title: Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner.
abstract: 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.
authors.affiliation: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 277, 05508-900, São Paulo, Brazil.
authors.forename: Juliana
authors.initials: J
authors.lastname: Almeida
authors.affiliation: Departamento de Ciências Biológicas, Escola Superior de Agricultura 'Luiz de Queiroz', Universidade de São Paulo, Av. Pádua Dias, 11, CP 09, 13418-900, Piracicaba, Brazil.
authors.forename: Mariana da Silva
authors.initials: Mda S
authors.lastname: Azevedo
authors.affiliation: Laboratory of Plant Physiology, University of Neuchâtel, 2000 Neuchâtel, Switzerland.
authors.forename: Livia
authors.initials: L
authors.lastname: Spicher
authors.affiliation: Neuchâtel Platform of Analytical Chemistry, University of Neuchâtel, 2000 Neuchâtel, Switzerland.
authors.forename: Gaétan
authors.initials: G
authors.lastname: Glauser
authors.affiliation: Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, D-53115 Bonn, Germany.
authors.forename: Katharina
authors.initials: K
authors.lastname: vom Dorp
authors.affiliation: Institute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland.
authors.forename: Luzia
authors.initials: L
authors.lastname: Guyer
authors.affiliation: CIBICI, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, CC 5000, Córdoba, Argentina.
authors.forename: Andrea
authors.initials: A
authors.lastname: del Valle Carranza
authors.affiliation: CIBICI, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, CC 5000, Córdoba, Argentina.
authors.forename: Ramón
authors.initials: R
authors.lastname: Asis
authors.affiliation: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 277, 05508-900, São Paulo, Brazil.
authors.forename: Amanda Pereira
authors.initials: AP
authors.lastname: de Souza
authors.affiliation: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 277, 05508-900, São Paulo, Brazil.
authors.forename: Marcos
authors.initials: M
authors.lastname: Buckeridge
authors.affiliation: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 277, 05508-900, São Paulo, Brazil.
authors.forename: Diego
authors.initials: D
authors.lastname: Demarco
authors.affiliation: INRA and Université de Bordeaux, UMR 1332 Biologie du Fruit et Pathologie, F-33140 Villenave d'Ornon, France.
authors.forename: Cécile
authors.initials: C
authors.lastname: Bres
authors.affiliation: INRA and Université de Bordeaux, UMR 1332 Biologie du Fruit et Pathologie, F-33140 Villenave d'Ornon, France.
authors.forename: Christophe
authors.initials: C
authors.lastname: Rothan
authors.affiliation: Departamento de Ciências Biológicas, Escola Superior de Agricultura 'Luiz de Queiroz', Universidade de São Paulo, Av. Pádua Dias, 11, CP 09, 13418-900, Piracicaba, Brazil.
authors.forename: Lázaro Eustáquio Pereira
authors.initials: LE
authors.lastname: Peres
authors.affiliation: Institute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland.
authors.forename: Stefan
authors.initials: S
authors.lastname: Hörtensteiner
authors.affiliation: Laboratory of Plant Physiology, University of Neuchâtel, 2000 Neuchâtel, Switzerland.
authors.forename: Félix
authors.initials: F
authors.lastname: Kessler
authors.affiliation: Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, D-53115 Bonn, Germany.
authors.forename: Peter
authors.initials: P
authors.lastname: Dörmann
authors.affiliation: Instituto de Biotecnología, Instituto Nacional de Tecnología Agropecuaria and Consejo Nacional de Investigaciones Científicas y Técnicas, PO Box 25, B1712WAA, Castelar, Argentina.
authors.forename: Fernando
authors.initials: F
authors.lastname: Carrari
authors.affiliation: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 277, 05508-900, São Paulo, Brazil mmrossi@usp.br.
authors.forename: Magdalena
authors.initials: M
authors.lastname: Rossi
mesh_terms: D053898:Biosynthetic Pathways / Q000235:genetics; D050260:Carbohydrate Metabolism / Q000235:genetics; D002734:Chlorophyll / Q000378:metabolism; D015536:Down-Regulation / Q000235:genetics; D004952:Esters / Q000378:metabolism; D005638:Fruit / Q000378:metabolism; D005740:Gases / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D055785:Gene Knockdown Techniques; D017343:Genes, Plant; D050356:Lipid Metabolism / Q000235:genetics; D018551:Solanum lycopersicum / Q000201:enzymology* / Q000235:genetics; D009154:Mutation / Q000235:genetics; D009928:Organ Specificity; D010788:Photosynthesis / Q000235:genetics; D045332:Photosystem II Protein Complex / Q000378:metabolism; D010836:Phytol / Q000378:metabolism; D018515:Plant Leaves / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D030821:Plants, Genetically Modified; D054876:Prenylation; D034622:RNA Interference; D012995:Solubility; D013213:Starch / Q000378:metabolism; D024505:Tocopherols / Q000378:metabolism*
chemical_list: D004952:Esters; D005740:Gases; D045332:Photosystem II Protein Complex; D010940:Plant Proteins; D002734:Chlorophyll; D010836:Phytol; D013213:Starch; D024505:Tocopherols
keywords: Carotenoids; Solanum lycopersicum; chlorophyll; phytol; phytol kinase; prenyllipids; tocopherol; tomato; vitamin E.