Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis

Abstract

Given their essential role as vitamin E, tocopherols and tocotrienols have been studied extensively in animals and plants. In contrast, our understanding of the function of plastochromanol-8 (PC-8), a third type of tocochromanol with a longer side chain, is very limited despite the wide distribution of PC-8 in the plant kingdom, including species consumed by humans. To investigate PC-8 function in vivo, we combined the Arabidopsis vte1 mutation that eliminates tocopherols and PC-8 and causes the accumulation of 2,3-dimethyl-6-phytyl-1,4-benzoquinol (DMPBQ), a redox-active tocopherol precursor, and the vte2 mutation that eliminates tocopherols without affecting PC-8. The vte2 vte1 double mutant lacks tocopherols, PC-8, and DMPBQ, and exhibits the most severe physiological and biochemical phenotypes of any tocochromanol-affected genotype isolated to date, most notably a severe seedling developmental phenotype associated with massive lipid oxidation initiated during seed desiccation and amplified during seed quiescence. In contrast, the presence of PC-8 in vte2 suppresses or attenuates all of the developmental and biochemical phenotypes observed in vte2 vte1, demonstrating that PC-8 is a lipid antioxidant in vivo. Finally, the low relative fitness of vte2 vte1 demonstrates that tocopherols and PC-8 are in vivo lipid antioxidants essential for seed plant survival.eed-bearing plants (spermatophytes) first appeared in the fossil record during the late Devonian period (about 370 mya) and represent 90% of the extant terrestrial flora (1). One of the key innovations for this evolutionary success is the capacity of seed to maintain a viable desiccated embryo for extended periods (quiescence), thereby allowing seed plants to occupy ecosystems experiencing temporary nonpermissive growth conditions (e.g., drought, frost). Extreme examples of the ability of seed to preserve plant genetic resources are demonstrated by the germination and development of plants from 2,000-y-old date seed, 1,300-y-old lotus seed, and 600-y-old canna seed (2). More commonly, seed viability gradually decreases during quiescence as a function of storage conditions (e.g., temperature, humidity, oxygen) and initial seed quality (e.g., moisture, pathogens) (3).Genetic factors underlying seed longevity have been studied only recently (reviewed in ref. 2). Protein repair and folding during seed development, maturation, and storage have been shown to be important factors affecting seed longevity. Overexpression of L-isoaspartyl O-methyltransferase 1, an enzyme that repairs damaged aspartate residues in proteins, reduced seed protein L-isoaspartyl levels, and enhanced germination compared with WT in accelerated aging tests, which subject dry seed to heat and high humidity (4). Similarly, overexpression of the heat stress transcription factor HaHSFA9 increased several heat-shock proteins in seed and improved resistance to accelerated aging treatments (5). Proper development and maturation of the seed coat (testa) also impacts seed longevity. For example, Ar...

Chloroplast lipid droplet type II NAD(P)H quinone oxidoreductase is essential for prenylquinone metabolism and vitamin K 1 accumulation

“…3G). PC-8 is derived from PQ by the activity of VTE1, the tocopherol cyclase, present in the plastoglobule (18,19,32). For the cyclase to close the chromanol ring in dimethylphytylquinone (the precursor of γ-tocopherol) or in PQ, the quinol groups must preferentially be present in the reduced form (33).…”

A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation

“…VTE1, even penetrated the polar lipid monolayer, and extended into the core of the PG potentially allowing it to access its hydrophobic substrates Kobayashi and DellaPenna 2008;Mene-Saffrane et al 2010).…”

Novel Loci Underlie Natural Variation in Vitamin E Levels in Maize Grain

“…Tocochromanols are synthesized by all plant tissues but are most abundant in seeds, where they limit the oxidation of membrane and storage lipids, making them essential for seed viability (Sattler et al, 2004;Mène-Saffrané et al, 2010) and overall plant fitness (Maeda et al, 2006;Maeda and DellaPenna, 2007;DellaPenna and Mène-Saffrané, 2011;Inoue et al, 2011). In the human diet, tocochromanols serve as both lipid-soluble antioxidants and the essential nutrient vitamin E (Hussain et al, 2013;Ahsan et al, 2015), with a-tocopherol having the highest vitamin E activity, a-tocotrienol and g-tocopherol 3-and 6-fold lower activity, respectively, and that of other tocochromanols being negligible (Kamal-Eldin and Appelqvist, 1996;DellaPenna and Mène-Saffrané, 2011).…”