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Tocochromanols: Rancid Lipids, Seed Longevity, and Beyond

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Tocochromanols: Rancid Lipids, Seed Longevity, and Beyond COMMENTARY Tocochromanols: Rancid lipids, seed longevity, and beyond Nicholas Smirnoff1 College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4QD, United Kingdom nvestigation of tocochromanols, li- pophilic molecules that protect I against fatty acid peroxidation, is still providing surprises. They are uniquely synthesized by photosynthetic organisms, widely studied in relation to their photoprotective role in photosyn- thesis, and are of importance in human nutrition as vitamin E. An article in PNAS from the DellaPenna laboratory (1) makes a significant step forward by showing that tocochromanols are essential for main- taining the viability of Arabidopsis thaliana seeds, suggesting that tocochromanols are a key component in the evolution of des- iccation-resistant seeds. Tocochromanols Protect Against Lipid Peroxidation Lipid peroxidation is a chain reaction in which unsaturated fatty acids in lipids of Fig. 1. Peroxidation of an unsaturated fatty acyl chain is initiated by a hydroxyl radical (OH·)oranacyl various types are oxidized, producing peroxyl radical (R·). Tocochromanols scavenge acyl peroxyl radicals and therefore minimize their reaction highly reactive products that can cause with further acyl chains. Details of the tocochromanol oxidation products are not shown, but most of further cellular damage. Polyunsaturated these can be converted back to tocochromanol. fatty acids (PUFAs) are particularly sus- ceptible to peroxidation, a chain reaction active oxygen species formed during pho- PC-8. The double vte1 vte2 mutant lacks initiated by hydroxyl radicals (Fig. 1). tosynthesis (7). both tocopherols and PC-8 (1). Its seeds The first reasonably stable products, fatty rapidly lose viability after harvesting owing acyl hydroperoxides, are still sufficiently Rancid Lipids and Seed Longevity to catastrophic fatty acid peroxidation, reactive to produce aldehydes (reactive The article by Mène-Saffrané et al. (1) clearly indicating a role for tocochroma- electrophiles) that cause cellular damage focuses attention on plastochromanol-8 nols, including PC-8, in protecting un- and induce the expression of defense- (PC-8), a less well-studied tocochromanol. saturated fatty acids from peroxidation. related genes (2, 3). This process is seen in Seeds, particularly oil seeds that store tri- The results also show that PC-8 and to- fi the rancidi cation of fats and oils stored acylglyerols (TAGs) as a food reserve in copherols are essential for the long-term in the air. Chain reactions are minimized oil bodies, are rich in γ-tocopherol (8). viability and maintenance of vigor of Ara- by preventing initiation or propagation. Previously, the DellaPenna group showed bidopsis seeds. Because PC-8 concentra- Initiation is minimized by antioxidant sys- that Arabidopsis thaliana mutants lacking tion is low compared with the tocopherols, tems that decrease hydroxyl radical pro- homogentisate phytyltransferase (VTE2) the results suggest that its longer prenyl duction (4). The tocochromanols are fi are unable to synthesize tocopherols. The tail improves its antioxidant ef ciency or effective in preventing the propagation of mutant seeds had reduced longevity during helps to target it to the oil bodies. The rate peroxidation. Of these, α-tocopherol and storage and suffered fatty acid perox- constants of the reaction of tocopherols γ-tocopherol (1) are the most common in and PC-8 with singlet oxygen are similar plants (5, 6). Tocochromanols consist of idation during germination (8), suggesting an important role for tocopherols in pro- (10), as might be expected from the iden- a hydrophobic isoprenoid tail that is an- tical structure of their hydroxychroman tecting seeds that use TAGs as a food re- chored into membrane bilayers, whereas rings; thus, prenyl chain length must be serve. The present article extends these a more hydrophilic hydroxychroman ring important in the effectiveness of PC-8. observations and shows that PC-8 plays sits nearer the surface. To prevent propa- Significantly, Mène-Saffrané et al. as- gation of fatty acid peroxidation, the hy- a key role in preventing fatty acid perox- Arabidopsis sessed the viability of seeds stored in dry droxyl group on the hydroxychroman ring idation in seeds. The authors conditions, the usual situation for crop readily donates H to acyl peroxyl radicals demonstrated this function by making plants. However, seeds that lie dormant to form an acyl hydroperoxide and a toco- a double mutant affected in VTE2 and in soil are fully hydrated or at least will pheroxyl radical (Fig. 1). Tocochromanols VTE1 (tocopherol cyclase). Tocopherol go through cycles of wetting and drying. also react with singlet oxygen, a reactive cyclase forms the hydroxychroman ring of form of oxygen produced during photo- tocochromanols. The role of VTE1 in PC- synthesis. This suggests an important role 8 synthesis was recently demonstrated in Author contributions: N.S. wrote the paper. in protection of the photosynthetic thyla- Arabidopsis (9). In these studies, as in the The author declares no conflict of interest. koid membranes, which are rich in PUFAs present article, PC-8 was not detected in See companion article on page 17815 in issue 41 of volume and therefore susceptible to peroxidation the vte1 mutant, leading to the suggestion 107. initiated by singlet oxygen and other re- that plastoquinol-9 is the precursor of 1E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1012749107 PNAS Early Edition | 1of2 Downloaded by guest on September 28, 2021 It would be interesting to know whether tocopherol has been engineered in Arabi- important in protecting photosynthesis the protective effect of tocochromanols is dopsis seeds by expression of homoge- from photooxidative stress. However, specific to desiccated cells or also required ntisate phytyltransferase, driven bya a strong phenotype is only revealed under to maintain the viability of hydrated dor- seed-specific promoter (15). The seedlings under extreme conditions or in combina- mant seeds. Under hydrated conditions, were not more resistant to oxidative stress tion with mutations in other photopro- other antioxidant and repair systems may during germination, but it would be in- tective components (6, 7). The emergence operate. Also, it would be interesting to teresting to know whether they show of PC-8 as a key player in protecting seed know whether tocochromanols, particu- lipids and its effectiveness as a singlet larly PC-8, are also involved in the desic- oxygen scavenger suggest that the role of cation resistance of photosynthetic cells Tocochromanols tocochromanols in photoprotection of in algae, bryophytes, and the angiosperm are essential for photosynthesis needs further investigation resurrection plants. using the vte1 vte2 double mutant. The present results agree with previous maintaining the viability observations that seed longevity is oxygen Conclusion dependent and that oxidative damage is of Arabidopsis Mène-Saffrané et al. (1) show very clearly a determinant of desiccation resistance the key role of tocochromanols in Arabi- (11, 12). Glutathione redox state has been thaliana seeds. dopsis seed longevity and vigor, indicating suggested as another determinant of via- their importance in the formation of bility in the desiccated state: the glutathi- desiccation-resistant seeds. Further in- one pool oxidizes over time until viability increased longevity after harvest. A class vestigation could determine if this role is is lost at a specific redox state (13). The of protective hydrophilic proteins that ac- equally important in seeds that store more relationship between glutathione and to- cumulate during seed maturation is the starch than oil. Nonantioxidant roles have cochromanols in desiccated cells is not dehydrins (hydrophilins). Various roles in been proposed for tocochromanols (18), known—are they protecting the same cel- protecting desiccated proteins and mem- including possible effects on membrane lular components, and do they interact? branes have been proposed for these pro- function in the cold or under desiccation Because metabolism is slow in anhydro- teins (16). A histidine-rich dehydrin binds (19). Not commented upon by the authors biotic conditions, another question to be metals with high affinity (17) and could is the ability of a few vte1 vte2 double resolved is whether oxidized tocochroma- therefore act as an antioxidant by scav- mutants to survive the seedling stage nols can be regenerated in dry seeds or enging redox active metals, minimizing and apparently grow normally. Therefore, whether tocochromanol content falls sub- initiation of fatty acid peroxidation by unlike their hydrophilic antioxidant “col- stantially during storage. The intriguing preventing hydroxyl radical formation league” ascorbic acid (20), tocochroma- possibility that selection for longevity and through the Fenton reaction. nols may not be absolutely essential for vigorous seedling growth in crop plants plant growth, at least under laboratory has inadvertently increased their seed Tocochromanols and Photosynthesis conditions. Clearly, more remains to be tocochromanol levels (14) is mentioned Tocopherols and the precursor 2,3-di- learned about the biological functions of by Mène-Saffrané et al. Increased seed methyl-6-phytyl-1,4-benzoquinol (1) are this intriguing group of molecules. 1. Mène-Saffrané L, Jones AD, DellaPenna D (2010) Plasto- for seed longevity and for preventing lipid peroxida- 14. Velasco L, Goffman FD (2000) Tocopherol, plastochro-
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