do not, however, support a role of anthocyanins as an effective mechanism for coping with carbon excess in high carbon to nitrogen ratio situations in grape cells. Instead, constraint-based modeling output and biomass analysis indicate that carbon excess is dealt with by vacuolar storage of soluble sugars. |
| first_indexed | 2024-12-12T14:58:50Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-12T14:58:50Z |
| publishDate | 2018-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-9b4f4951fac6491aaac97b398eb5443c2022-12-22T00:20:51ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-05-01910.3389/fpls.2018.00421348377Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen LimitationEric Soubeyrand0Sophie Colombié1Bertrand Beauvoit2Zhanwu Dai3Stéphanie Cluzet4Ghislaine Hilbert5Christel Renaud6Lilly Maneta-Peyret7Martine Dieuaide-Noubhani8Jean-Michel Mérillon9Yves Gibon10Serge Delrot11Eric Gomès12UMR 1287 Ecophysiologie et Génomique Fonctionnelle de la Vigne, Université de Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceUMR 1332 Biologie du Fruit et Pathologie, INRA-Bordeaux, IBVM, Bordeaux, FranceUMR 1332 Biologie du Fruit et Pathologie, INRA-Bordeaux, IBVM, Bordeaux, FranceUMR 1287 Ecophysiologie et Génomique Fonctionnelle de la Vigne, INRA-Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceEA 3675 GESVAB, Université de Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceUMR 1287 Ecophysiologie et Génomique Fonctionnelle de la Vigne, INRA-Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceUMR 1287 Ecophysiologie et Génomique Fonctionnelle de la Vigne, INRA-Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceUMR 5200 Laboratoire de Biogenèse Membranaire, Université de Bordeaux, Bordeaux, FranceUMR 1332 Biologie du Fruit et Pathologie, Université de Bordeaux, IBVM, Bordeaux, FranceEA 3675 GESVAB, Université de Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceUMR 1332 Biologie du Fruit et Pathologie, INRA-Bordeaux, IBVM, Bordeaux, FranceUMR 1287 Ecophysiologie et Génomique Fonctionnelle de la Vigne, Université de Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceUMR 1287 Ecophysiologie et Génomique Fonctionnelle de la Vigne, Université de Bordeaux, Institut des Sciences de la Vigne et du Vin, Bordeaux, FranceAnthocyanin biosynthesis is regulated by environmental factors (such as light, temperature, and water availability) and nutrient status (such as carbon, nitrogen, and phosphate nutrition). Previous reports show that low nitrogen availability strongly enhances anthocyanin accumulation in non carbon-limited plant organs or cell suspensions. It has been hypothesized that high carbon-to-nitrogen ratio would lead to an energy excess in plant cells, and that an increase in flavonoid pathway metabolic fluxes would act as an “energy escape valve,” helping plant cells to cope with energy and carbon excess. However, this hypothesis has never been tested directly. To this end, we used the grapevine Vitis vinifera L. cultivar Gamay Teinturier (syn. Gamay Freaux or Freaux Tintorier, VIVC #4382) cell suspension line as a model system to study the regulation of anthocyanin accumulation in response to nitrogen supply. The cells were sub-cultured in the presence of either control (25 mM) or low (5 mM) nitrate concentration. Targeted metabolomics and enzyme activity determinations were used to parametrize a constraint-based model describing both the central carbon and nitrogen metabolisms and the flavonoid (phenylpropanoid) pathway connected by the energy (ATP) and reducing power equivalents (NADPH and NADH) cofactors. The flux analysis (2 flux maps generated, for control and low nitrogen in culture medium) clearly showed that in low nitrogen-fed cells all the metabolic fluxes of central metabolism were decreased, whereas fluxes that consume energy and reducing power, were either increased (upper part of glycolysis, shikimate, and flavonoid pathway) or maintained (pentose phosphate pathway). Also, fluxes of flavanone 3β-hydroxylase, flavonol synthase, and anthocyanidin synthase were strongly increased, advocating for a regulation of the flavonoid pathway by alpha-ketoglutarate levels. These results strongly support the hypothesis of anthocyanin biosynthesis acting as an energy escape valve in plant cells, and they open new possibilities to manipulate flavonoid production in plant cells. They do not, however, support a role of anthocyanins as an effective mechanism for coping with carbon excess in high carbon to nitrogen ratio situations in grape cells. Instead, constraint-based modeling output and biomass analysis indicate that carbon excess is dealt with by vacuolar storage of soluble sugars.https://www.frontiersin.org/article/10.3389/fpls.2018.00421/fullanthocyaninsgrapevinecell redox statusenergy escape valve hypothesisconstraint-based modeling |
| spellingShingle | Eric Soubeyrand Sophie Colombié Bertrand Beauvoit Zhanwu Dai Stéphanie Cluzet Ghislaine Hilbert Christel Renaud Lilly Maneta-Peyret Martine Dieuaide-Noubhani Jean-Michel Mérillon Yves Gibon Serge Delrot Eric Gomès Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen Limitation Frontiers in Plant Science anthocyanins grapevine cell redox status energy escape valve hypothesis constraint-based modeling |
| title | Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen Limitation |
| title_full | Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen Limitation |
| title_fullStr | Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen Limitation |
| title_full_unstemmed | Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen Limitation |
| title_short | Constraint-Based Modeling Highlights Cell Energy, Redox Status and α-Ketoglutarate Availability as Metabolic Drivers for Anthocyanin Accumulation in Grape Cells Under Nitrogen Limitation |
| title_sort | constraint based modeling highlights cell energy redox status and α ketoglutarate availability as metabolic drivers for anthocyanin accumulation in grape cells under nitrogen limitation |
| topic | anthocyanins grapevine cell redox status energy escape valve hypothesis constraint-based modeling |
| url | https://www.frontiersin.org/article/10.3389/fpls.2018.00421/full |
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