Abstract
Vitamin E occurs in all photosynthetic organisms examined to date. Tocopherols predominate in photosynthetic tissues (α-tocopherol being the major form), while either tocopherols or tocotrienols (or both) are present in seeds. Tocotrienols have not been described in photosynthetic tissues thus far. Here, we report on the presence of tocotrienols in leaves of higher plants. Both tocopherols and tocotrienols accumulated in leaves of Vellozia gigantea, an endemic plant found in the rupestrian fields of Serra do Cipó, Brazil. Increased plant size had a remarkable effect on the vitamin E composition of leaves, α-tocopherol and β-tocotrienol levels being highest in the largest individuals, but only during the dry season. Vitamin E levels positively correlated with lipid hydroxyperoxide levels, which also increased in the largest individuals during the dry season. However, the maximum efficiency of PSII photochemistry (F v/F m ratio) kept above 0.75 throughout the experiment, thus indicating absence of photoinhibitory damage to the photosynthetic apparatus. It is concluded that higher plants, such as V. gigantea, can accumulate tocotrienols in leaves, aside from tocopherols, and that the levels of both tocopherols and tocotrienols in the leaves of this species are strongly modulated by seasonal and plant size effects.
Abbreviations
- F v/F m ratio:
-
Maximum efficiency of photosystem II photochemistry
- HPLC:
-
High performance liquid chromatography
- LC:
-
Liquid chromatography
- LMA:
-
Leaf mass per area ratio
- MS:
-
Mass spectrometry
- PSII:
-
Photosystem II
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
References
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396
Cahoon EB, Hall SE, Ripp KG, Ganzke TS, Hitz WD, Coughlan SJ (2003) Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat Biotechnol 21:1082–1087
Cela J, Chang C, Munné-Bosch S (2011) Accumulation of γ-rather than α-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52:1389–1400
DeLong JM, Prange RK, Hodges DM, Forney CF, Bishop MC, Quilliam M (2002) Using a modified ferrous oxidation-xylenol orange (FOX) assay for detection of lipid hydroperoxides in plant tissue. J Agric Food Chem 50:248–254
Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61:1549–1566
Galli F, Azzi A (2010) Present trends in vitamin E research. BioFactors 36:33–42
Havaux M, Bonfils J-P, Lütz C, Niyogi KK (2000) Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol 124:273–284
Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Horvath G, Wessjohann L, Bigirimana J, Jansen M, Guisez Y, Caubergs R, Horemans N (2006) Differential distribution of tocopherols and tocotrienols in photosynthetic and non-photosynthetic tissues. Phytochemistry 67:1185–1195
Hussain N, Irshad F, Jabeen Z, Shamsi IH, Li Z, Jiang L (2013) Biosynthesis, structural, and functional attributes of tocopherols in planta: past, present, and future perspectives. J Agric Food Chem 61:6137–6149
Lanina AS, Toledo P, Sampels S, Kamal-Eldin A, Jastrebova JA (2007) Comparison of reversed-phase liquid chromatography–mass spectrometry with electrospray and atmospheric pressure chemical ionization for analysis of dietary tocopherols. J Chromatogr 1157:159–170
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R (2013) Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc Natl Acad Sci USA 110:E623–E632
Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2005) Tocopherols protect Synechocystis sp. Strain PCC 6803 from lipid peroxidation. Plant Physiol 138:1422–1435
Matringe M, Ksas B, Rey P, Havaux M (2008) Tocotrienols, the unsaturated forms of vitamin E, can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiol 147:764–778
Mencuccini M, Grace J (1996) Developmental patterns of above-ground hydraulic conductance in a Scots pine (Pinus sylvestris L.) age sequence. Plant Cell Environ 19:939–948
Menezes NL, Giulietti AM (1986) Serra do Cipó—Paraíso dos Botânicos. Ciência Hoje 25:38–44
Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748
Munné-Bosch S, Alegre L (2000) Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210:925–931
Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57
Munné-Bosch S, Lalueza P (2007) Age-related changes in oxidative stress markers and abscisic acid levels in a drought-tolerant shrub, Cistus clusii grown under Mediterranean field conditions. Planta 225:1039–1049
Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161:5–19
Padley FB, Gunstone FD, Harwood J (1994) The lipid handbook, 2nd edn. Chapman & Hall, London
Siles L, Cela J, Munné-Bosch S (2013) Vitamin E analyses in seeds reveal a dominant presence of tocotrienols over tocopherols in the Arecaceae family. Phytochemistry 95:207–214
Szymanska R, Kruk J (2008) γ-Tocopherol dominates in young leaves of runner bean (Phaseolus coccineus) under a variety of growing conditions: the possible functions of γ-tocopherol. Phytochemistry 69:2142–2148
Tan B, Watson RR, Preedy VR (2012) Tocotrienols: Vitamin E beyond tocopherols, 2nd edn. CRC Press, USA, pp 1–16
Trebst A, Depka B, Holländer-Czytko H (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett 43:2157–2162
Van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150
Yang W, Cahoon RE, Hunter SC, Zhang C, Han J, Borgschulte T, Cahoon EB (2011) Vitamin E biosynthesis: functional characterization of the monocot homogentisate geranylgeranyltransferase. Plant J 65:206–217
Acknowledgments
Support for the research was received through grants BFU2012-32057, BFU2009-07294, BFU2009-06045 and CSD2008-00040 from the Spanish Government, and the ICREA Academia prize to S.M.-B., which is funded by the Catalan Government. We thank Fábio Vieira for help in preparing Figure 1, and Leilane Barreto, Ana Laura Lamounier Magalhães and Daniela Moreira Duarte for help in samplings. We are also very grateful to Maren Müller for her help with LC–MS/MS analyses.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Morales, M., Garcia, Q.S., Siqueira-Silva, A.I. et al. Tocotrienols in Vellozia gigantea leaves: occurrence and modulation by seasonal and plant size effects. Planta 240, 437–446 (2014). https://doi.org/10.1007/s00425-014-2104-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-014-2104-4