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

• Published in: Journal of experimental botany 2016-02, Vol.67 (3), p.919-934
• Main Authors: Almeida, Juliana, da Silva Azevedo, Mariana, Spicher, Livia, Glauser, Gaétan, vom Dorp, Katharina, Guyer, Luzia, del Valle Carranza, Andrea, Asis, Ramón, de Souza, Amanda Pereira, Buckeridge, Marcos, Demarco, Diego, Bres, Cécile, Rothan, Christophe, Peres, Lázaro Eustáquio Pereira, Hörtensteiner, Stefan, Kessler, Félix, Dörmann, Peter, Carrari, Fernando, Rossi, Magdalena
• Format: Article
• Language: English
• Subjects: Biosynthetic Pathways - genetics; Carbohydrate Metabolism - genetics; Chlorophyll - metabolism; Down-Regulation - genetics; Esters - metabolism; Fruit - metabolism; Gases - metabolism; Gene Expression Regulation, Plant; Gene Knockdown Techniques; Genes, Plant; Life Sciences; Lipid Metabolism - genetics; Lycopersicon esculentum - enzymology; Lycopersicon esculentum - genetics; Mutation - genetics; Organ Specificity; Photosynthesis - genetics; Photosystem II Protein Complex - metabolism; Phytol - metabolism; Plant Leaves - metabolism; Plant Proteins - genetics; Plant Proteins - metabolism; Plants, Genetically Modified; Prenylation; RESEARCH PAPER; RNA Interference; Solubility; Starch - metabolism; Tocopherols - metabolism; Vegetal Biology
• ISSN: 0022-0957; 1460-2431
• DOI: 10.1093/jxb/erv504

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 SIVTE5 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.