Essential role for phytol kinase and tocopherol in tolerance to combined light and temperature stress in tomato.

In a changing environment, plants need to cope with the impact of rising temperatures together with high light intensity. Here, we used lipidomics in the tomato model system to identify lipophilic molecules that enhance tolerance to combined high-temperature and high-light stress. Among several hundred metabolites, the two most strongly up-regulated compounds were α-tocopherol and plastoquinone/plastoquinol. Both are well-known lipid antioxidants and contribute to the protection of photosystem II (PSII) against photodamage under environmental stress. To address the protective function of tocopherol, an RNAi line (vte5) with decreased expression of VTE5 and reduced levels of α-tocopherol was selected. VTE5 encodes phytol kinase, which acts in the biosynthetic pathway of tocopherols. vte5 suffered strong photoinhibition and photobleaching when exposed to combined high-light and high-temperature stress, but neither stress alone produced a visible phenotype. As vte5 had plastoquinone levels similar to those of the wild type under combined stress, the strong phenotype could be attributed to the lack of α-tocopherol. These findings suggest that VTE5 protects against combined high-light and high-temperature stress and does so by supporting α-tocopherol production.

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

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.

Lipid Antioxidant and Galactolipid Remodeling under Temperature Stress in Tomato Plants.

Increased temperatures are a major scenario in climate change and present a threat to plant growth and agriculture. Plant growth depends on photosynthesis. To function optimally, the photosynthetic machinery at the thylakoid membrane in chloroplasts continuously adapts to changing conditions. Here, we set out to discover the most important changes arising at the lipid level under high temperature (38°C) in comparison to mild (20°C) and moderately cold temperature (10°C) using a non-targeted lipidomics approach. To our knowledge, no comparable experiment at the level of the whole membrane system has been documented. Here, 791 molecular species were detected by mass spectrometry and ranged from membrane lipids, prenylquinones (tocopherols, phylloquinone, plastoquinone, plastochromanol), carotenoids (ß-carotene, xanthophylls) to numerous unidentified compounds. At high temperatures, the most striking changes were observed for the prenylquinones (α-tocopherol and plastoquinone/-ol) and the degree of saturation of fatty acids in galactolipids and phosphatidyl ethanolamine. Photosynthetic efficiency at high temperature was not affected but at moderately cold temperature mild photoinhibition occurred. The results indicate, that the thylakoid membrane is remodeled with regard to fatty acid saturation in galactolipids and lipid antioxidant concentrations under high temperature stress. The data strongly suggest, that massively increased concentrations of α-tocopherol and plastoquinone are important for protection against high temperature stress and proper function of the photosynthetic apparatus.

Unexpected roles of plastoglobules (plastid lipid droplets) in vitamin K1 and E metabolism.

Tocopherol (vitamin E) and phylloquinone (vitamin K1) are lipid-soluble antioxidants that can only be synthesized by photosynthetic organisms. These compounds function primarily at the thylakoid membrane but are also present in chloroplast lipid droplets, also known as plastoglobules (PG). Depending on environmental conditions and stage of plant development, changes in the content, number and size of PG occur. PG are directly connected to the thylakoid membrane via the outer lipid leaflet. Apart from storage, PG are active in metabolism and likely trafficking of diverse lipid species. This review presents recent advances on how plastoglobules are implicated in the biosynthesis and metabolism of vitamin E and K.