Tocopherols and ER Fatty Acid Metabolism

Tocopherols (vitamin E) are synthesized only in photosynthetic organisms, but their function in plants has been uncertain for many years. It is widely believed that they function as antioxidants in animal membranes (Traber and Atkinson, 2007) but has more recently been suggested that they may also function in regulating signal transduction and gene expression (Azzi, 2007). The Arabidopsis mutant vitamin e deficient2 (vte2) is defective in homogentisate phytyl transferase, the first committed enzyme of the tocopherol biosynthetic pathway, and lacks all tocopherols and pathway intermediates. A number of studies on vte2 mutants have shown that tocopherols play a limited role in protection against photooxidative stress under normal growth or high light stress conditions, but they are essential as antioxidants during seed dormancy and early seedling development (Sattler et al., 2004) and also play a crucial role in phloem parenchyma transfer cell wall development and phloem loading in mature leaves, particularly at low nonfreezing temperatures (Maeda et al., 2006).

In this issue of The Plant Cell, Maeda et al. (pages 452–470) investigate the underlying cause of the defect in phloem loading in the vte2 mutant. The authors analyzed polyunsaturated fatty acid (PUFA) composition in the mutant because it is assumed that tocopherols are associated with PUFAs in the plastid membrane. Maeda et al. found that the PUFA composition was similar in the wild type and vte2 grown at 22°C, but significant differences became apparent after low temperature treatment. After 14 d at 7°C, vte2 mutant leaf tissue had lower levels of linolenic acid (18:3) and higher levels of linoleic acid (18:2) compared with the wild type.

Lipid profiling and oxidized lipid analysis suggested that decreased 18:3 content of the mutant at low temperature was due to a defect in 18:3 synthesis in the endoplasmic reticulum (ER), rather than increased 18:3 oxidation. Radioactive labeling experiments further suggested that tocopherol deficiency in the vte2 mutant was associated with a defect in ER-mediated conversion of dienoic to trienoic fatty acids at low temperature. In addition, creation of a double mutant of vte2 with fatty acid desaturase2 (fad2), which is defective in ER-mediated conversion of monoenoic to dienoic fatty acids, suppressed the low temperature–induced vte2 phenotype (see figure), including impaired development of phloem parenchyma transfer cell walls, whereas combination with various other fad mutants had little or no effect. These results provide new information on the interaction of tocopherols and ER fatty acid metabolism and show that tocopherols function in the adaptation of Arabidopsis to growth at low temperature by modulating PUFA metabolism in the ER.

Figure 1.

The chilling-sensitive phenotype of the vte2 tocopherol-deficient mutant was suppressed when combined with the fad2 mutation in the vte2 fad2 double mutant, suggesting a role for tocopherols in ER-mediated conversion of dienoic to trienoic fatty acids at low temperature (8-week-old plants shown after 4 weeks at 7°C).