Vitamin E–Defective Mutants of Arabidopsis Tell Tales of Convergent Evolution

Tocopherols (collectively known as vitamin E) are lipophilic antioxidants that are essential in the human diet. Not surprisingly, most of what is known about the biological functions of tocopherols comes from studies of mammalian systems, yet they are synthesized only by photosynthetic eukaryotes and some oxygenic cyanobacteria. Tocopherols belong to a diverse group of compounds known as prenylquinones, which also includes the photosynthetic electron carrier plastoquinone. These compounds have aromatic redox-active head groups that are exposed to the membrane surface and hydrophobic prenyl tails that are embedded in the membrane. Tocopherols generally are believed to play an important antioxidant role against lipid free radicals generated as a result of aerobic metabolism and to help prevent human diseases associated with oxidative stress, such as cardiovascular disease, cancer, chronic inflammation, and neurological disorders (Ricciarelli et al., 2002). There is growing evidence that tocopherols play other important roles in signaling and gene regulation in animals that are not related to their antioxidant function (Ricciarelli et al., 2002). In plants, tocopherols are synthesized at the inner chloroplast envelope and are believed to have an important function in protecting the photosynthetic apparatus from toxic free radicals generated during photosynthesis (Porfirova et al., 2002). To date, there is very little evidence for signal transduction–related or other nonantioxidant roles in plants. One of the only studies to suggest such a function is based on the characterization of the sucrose export defective1 ( sxd1 ) mutant of maize. The sxd1 mutant was identified originally based on a block in sucrose transport from leaves caused by the aberrant formation of plasmodesmata between bundle sheath cells and vascular parenchyma cells (Provencher et al., 2001). When the sxd1 locus was cloned, it was found to encode a chloroplast protein of unknown function, leading to the hypothesis that SXD1 somehow functions in signaling from the chloroplast. Sattler et al. (2003) subsequently showed that the maize SXD1 gene encodes tocopherol cyclase, which catalyzes the conversion of phytyl quinol intermediates to their corresponding tocopherols and is essential for the biosynthesis of all four tocopherol products (Figure 1). These authors postulated that tocopherols might modulate signals required specifically for the development of maize bundle sheath vascular parenchyma plasmodesmata, and tocopherol cyclase mutants of Arabidopsis and Synechocystis sp PCC 6803 do not show a similar phenotype because they lack a cell type physiologically equivalent to the C4 bundle sheath cell (Sattler et al., 2003). However, direct evidence of a role for tocopherols in signaling or gene regulation is lacking. In plants, tocopherols and plastoquinone are synthesized from the precursor homogentisic acid (HGA) (Figure 1). The first