Phytochemistry xxx (2014) xxx–xxx

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Molecules of Interest

Plastochromanol-8: Fifty years of research Jerzy Kruk a, Renata Szyman´ska b, Jana Cela c, Sergi Munne-Bosch c,⇑ a

Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland Department of Medical Physics and Biophysics, Faculty of Physics and Applied Computer Science, AGH University of Science and Technology, Reymonta 19, 30-059 Krakow, Poland c Departament de Biologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 643, E-08028 Barcelona, Spain b

a r t i c l e

i n f o

Article history: Received 11 May 2014 Received in revised form 8 September 2014 Available online xxxx Keywords: Antioxidants Plastochromanol-8 Tocochromanols Tocopherols Vitamin E

a b s t r a c t Plastochromanol-8 (PC-8) is an antioxidant that, together with tocopherols and tocotrienols, belongs to the group of tocochromanols. Plastochromanol-8 has been found to occur in several plant species, including mosses, and lichens. PC-8 is found in seeds, leaves and other organs of higher plants. In leaves, PC-8 is restricted to chloroplasts. The identification of tocopherol cyclase (VTE1) as the key enzyme in the biosynthesis of PC-8 suggests that plastoglobules are the primary site of its biosynthesis. Other enzymes related with PC-8 biosynthesis in plastoglobules include: NDC1 and the ABC1-like kinase ABC1K3. The antioxidant properties of PC-8 are similar to those of other chloroplastic antioxidants in polar solvents but considerably they are enhanced in hydrophobic environments, suggesting that the unsaturated side chain performs some quenching activity. As a result of a non-enzymatic reaction, singlet oxygen can oxidize any of the 8 double bonds in the side chain of PC-8, giving at least eight hydroxy-PC-8 isomers. This review summarizes current evidence of a widespread distribution of PC-8 in photosynthetic organisms, as well as the contribution of PC-8 to the pool of lipid-soluble antioxidants in both leaves and seeds. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Plastochromanol-8 (PC-8), as a natural component of plant tissues, was discovered 50 years ago in the leaves of the rubber tree (Hevea brasiliensis), where its content exceeded even that of a-tocopherol and plastoquinone (Whittle et al., 1965). Spectroscopic and chromatographic properties of the compound were found to be identical to those of synthetic PC-8, a c-tocotrienol homologue but with a longer side chain (Fig. 1). Together with tocopherols and tocotrienols, PC-8 belongs to the group of tocochromanols, all of which contain a chromanol ring that is responsible for their spectral and antioxidant properties. Further research revealed that PC-8 occurs in the leaves of other plants (Dunphy et al., 1966), as well as in rape and maize seed oils (Dunphy et al., 1966) and that of flax (Leerbeck et al., 1967). Besides the leaves, PC-8 was also found in abundant amounts in latex from H. brasiliensis together with PC-8 esters (Dunphy et al., 1966). Interest in PC-8 was renewed through recent studies of Arabidopsis vitamin E (vte)-biosynthetic mutants that revealed the biosynthetic pathway of PC-8 (Fig. 1) (Szyman´ska and Kruk, 2008, 2010a; Zbierzak et al., 2010). Earlier studies of Brassica napus with overexpressed tocopherol cyclase (Kumar et al., 2005), where

⇑ Corresponding author. Fax: +34 934112842. E-mail address: [email protected] (S. Munne-Bosch).

the PC-8 level was increased in seeds, had led to the suggestion that the enzyme might be involved in PC-8 formation from plastoquinol. This review summarizes current evidence of a widespread distribution of PC-8 in photosynthetic organisms. Furthermore, the contribution of PC-8 to the pool of lipid-soluble antioxidants in both leaves and seeds is discussed.

2. Distribution of PC-8 in photosynthetic organisms Together with tocopherols and tocotrienols, PC-8 belongs to the group of tocochromanols. Tocopherols are ubiquitous in all plant species and are particularly concentrated in photosynthetic tissues, while tocotrienols are only found in some plant species and are almost exclusively found in seeds and fruits, particularly in monocots (Falk and Munné-Bosch, 2010). Although our knowledge of PC-8 distribution is still limited, the data accumulated thus far suggest a widespread distribution of PC-8 in the plant kingdom. PC-8 appears not to be found in cyanobacteria that synthesize tocopherols (Kruk, unpublished). Since its discovery in the leaves of the rubber tree (H. brasiliensis) (Whittle et al., 1965), PC-8 has been found in the leaves of several species belonging to unrelated families, including mosses and lichens (Tables 1 and 2). The relative abundance of PC-8 depends on several factors, including the species, subspecies, cultivar,

http://dx.doi.org/10.1016/j.phytochem.2014.09.011 0031-9422/Ó 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Kruk, J., et al. Plastochromanol-8: Fifty years of research. Phytochemistry (2014), http://dx.doi.org/10.1016/ j.phytochem.2014.09.011

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J. Kruk et al. / Phytochemistry xxx (2014) xxx–xxx Table 1 Occurrence of plastochromanol-8 (PC-8) in leaves of several higher plant species. The amounts of PC-8 are given in lg/g of dry matter (DW) and as a percentage of total tocochromanols (%, w/w). Note that PC-8 has also been detected, although not at quantifiable levels, in leaves of Lotus japonicus, Nicotiana tabacum, Solanum lycopersicum, Solanum tuberosum and Oryza sativa (Zbierzak et al., 2010).

Fig. 1. Biosynthesis of plastochromanol-8 (PC-8) in plants.

growth conditions and tissue. Many species have been analyzed to date and PC-8 has generally been found to be less abundant than tocopherols, with the exception of Cecropia sp., Pseudobombax munguba and H. brasiliensis. It is notable that the levels of PC-8 in leaves depend not only on the species but also on the leaf age or developmental stage. In B. napus leaves, the highest contents were found during stem formation; and in Arabidopsis, PC-8 levels were found to increase in young leaves under strong light conditions (Nogala-Kalucka et al., 2002; Szyman´ska and Kruk, 2010a). Very few studies report the distribution of PC-8 in different organs of the same species; although, PC-8 has been detected in several organs, including leaves, buds, flowers, pods and seeds of B. napus (Nogala-Kałucka et al., 2002). PC-8 was also detected in tomato fruit (Zbierzak et al., 2010), but the highest levels are generally found in leaves (9.5 lg/g DW) and seeds (4 lg/g DW, Table 3). PC-8 has also been detected at non-quantifiable levels in the yam tuber (Dioscorea alata, Cheng et al., 2007). Seeds and seed oils are another natural source of PC-8 (Table 4); it has been detected, although not quantified, in several species (Bagci et al., 2004; Bagci and Özçelik, 2009; Velasco and Goffman, 2000). In general, the levels of PC-8 in seeds and in seed oils are similar to those in leaves. In all the seeds and seed oils analyzed, PC-8 levels are lower than those of tocopherols, although in Linum usitatissimum ‘‘oleofarm’’, PC-8 content is more than 50% that of tocopherol (Gruszka and Kruk, 2007). PC-8 levels in seeds or seed oils can vary within the same species, as illustrated in B. napus, Camelia sativa, Cannabis sativa and L. usitatissimum. Different experimental approaches to the growth of plants or the extraction of oil as well as the use of different subspecies could explain these

Species

PC-8 (lg/g DW) PC-8 (%) References

Alchornea castaneaefolia Amomyrtus luma Annona cf. hypoglauca Apeiba sp. Araucaria araucana Berberis buxifolia Cecropia sp. Chusquea quila Crathaeva benthamii Crescentia amazonica Erythrina fusca Fuchsia magellanica Garcinia brasiliensis Hevea brasiliensis Hypopterygium arbuscula Laetia corymbulosa Macrolobium acaciifolium Misodendrum linearifolium Misodendrum punctulatum Mitraria coccinea Mutisia spinosa Nectandra amazonum Notophagus betuloides Pouteria glomerata Pseudobombax munguba Psidium acutangulum Pterocarpus amazonum Tabaernamontana siphilitica Triplaris pyramidales Vitex cymosa Zygia sp.

218 45 23 617 132 9 1783 32 13 35 220 66 101 318 3 84 41 24 3 11 3 55 44 20 3640 10 36 276 5 55 40

46 23 47 84 58 3 106 25 36 11 38 55 4 225 9 19 5 12 0.5 17 7 5 42 7 182 9 17 80 2 13 8

Kruk, unpublished Strzałka et al., 2009 Kruk, unpublished Kruk, unpublished Strzałka et al., 2009 Strzałka et al., 2009 Kruk, unpublished Strzałka et al., 2009 Kruk, unpublished Kruk, unpublished Kruk, unpublished Strzałka et al., 2009 Kruk, unpublished Whittle et al., 1965 Strzałka et al., 2009 Kruk, unpublished Kruk, unpublished Strzałka et al., 2009 Strzałka et al., 2009 Strzałka et al., 2009 Strzałka et al., 2009 Kruk, unpublished Strzałka et al., 2009 Kruk, unpublished Kruk, unpublished Kruk, unpublished Kruk, unpublished Kruk, unpublished Kruk, unpublished Kruk, unpublished Kruk, unpublished

Table 2 Occurrence of plastochromanol-8 (PC-8) in mosses and lichens. The amounts of PC-8 are given in absolute amounts (as lg/g DW) and as a percentage of total tocochromanols (%, w/w). All values are taken from Strzałka et al. (2011).

Bryum pseudotriquetrum Placopsis contortuplicata Polytrichastrum alpinum Syntrichia magellanica Usnea aurantiaco-atra Warnstrofia sarmentosa

PC-8 (lg/g DW)

PC-8 (%)

13 0.6 19 4 1 4

8 1 9 2 44 4

differences. In L. usitatissimum, different subspecies display important differences in PC-8 levels, ranging from 26 lg/g of seed in L. usitatissimum subsp. angustifolium to 72 lg/g of seed in L. usitatissimum subsp. usitatissimum var pekinense (Velasco and Goffman, 2000). 3. Intracellular distribution and antioxidant function Fractionation of Polygonum leaves indicated that PC-8 is mainly, if not exclusively, located in chloroplasts (Dunphy et al., 1966). The identification of tocopherol cyclase (VTE1) as the key enzyme in PC-8 biosynthesis suggested plastoglobules as the primary site of PC-8 formation and its localization within chloroplasts (Sattler et al., 2003; Vidi et al., 2006). As the content of plastoglobules is in equilibrium with thylakoid membranes (Austin et al., 2006), it can be assumed that PC-8 is also found in thylakoids where it fulfills an antioxidant function (Zbierzak et al., 2010). In wild-type Arabidopsis plants, a large fraction of plastid PC-8 was located in plastoglobules with most of the remaining fraction more

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J. Kruk et al. / Phytochemistry xxx (2014) xxx–xxx

Table 3 Occurrence of plastochromanol-8 (PC-8) in various organs of higher plant species and under different climatic conditions. The amounts of PC-8 are given in absolute amounts and as a percentage of total tocochromanols. DW, dry weight; FW, fresh weight; ND, not detected; a-T, a-tocopherol; NQ, not quantified. Organs

PC-8 (lg/g FW or DW⁄)

PC-8 (%)

References

Arabidopsis thaliana (young leaves, low light) Arabidopsis thaliana (young leaves, strong light) Arabidopsis thaliana (old leaves, low light) Arabidopsis thaliana (old leaves, strong light) Brassica napus buds Brassica napus flowers Brassica napus pods Brassica napus seeds Brassica napus leaves during stem formation Brassica napus leaves during blooming Brassica napus leaves during seed formation Dioscorea alata (tuber)

2 3 2 2 2⁄ 1⁄ 2⁄ 4⁄ 9⁄ 1⁄ 1⁄ NQ

17 12 25 6 2 11 46 13 18 3 2 NQ

Szyman´ska and Kruk, 2010a Szyman´ska and Kruk, 2010a Szyman´ska and Kruk, 2010a Szyman´ska and Kruk, 2010a Nogala-Kalucka et al., 2002 Nogala-Kałucka et al., 2002 Nogala-Kałucka et al., 2002 Nogala-Kałucka et al., 2002 Nogala-Kałucka et al., 2002 Nogala-Kałucka et al., 2002 Nogala-Kałucka et al., 2002 Cheng et al., 2007

An asterisk indicates values are given on a DW basis.

associated with thylakoids and a very small quantity in the envelope membranes. However, when VTE1 was over-expressed, PC-8 levels in thylakoids increased (Zbierzak et al., 2010). Fractionation of Arabidopsis chloroplasts revealed that PC-8 is fairly evenly distributed between plastoglobules and thylakoids, accounting for 80% of the prenyllipids identified in plastoglobules (Szyman´ska and Kruk, 2010a). Within thylakoid membranes, PC-8 is believed to be mainly located among the antioxidant prenyllipids as it is considerably more hydrophobic than tocopherols are; even more than plastoquinol is. Although the structural relationship of PC-8 with tocopherols and tocotrienols was evident when it was discovered, research into its antioxidant properties began relatively late. The earliest data came from experiments to quantify PC-8 inhibition of lard oxidation where it was found to be 50% more efficient than a-tocopherol (Olejnik et al., 1997). Comparative analysis of the singlet oxygen scavenging activity of PC-8 and other prenyllipids in organic solvents (Gruszka et al., 2008) revealed that the activity of PC-8 is similar to that of c-tocopherol and c-tocotrienol in a polar solvent (acetonitrile) but higher than that of plastoquinol or ubiquinol; while in a hydrophobic environment (carbon tetrachloride) its activity was considerably higher than that of either tocochromanol. Since tocopherols, tocotrienols and PC-8 share the same chromanol ring, these data indicate that as well as the chromanol ring, the more unsaturated side chain of PC-8 provides additional quenching properties. Among the oxidation products of PC-8 as a result of (chemical) scavenging, oxidation derivatives of both the chromanol ring and the side chain (hydroxy-plastochromanol) were identified (Gruszka et al., 2008, Fig. 2). Furthermore, PC-8 was also found to be the most efficient and versatile inhibitor of lipid peroxidation in vitro (Nowicka et al., 2013). When lipid peroxidation of liposomes was initiated in the water phase, PC-8 and tocopherols inhibited the propagation of lipid peroxidation more efficiently than other prenylquinols. However, if the peroxidation was initiated within the hydrophobic interior of liposome membranes, PC-8 and plastoquinol were more efficient inhibitors than tocopherols. It was also found that PC-8 was one of the most active inhibitors of singlet oxygen-mediated lipid peroxidation (Nowicka et al., 2013). During strong light stress, plants respond to elevated production of reactive oxygen species by synthesis of prenyllipids and other water-soluble antioxidants. During acclimation of Arabidopsis to strong light, a-tocopherol and plastoquinol levels increased several fold, while PC-8 only increased in young leaves of both the wild type and the vte4 mutant (Szyman´ska and Kruk, 2010a). Meanwhile, PC-8 content increased considerably during aging of Arabidopsis, reaching more than 50% of a-tocopherol and total plastoquinone in 3-month-old plants. PC-8 was also found in seeds, at nearly 10% of the amount of tocopherols. It was later found that

during strong light acclimation, in both younger and older leaves, hydroxy-plastochromanol (PC-OH) is formed in large amounts (Szyman´ska and Kruk, 2010b). This product was found in vitro to be formed specifically due to the action of singlet oxygen (Szyman´ska et al., 2014), so its level in leaves could be an indicator of singlet oxygen stress. However, neither PC-8 nor PC-OH accumulated during short-term excess light stress, even in D2Oinfiltrated leaves, but only during long-term less pronounced generation of singlet oxygen (Szyman´ska et al., 2014). Both PC-8 and its hydroxyl-derivative were found to be accumulated during Arabidopsis development, as is a-tocopherol, and this accumulation was proportional to the growth light intensity (Szyman´ska et al., 2014). Although the vte1 mutant of Arabidopsis, deficient in tocopherols and PC-8, is supposed to exhibit enhanced production of singlet oxygen, this was only recently demonstrated directly using a singlet oxygen spin-trap and electron paramagnetic spectroscopy (Rastogi et al., 2014). Under strong light, more singlet oxygen was produced by isolated chloroplasts than in the case of wild-type Arabidopsis. Moreover, formation of the lipid peroxidation product malondialdehyde was enhanced in vte1 mutants under strong light. These data indicate that both PC-8 and tocopherols act as efficient singlet oxygen scavengers in vivo and protect membrane lipids against photo-oxidative damage in Arabidopsis leaves. Furthermore, together with tocopherols, PC-8 protects polyunsaturated fatty acids from oxidation during seed desiccation and quiescence (Sattler et al., 2004). The presence of PC-8 in the vte2-1 mutant, which does not accumulate tocopherols, delays the initiation and amplification of lipid oxidation during seed quiescence (Mène-Saffrané et al., 2010). Therefore, both tocopherols and PC-8 exert a protective role against oxidative stress in seeds. 4. PC-8 biosynthesis and its regulation With the finding that the Arabidopsis vte1 mutant, deficient in tocopherol cyclase, lacks PC-8, it became evident that the cyclase is involved in PC-8 synthesis from plastoquinol. An indication that the cyclase was involved in PC-8 synthesis from plastoquinol had come earlier from the observation of increased PC-8 levels in seeds of transgenic B. napus plants overexpressing the VTE1 gene (Kumar et al., 2005). Tocopherol cyclase was originally thought only to be responsible for cyclization of d- and c-tocopherol precursors. However, the enzyme’s involvement in an analogous reaction during the synthesis of tocotrienols and tocomonoenols (Kruk et al., 2011) implied that it is not strictly specific for substrates with a phytol side chain, but also accepts unsaturated substrates. Studies of the substrate specificity of tocopherol cyclase performed using purified enzyme and intact spheroplasts from the cyanobacterium

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J. Kruk et al. / Phytochemistry xxx (2014) xxx–xxx

Table 4 Occurrence of plastochromanol-8 (PC-8) in seeds (A) and the seed oil (B) of several higher plant species. The amounts of PC-8 are given in absolute amounts (lg/g of seed or lg/g of oil) and as a percentage of total tocochromanols. DW, dry weight; FW, fresh weight; ND, not detected. Note that PC-8 has also been detected, although not at quantifiable levels, in seeds of Colutea melanocalyx, Hedysarum cappadocicum, Isatis cappadocia, Isatis kotschyana, Isatis candolleana, Isatis spectabilis, Isatis kozlowskyii, Isatis galusa, Lathyrus inconscpicuus, Lathyrus laxiflorus, Onobrychis major, Pinus nigra, Onobrychis major, Trigonella cretica and Vicia cappadocica (Bagci and Karaagaçli, 2004; Bagci et al., 2004; Bagci and Özçelik, 2009). PC-8 (lg/g)

PC-8 (%)

References

(A) Seeds Linum altaicum Linum austriacum Linum decumbens Linum grandiflorum Linum komarovii Linum leonii Linum lewisii Linum macrorhyzum Linum mesostylum Linum narbonense Linum pallescens Linum perenne Linum usitatissimum subsp. angustifolium Linum stelleroides Linum suffrutisocum

7 7 9 7 5 5 6 11 10 13 8 6 26 8 40

6 7 11 7 4 7 4 11 8 9 6 5 25 0.8 29

Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco Velasco

(B) Seed oils Achras sapota Aesculus sinensis Amaranthus mangostanus Antethum graveolems Arachis hypogaea Basella rubra Brassica campestris Brassica chinensis Brassica juncea Brassica napus Brassica oleracea Camelina sativa Canavalia ensiformis Cannabis sativa ‘‘Beniko’’ Cannabis sativa ‘‘Gluchivski-33’’ Capparis ovata Capparis spinosa Carthamus tinctorius Chaenomeles japonica Connarus paniculatus Corchorus olitorius Corylus avellana Cucumis sativus Cucurbita pepo Erythrophleum fordii Helianthus annuus Hibiscus sabdariffa Hippophae rhamnoides Juglans regia Linum usitatissimum ‘‘oleofarm’’ Linum usitatissimum Nicandra physaloides Oenothera biennis Olea europea Oryza sativa Papaver somniferum Perilla frutescens Plukenetia volubilis Raphanus sativus Ricinus communis Salvia hispanica Schizonepeta tenuifolia Silybum marianum Solanum melongena Vitis vinifera Zea mays

32 69 36 45 19 32 56 34 46 8–90 64 15–43 52 4 1 22 10 1.2 21.6 76 109 0.1 16 0.5 167 2 36 30 0.4 179 191 7 1 5 1 1.1 10 5 20 1 2 33 2 34 13 17

33 24 5 29 8 7 10 6 10 1–24 17 2–9 6 2 0.6 0.5 0.2 0.3 3 16 6 0.03 2 0.2 20 0.4 10 1 0.1 62 34 22 0.4 9 0.4 0.6 1 0.8 4 0.2 0.5 5 0.9 6.8 3 1

Matthäus et al., 2003 Matthäus et al., 2003 Matthäus et al., 2003 Matthäus et al., 2003 Gruszka and Kruk, 2007 Matthäus et al., 2003 Matthäus et al., 2003 Matthäus et al., 2003 Matthäus et al., 2003 Gruszka and Kruk, 2007; Kumar et al., 2005 Matthäus et al., 2003 Gruszka and Kruk, 2007 Matthäus et al., 2003 Kriese et al., 2004 Kriese et al., 2004 Matthäus and Özcan, 2005 Matthäus and Özcan, 2005 Gruszka and Kruk, 2007 Gornás et al., 2013 Matthäus et al., 2003 Matthäus et al., 2003 Gruszka and Kruk, 2007 Matthäus et al., 2003 Gruszka and Kruk, 2007 Matthäus et al.,2003 Gruszka and Kruk, 2007 Matthäus et al., 2003 George and Cenkowski, 2007 Gruszka and Kruk, 2007 Gruszka and Kruk, 2007 Ciftci et al., 2012 SOFA Database Gruszka and Kruk, 2007 Gruszka and Kruk, 2007 Gruszka and Kruk, 2007 Gruszka and Kruk, 2007 Ciftci et al., 2012 SOFA Database Matthaus et al., 2003 Gruszka and Kruk, 2007 Ciftci et al., 2012 Matthäus et al., 2003 Gruszka and Kruk, 2007 Matthäus et al., 2003 Gruszka and Kruk, 2007 Gruszka and Kruk, 2007

Anabaena variabilis (Stocker et al., 1996) demonstrated that the enzyme converts substrates having different numbers of methyl groups in their chromanol ring and both saturated and unsaturated side chains. However, the substrate must have free hydroxyl groups in its ring. The enzyme recognizes the chiral configuration

and and and and and and and and and and and and and and and

Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman, Goffman,

2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000 2000

of the side chain, thus its highest preference was for the natural phytol stereoisomer. Among the substrates analyzed with unsaturated side chains of different lengths (plastoquinols with 2–4 isoprenoid units), the highest yield was observed for the substrate with 4 units (83%) followed by that for the substrate with 3 units

Please cite this article in press as: Kruk, J., et al. Plastochromanol-8: Fifty years of research. Phytochemistry (2014), http://dx.doi.org/10.1016/ j.phytochem.2014.09.011

J. Kruk et al. / Phytochemistry xxx (2014) xxx–xxx

Fig. 2. Chemical structure of hydroxy-plastochromanol (PC-OH) and plastochromenol-8.

(14%), while plastoquinol-2 was not converted to the chromanol form. Furthermore, the enzyme is also capable of forming tocotrienols (Porfirova et al., 2002). The level of PC-8 is also regulated by other enzymes found in plastoglobules, such as NDC1 (NADPH-dependent quinone dehydrogenase C1) (Piller et al., 2012) and ABC1-like kinase ABC1K3 (Martinis et al., 2013). NDC1 is involved in the reduction of oxidized plastoquinone to plastoquinol, thus recycling plastoquinol that might oxidize during strong light stress. In fact, the ndc1 mutant had a significantly higher percentage of oxidized plastoquinone than the wild type (Piller et al., 2012). Moreover, the PC-8 level was lower in the mutant, which is most probably the result of a decreased level of plastoquinol, the substrate of the cyclase. It has been predicted that a kinase in the plastoglobules, named ABC1 kinase, acts on the VTE1 in the plastoglobules. The levels of PC-8 were about fourfold lower in the abc1k3 mutant than in the wild type and did not change significantly after strong light exposure (Martinis et al., 2013). In contrast, the level of tocopherols was not affected in the mutant. This indicates that VTE1 activity is a limiting factor for PC-8 but not for tocopherol synthesis. However, levels of plastoquinol were not analyzed and it cannot be ruled out that the mutation also affects them. It was hypothesized that phosphorylation stabilizes VTE1 in the plastoglobules. It is possible that phosphorylation of the enzyme increases its activity on plastoquinol through conformational changes and a deeper location within the plastoglobules. Interesting data come from the analysis of solanesyl-diphosphate synthase, that forms the side chain of plastoquinol/PC-8 (Fig. 1), which is encoded in Arabidopsis by two genes atsps1 and atsps2; the latter mainly contributes to plastoquinol biosynthetic flux (Block et al., 2013). The level of PC-8 in leaves was approximately 35% lower in the atsps1 mutant than in wild-type controls; while PC-8 was not detected in atsps2 plants. At the same time, the content of plastoquinone in the atsps1 mutant was similar to that in the wild type but only about 50% in the atsps2 plants. These and other data (Block et al., 2013) suggest that PC-8 synthesis is restricted to the non-photoactive pool of plastoquinol that resides in the plastoglobules. A decrease in the content of plastoquinol in the plastoglobules strongly affects PC-8 synthesis, probably due to marked decrease in the number of substrate molecules available at the plastoglobule surface for the enzyme to act on. It was recently found that AtSIA1 and AtOSA1 proteins, mainly associated with thylakoids and envelope membranes, respectively, participate in the regulation of iron distribution within chloroplasts (Manara et al., 2014). Both the single atsia1 and atosa1 mutants as well as the double mutant showed several-fold increases in PC-8 levels, while the total plastoquinone level was only slightly affected in these mutants. The a-tocopherol content

5

was only elevated in the atsia1 plants. These data indicate that both the kinases may play a role in the biosynthesis of prenylquinones; they probably do not participate directly in the biosynthesis of prenylquinones, however, but act as regulators (Manara et al., 2014). An interesting study, although one that requires verification, concerns the effect of the photoperiod on c-tocopherol and PC-8 levels in leaves of Xanthium struminarium (Battle et al., 1976). It was found that in contrast to a-tocopherol levels, but similar to those of c-tocopherol, the content of PC-8 undergoes significant diurnal changes both in photoperiodically induced and vegetative leaves of this species; its level increased considerably at the end of the dark period. An unresolved and intriguing question regarding the substrate specificity of this cyclase is why PC-8 is not found in cyanobacteria that synthesize tocopherols (Kruk, unpublished). The possibility that the enzyme in these organisms is strictly specific for tocopherol precursors was not confirmed using purified cyclase and membrane fragments (spheroplasts) from A. variabilis (Stocker et al., 1996). The other, more probable reason would be that cyanobacteria do not form plastoglobules, in contrast to higher plants, and therefore the cyclase must be located in a different chloroplast/cell compartment such as thylakoid or the cell/chloroplast membrane. Plastoquinol is believed to be relatively deeply located in the hydrophobic interior of the membrane and therefore it might not be accessible to the enzyme.

5. Hydroxy-plastochromanol and other PC-8 metabolites Hydroxy-plastochromanol (PC-OH) was identified in Arabidopsis by comparative analysis of leaf extracts from the wild type and the vte1 mutant using fluorescence detection in HPLC (Szyman´ska and Kruk, 2010b). It was suggested that this compound is the non-enzymatic product of the singlet oxygen scavenging activity of PC-8 that was previously identified in vitro as the main product of the reaction (Gruszka et al., 2008). Its level increased in Arabidopsis leaves under strong light stress both in older and younger leaves of the rosettes and especially during the aging of Arabidopsis; it exceeded the content of PC-8 in both cases (Szyman´ska and Kruk, 2010b). In vitro studies revealed that PC-OH is only formed from PC-8 as a result of the action of singlet oxygen and not by other radicals that can be found in biological systems (Szyman´ska et al., 2014). This indicates that PC-OH is formed in vivo specifically upon the action of singlet oxygen and that this prenyllipid can therefore be an indicator of singlet oxygen stress. As a result of a non-enzymatic reaction, singlet oxygen can oxidize any of the 8 double bonds in the side chain of PC-8 and as a consequence at least 8 isomers of PC-OH can be expected. Indeed, when the PC-OH fraction corresponding to one band in reverse-phase HPLC was run under normal-phase conditions, at least 8 bands were evident; they correspond to individual isomers of PC-OH differing in the position of the hydroxyl group on the side chain. All the isomers should have antioxidant properties similar to those of PC-8; however, their location within membranes should be closer to the membrane interface the more polar the oxidized side chain is. Within chloroplasts, PC-OH was found both in plastoglobules (80%) and thylakoids (20%), similar to PC-8 localization (Szyman´ska and Kruk, 2010a). In contrast to the case of leaves, PC-OH was not found in Arabidopsis seeds (Szyman´ska and Kruk, 2010a). This confirms the suggestion that singlet oxygen is required for the formation of this compound, as it is produced only under light conditions. In Arabidopsis leaves, PC-OH accumulates under both very low and strong light conditions, and mainly during long-term, less pronounced generation of singlet oxygen (Szyman´ska et al., 2014). Under

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Fig. 3. Scavenging of singlet oxygen by plastochromanol-8 (A) and chemical structure of compounds involved (B).

strong light (400 lmol photons/m2/s) after 3 days, the PC-OH level increased, as did that of other prenyllipids; while under short-term illumination under excess light (2000 lE/m2/s), in both water and D2O, its level gradually decreased in the wild type, as well as in vte4 and vte2 mutants. This suggests that under excess light conditions, PC-OH is oxidized further by singlet oxygen to other products (Fig. 3). Such compounds could include: trihydroxy-PC-8, which was found among PC-8 oxidation products in vitro (Gruszka et al., 2008); quinone forms of PC-8 and PC-OH, corre-

sponding to a-tocopherolquinone, an oxidation product of atocopherol that was identified in many species (Szymanska and Kruk, 2008); or fatty esters of PC-OH, corresponding to plastoquinone-B (Kruk et al., 1998). Among further derivatives of PC-8, fatty acid esters of the hydroxyl group on the chromanol ring of PC-8 were found in latex from H. brasiliensis (Dunphy et al., 1966) as well as tocotrienol esters and free tocotrienols (Dunphy et al., 1965), and their presence in other plant species cannot be ruled out.

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Before PC-8 was discovered in leaves of Hevea (Whittle et al., 1965), solanachromene (plastochromenol-8), an unsaturated analogue with a double bond in the heterocyclic ring of the chromanol moiety (Fig. 2), was detected in aged flue-cured tobacco leaves. It was quantified as 0.05% of the dry weight (Rowland, 1958), exceeding that of a-tocopherol and that of PC-8 considerably (Dunphy et al., 1966). However, it is not certain whether this compound is a natural product or a curing artifact; and its biosynthetic relation to PC-8 remains unclear. It was recently found that a-tocopherol can be recycled from a-tocopherolquinone via a-tocopherolquinol and a hypothetical dehydratase is also required in this process to form trimethylbenzoquinol, which would be converted by tocopherol cyclase to a-tocopherol (Kobayashi and DellaPenna, 2008). A similar redox cycle could also occur in the case of PC-8 (Fig. 3). 6. Conclusions and perspectives Interest in PC-8 has increased over recent years, but many questions are still not clearly answered. Although the studies performed to date suggest that PC-8 is widespread within the plant kingdom, more research is required to establish its distribution, including studies of several other taxonomic groups. Its role and behavior under stress conditions remain poorly understood and further research is needed to reveal its exact location in plant cells and tissues. PC-8 has antioxidant functions that are mainly related to preventing photo-oxidative damage in leaves and oxidation processes in seeds; but we have incomplete knowledge of its response to stress factors such as salt and drought in both leaves and seeds. Another important issue that deserves further attention is the absence of PC-8 and the subcellular location of VTE1 in cyanobacteria. Acknowledgments Work in J.K. lab is supported by grant 2011/01/B/NZ1/00079 from the National Center of Science of Poland. Work in S.M.-B. lab is supported by grant BFU2012-32057 from the Spanish Government. References Austin, J.R., Frost, E., Vidi, P.A., Kessler, F., Staehlin, L.A., 2006. Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18, 1693–1703. Bagci, E., Bruehl, L., Özçelik, H., Aitzetmuller, K., Vural, M., Sahim, A., 2004. A study of the fatty acid and tocochromanol patterns of some Fabaceae (Leguminosae) plants from Turkey I. Grasas Aceites 378, 378–384. Bagci, E., Karaagaçli, Y., 2004. Fatty acid and tocochromanol patterns of Turkish pines. Acta Biol. Cracov. 46, 95–100. Bagci, E., Ozcelik, H., 2009. Fatty acid and tocochromanol patterns of some Isatis L. (Brassicaceae) species from Turkey. Pak. J. Bot. 41, 639–646. Battle, R.W., Gaunt, J.K., Laidman, D.L., 1976. The effect of photoperiod on endogenous c-tocopherol and plastochromanol in leaves of Xanthium struminarium L. (Cocklebur). Biochem. Soc. Trans. 4, 484–486. Block, A., Fristedt, R., Rogers, S., Kumar, J., Barnes, B., Barnes, J., Elowsky, J.G., Wamboldt, Y., Mackenzie, S.A., Redding, K., Merchant, S.S., Basset, J.G., 2013. Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids. J. Biol. Chem. 288, 27594–27606. Ciftci, O.N., Przybylski, R., Rudzinska, M., 2012. Lipid components of flax, perilla, and chia seeds. Eur. J. Lipid Sci. Technol. 114, 794–800. Cheng, W.Y., Kuo, Y.H., Huang, C.J., 2007. Isolation and identification of novel estrogenic compounds in yam tuber (Dioscorea alata Cv. Tainung No. 2). J. Agric. Food Chem. 55, 7350–7358. Dunphy, P.J., Whittle, K.J., Pennock, J.F., Morton, R.A., 1965. Identification and estimation of tocotrienols in Hevea latex. Nature 207, 521–522. Dunphy, P.J., Whittle, K.J., Pennock, J.F., 1966. Plastochromanol. In: Goodwin, T.W. (Ed.), Biochemistry of Chloroplasts. Academic Press, London, pp. 165–171. Falk, J., Munné-Bosch, S., 2010. Tocochromanol functions in plants: antioxidation and beyond. J. Exp. Bot. 61, 1549–1566.

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Plastochromanol-8: fifty years of research.

Plastochromanol-8 (PC-8) is an antioxidant that, together with tocopherols and tocotrienols, belongs to the group of tocochromanols. Plastochromanol-8...
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