JXB Advance Access published online on November 26, 2008
Journal of Experimental Botany, doi:10.1093/jxb/ern297
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OPINION PAPER |
Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging?
1Laboratory for Molecular Plant Physiology, KU Leuven, Kasteelpark Arenberg 31, B-3001 Leuven, Belgium
2Institute for Crop Production and Grassland Research, University of Hohenheim, D-70599 Stuttgart, Germany
* To whom correspondence should be addressed. E-mail: wim.vandenende{at}bio.kuleuven.be
Received 25 September 2008; Revised 20 October 2008 Accepted 23 October 2008
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Abstract |
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 Top Abstract IntroductionSOS: a role in...Links between oxidative stress...Conclusions and perspectivesReferences |
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In nature, no single plant completes its life cycle without encountering environmental stress. When plant cells surpass stress threshold stimuli, chemically reactive oxygen species (ROS) are generated that can cause oxidative damage or act as signals. Plants have developed numerous ROS-scavenging systems to minimize the cytotoxic effects of ROS. The role of sucrosyl oligosaccharides (SOS), including fructans and the raffinose family oligosaccharides (RFOs), is well established during stress physiology. They are believed to act as important membrane protectors in planta. So far a putative role for sucrose and SOS during oxidative stress has largely been neglected, as has the contribution of the vacuolar compartment. Recent studies suggest a link between SOS and oxidative defence and/or scavenging. SOS might be involved in stabilizing membrane-associated peroxidases and NADPH oxidases, and SOS-derived radicals might fulfil an intermediate role in oxido-reduction reactions taking place in the vicinity of membranes. Here, these emerging features are discussed and perspectives for future research are provided.
Key words: Fructan, oxidative stress, raffinose, ROS, sucrose, sucrosyl oligosaccharides
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Introduction |
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TopAbstractIntroductionSOS: a role in...Links between oxidative stress...Conclusions and perspectivesReferences |
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Plant cells are challenged with hyperactive compounds derived from oxygen, the so-called reactive oxygen species (ROS) (Mittler et al., 2004; Couée et al., 2006). ROS include singlet oxygen (1O2), superoxide oxygen (O2·–), hydroxyl radical (OH·), and hydrogen peroxide (H2O2), generated as by-products of photosynthesis and respiration (Mittler et al., 2004). ROS production is directly connected to many metabolic processes in various subcellular compartments, especially chloroplasts, peroxisomes, and mitochondria (Fig. 1) (Bartoli et al., 2004).
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Chloroplasts and peroxisomes are the major ROS generators under excess light (Asada, 2006). It has been estimated that under normal physiological conditions, chloroplasts can generate
150–250 µmol of H2O2 mg–1 chlorophyll h–1 (Wang and Song, 2008). Mitochondria can produce O2·– in the dark (Bartoli et al., 2004; Møller et al., 2007), rapidly inducing mitochondrial morphology transitions and leading to cell death (Scott and Logan, 2008). In addition, NADPH oxidases release ROS in the apoplast (Bolwell et al., 2002). The participation of the vacuole in oxidative stress has been totally neglected by most authors, but not by all (Mittler et al., 2004). However, it should be realized that vacuoles occupy >95% of the cell volume in many plant cells. Moreover, the vacuole/tonoplast shows unusual structural adaptations under stress, triggering several stress-defensive mechanisms (Valluru et al., 2008). Accordingly, vacuoles accumulate a mixture of strong antioxidant compounds (anthocyanins, phenolics, malate etc.; Kytridis and Manetas, 2006), probably fulfilling unanticipated roles in redox buffering.
ROS production can be accelerated by various environmental stresses, leading to lipid peroxidation and photo-oxidative damage (Murata et al., 2007; Takahashi and Murata, 2008). These stresses have different effects on antioxidants (Kellos et al., 2008). Stress stimuli can reduce CO2 fixation, and impair net consumption of ATP and NADPH, generating singlet oxygen and causing photodamage to photosystem II (PSII; Hideg et al., 2002). The increase in ROS concentration, in turn, activates antioxidants as well (Foyer and Noctor, 2005). Interestingly, stress stimuli seem to accelerate the photodamage to PSII by inhibiting its repair (Nishiyama et al., 2006; Murata et al., 2007; Takahashi and Murata, 2008). However, due to their sessile lifestyle, plants have developed a plethora of mechanisms to minimize oxidative damage under stress (see below).
In addition to well-known antioxidants, antioxidative defence systems and proteasome-dependent proteolytic systems (Møller et al., 2007; Xiong et al., 2007), small water-soluble sugars such as glucose and sucrose are now recognized as crucial compounds in coordinating plant developmental responses under oxidative stresses. In addition, other important water-soluble carbohydrates derived from sucrose [sucrosyl oligosaccharides (SOS)] include raffinose family oligosaccharides (RFOs) and fructans. As well as their role as sources of carbon and energy, which can back up growth and development during impaired metabolic activity, SOS have been assigned versatile regulatory functions at both the cellular and whole-organism level by controlling cellular metabolism, growth and development, and stress resistance of plants (Nishizawa et al., 2008; Valluru and Van den Ende, 2008).
SOS and the enzymes associated with their metabolism might interact in indirect ways with ROS signalling pathways. Indeed, small soluble sugars and the enzymes associated with their metabolic pathways are widely believed to be connected to oxidative stress and ROS signalling pathways (Couée et al., 2006; Sulmon et al., 2006; Suzuki and Mittler, 2006; Takahashi and Murata, 2008). Furthermore, it cannot be excluded that fructans and RFOs themselves might act as signals in pathways associated with stress tolerance (Van den Ende et al., 2004).
Here, the putative direct roles of SOS as primary ROS scavengers in the vicinity of cellular membranes, in close association with other key role players in antioxidative defence systems, are discussed. The modulating effects of fructans and RFOs are consistent with many observations scattered throughout the literature.
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SOS: a role in stress physiology |
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Raffinose, a
-galactosyl extension of sucrose, is nearly ubiquitous in plants (Keller and Pharr, 1996). The smallest RFOs, raffinose and stachyose, are synthesized in the cytoplasm. Both depend on galactinol [-D-Gal-(1
1)-L-myo-inositol], the product of galactinol synthase (GolS). Raffinose synthase (RafS) catalyses the reversible transfer of a galactosyl unit from galactinol (donor substrate) to sucrose (acceptor substrate) (Lehle and Tanner, 1973). Subsequently, raffinose is used as an acceptor in the galactinol-dependent stachyose biosynthetic reaction catalysed by stachyose synthase (Peterbauer et al., 1998). In contrast, the syntheses of the higher DP (degree of polymerization) RFOs (>DP 4) are galactinol independent. The enzyme galactan:galactan galactosyltransferase (GGT) catalyses the direct transfer of a terminal galactosyl residue from one RFO molecule to another, resulting in the next higher and lower RFO oligomers, respectively (Haab and Keller, 2002; Tapernoux-Luthi et al., 2004).
Fructans are sucrose-derived fructose polymers occurring in 15% of flowering plants (Hendry, 1993) as well as in a wide range of bacteria and fungi (Martinez-Fleites et al., 2005). Fructans are believed to be synthesized in the central vacuole (Frehner et al., 1994), but an involvement of pre-vacuolar vesicles cannot be excluded (Kaeser 1983). Fructan biosynthesis is initiated by sucrose:sucrose 1-fructosyltransferase (1-SST), donating a fructosyl moiety from one sucrose to another (Edelman and Jefford, 1968; Van den Ende and Van Laere, 1996). This process yields the trisaccharide 1-kestose, the simplest inulin with β(2,1)-linkages, which can be elongated further by adding β(2,1)- and/or β(2,6)-linked fructosyl moieties by other fructosyl transferase (FT) enzymes such as 1-FFT, 6G-FFT, and 6-SFT. Depolymerization of fructans is executed by fructan exohydrolases (FEHs). Different types of FEHs (1-FEH, 6-FEH, 6-KEH, and 6&1-FEH) have recently been described in fructan- and non-fructan-containing plants (De Coninck et al., 2007; Van Riet et al., 2008).
Fructans fulfil protective physiological roles in plants (Hendry, 1993; Morvan-Bertrand et al., 2001; Le Roy et al., 2007). During stresses, fructans can strongly interact with cell membranes through direct hydrogen bonding (Hincha et al., 2000, 2003). The surface-active effects of both inulin- and levan-type fructans contrast strongly with the maximal effects observed for trehalose, sucrose, and glucose. Inulin-type fructans show a deep interaction with membranes compared with levan-type fructans due to their variable molecular weight (Hinrichs et al., 2001) and flexible random coil structures (Vereyken et al., 2003). Fructans prevent lipid condensation and cessation of the phase transition by reducing the molecular motions of the lipid head groups (Vereyken et al., 2003). RFOs fulfil similar physiological roles in plants, and were shown to be involved in desiccation tolerance in seeds (Keller and Pharr, 1996). Both RFOs and fructans are believed to protect biological membranes under stress (Hincha et al., 2002, 2003).
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Links between oxidative stress and carbon metabolism |
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ROS and sugar signalling: a delicate balance
Soluble sugars such as glucose and sucrose have long been considered to play versatile roles in plants (Rolland et al., 2006). Recently, the remodelling of carbon metabolism in Arabidopsis is interpreted as an emergency strategy under oxidative stress (Scarpeci and Valle, 2008). Higher photosynthetic activity induces both the generation of ROS and massive accumulation of soluble sugars. Therefore, sugars themselves might be effective candidates for the oxidative burst in tissues exposed to a wide range of environmental stresses.
Endogenous sugar availability can feed the oxidative-pentose phosphate pathway (OPP; Debnam et al., 2004; Couée et al., 2006), which can trigger ROS scavenging. Glucose 6-phosphate dehydrogenase (G6PDH), catalysing the first reaction in the OPP pathway, has been postulated to affect the redox poise of the chloroplast as well as the capacity to detoxify ROS (Debnam et al., 2004). Sugars can replenish NADPH, needed for monodehydroascorbate reductase (MDAR) and glutathione reductase (GR) (Nishikawa et al., 2005). The effects of soluble sugars on gene expression are mediated through sugar-specific signalling pathways (Couée et al., 2006). Interestingly, the responses to sugars and oxidative stress are not only co-linked, but also affect scores of stress-responsive genes (Price et al., 2004). Moreover, sugar availability can enhance ascorbate (ASC) biosynthesis (Nishikawa et al., 2005), perhaps due to the enhanced rate of respiration (Millar et al. 2003).
Conclusively, so far the protective effects of soluble sugars related to oxidative stress have been considered as indirect effects of sugar signalling, triggering the production of specific ROS scavengers.
Sucrose: an underestimated antioxidant capacity against ROS?
In vitro studies demonstrated that the ID50 values (the concentration of a compound required to inhibit OH·-catalysed hydroxylation of salicylate by 50% of the maximum yield observed in the absence of the compound) for galactinol (3.1 mM) and raffinose (2.9 mM) are similar to that of glutathione (GSH) (3.0 mM) and smaller than that of ASC (16.4 mM: Nishizawa et al., 2008), two classical antioxidants. Strikingly, when compared with other sugars, the strongest antioxidant capability was detected for sucrose (ID50: 2.7 mM), in line with earlier observations (Smirnoff and Cumbes, 1989). OH· are highly reactive radicals, which retrieve H· from virtually any organic compound to form water. In sugars, OH· preferentially attack HO–C–H linkages (Morelli et al., 2003). Accordingly, when sugars are compared at the same molar concentration, their free radical-scavenging capacity is strongly correlated with their total number of hydroxyl groups, explaining why sucrose (eight OH groups) is better compared with glucose and fructose (five OH groups). In a similar vein, lower DP fructans as soluble polyhydroxy compounds might be even more efficient in radical quenching (see Fig. 2). The identity of the liberated oxidized sucrose free radicals (OSFRs) might be diverse, and their exact nature and stability deserve further investigation. However, OSFRs are slower reacting radicals compared with OH· radicals and seem to undergo several possible reactions to form more stable non-radical compounds or, alternatively, to regain their reduced forms (Green, 1980; Gray and Mower, 1991).
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These in vitro studies convincingly demonstrate the ROS-scavenging capacity of sucrose, strongly suggesting that similar reactions can also occur in planta. At low concentrations, sucrose might serve as a substrate or signal for stress-induced alterations, while at high concentrations it can function directly as a protective agent (Uemura and Steponkus, 2003). The mechanism of OH· scavenging might be linked to the presence of stable OSFRs. However, these sugar radicals may easily regenerate in vivo (see later), providing higher stability of the sucrose and a more efficient quenching of the OH·. These processes might be of particular importance in vacuoles of sugar-accumulating tissues such as sugar beet and sugar cane, in phloem-associated tissues, or in any cells with enhanced sucrose concentrations.
So far, sucrose has not been recognized as an antioxidant compound. One of the reasons for this is the fact that so far research efforts have been almost entirely focused on Arabidopsis. Quite exceptionally, when compared with most other plants, Arabidopsis contains very low sucrose concentrations that cannot be substantially elevated under mild stress conditions (own unpublished observations), suggesting that the sucrose concentration is rather strictly controlled in this species. Instead, Arabidopsis rapidly diverts excess carbon to RFOs (Klotke et al., 2004) and/or to starch (Mita et al., 1995).
ROS and RFOs: a link in Arabidopsis
Recently, RFO sugars as well as galactinol have been proposed to fulfil important roles in oxidative stress defence in plants (Morsy et al., 2007; Nishizawa et al., 2008) and seeds (Buitink et al., 2000; Bailly et al., 2001; Lehner et al., 2006). In Arabidopsis, seven genes belonging to the GolS family were identified, among these, GolS1 and 2 mRNAs were detected in mature seeds that were induced by stresses in leaf tissues, while GolS3 mRNA seems to be induced by cold stress (Panikulangara et al., 2004). Overexpression of GolS1, GolS2, GolS4, and RafS2 in transgenic Arabidopsis increased the galactinol and raffinose concentrations and resulted in effective ROS-scavenging capacity and oxidative stress tolerance (Nishizawa et al., 2008). Concomitantly, the levels of the antioxidants ASC and GSH also increased. Moreover, lipid peroxidation was significantly lower than in wild-type plants (Nishizawa et al., 2008). Further, these transgenic plants exhibited higher PSII activities, compared with wild types, and responded positively to high light and chilling conditions. These results strongly suggest that endogenous galactinol and raffinose can act as antioxidants/osmoprotectants in planta, leading to increased tolerance to oxidative stress (methylviologen treatment).
Chloroplasts generate massive ROS under stress. O2·–, as an initial ROS, is readily converted into OH· and H2O2. This stimulates a battery of antioxidant systems capable of removing ROS from the chloroplasts, such as flavonoids (Agati et al., 2007), and ASC and GSH (Asada, 2006). The accumulation of raffinose in chloroplasts (Santarius and Milde, 1977; Lineberger and Steponkus, 1980; Heber and Heldt, 1981) indicates that raffinose transporters (cf. ASC and GSH transporters; Pignocchi and Foyer, 2003) might exist in chloroplast membranes (Heber and Heldt, 1981) but so far they have not been characterized. Similarly, the question of whether sucrose is present inside plastids has long been debated. Gerrits et al. (2001) have introduced sucrose-metabolizing enzymes into plastids. These experiments suggested substantial sucrose entry into plastids. Previously, raffinose was shown to protect photophosphorylation and electron transport of chloroplast membranes against freezing, desiccation, and high temperature stress (Santarius, 1973), strongly suggesting that chloroplastic RFOs might be operating as ideal ROS scavengers. The oxidized RFO radicals might be regenerated by ASC or other reducing antioxidants such as flavonoids (Agati et al., 2007).
ROS and fructans: a new link?
Mounting evidence has been generated over the last decade that fructans might protect plants against freezing/drought stresses (Hincha et al., 2000, 2003). The putative roles of fructans localized in the vacuole (Kawakami et al., 2008) and in the apoplast (Van den Ende et al., 2005; Valluru et al., 2008) were established, and a role in oxidative stress defence has been proposed (Parvanova et al., 2004). These studies suggest that fructans act directly as ROS scavengers (Fig. 2) or indirectly by stimulating other specific antioxidative defence mechanisms. Interestingly, changes in fructan concentrations showed a close relationship with changes in antioxidant (ASC and GSH) concentrations in immature wheat kernels (De Gara et al., 2003; Paradiso et al., 2006), strongly suggesting a link with well-known antioxidant systems, and may occupy an integral part of a complex ROS-scavenging concept.
So far, fructans are not recognized as ‘typical’ antioxidants in plants. However, hot water extracts of the fructan plants Chlorophytum borivillianum (Govindarajan et al., 2005) and Arctium lappa (edible burdock: Duh, 1998) showed strong antioxidant properties, acting as effective radical scavengers in in vitro tests. Moreover, these extracts showed prominent bioactive properties in animal studies (Kardosova et al., 2003). These data strongly suggest that vacuolar fructans, like vacuolar anthocyanins, could fulfil a role in redox regulation processes.
Since the vacuole harbours both peroxidases (Prx; Mittler, 2002; Sottomayor et al., 2004) and fructans (Frehner et al., 1984), a Prx-dependent oxidation of fructans seems possible in the vacuole of fructan-containing plants. Unlike ASC and phenolic compounds (PCs), fructans and other carbohydrates lack a double bond in their ring structure, which probably prevents them from acting as suitable substrates for Prx or oxidase enzymes. However, carbohydrate oxidase enzymes, oxidizing reducing sugars, have been characterized from fructan-containing plants (Custers et al., 2004), but vacuolar forms that prefer non-reducing carbohydrates such as fructans have not yet been reported. In the absence of such evidence for specific fructan oxidase or Prx enzymes, it seems reasonable to speculate that fructan oxidation could be initiated by O2·–, OH·, and OOH·, retrieving H· to form water and generating oxidized fructan free radicals (OFFRs).
Two mechanisms have been postulated to explain the origin of the initiator radicals in the vacuole, and these two systems are not mutually exclusive (Sottomayor et al., 2004).
The first possibility is the diffusion of excess cytoplasmic H2O2 through the tonoplast. Tonoplastic aquaporins may facilitate H2O2 uptake (Reisen et al., 2003; Bienert et al., 2007). Independent studies on isolated tonoplast fractions have repeatedly demonstrated the presence of membrane-associated Prx or class III peroxidases [barley peroxidase gene (Prx7), Kristensen et al., 2001; Catharanthus roseus peroxidase (CRPrx), Sottomayor and Ros Barcelo, 2003; Arabidopsis thaliana peroxidase (AtPrx34), Zimmermann et al., 2004; Catharanthus roseus peroxidase 1 (CrPrx1), Costa et al., 2008]. Importantly, these peroxidases are localized on the inner face of the tonoplast (Sottomayor et al., 2004), which can readily attack incoming H2O2, generating a blend of ROS (OH· and OOH·) by the hydroxylic cycle of these peroxidases (Passardi et al., 2004; Dunand et al., 2007). At the same time, these radicals might oxidize many vacuolar compounds likely to complement the classical ASC–ascorbate peroxidase (APX) system (Yamasaki and Grace, 1998; Grace and Logan, 2000).
A second possible mechanism of ROS generation involves the action of a tonoplastic NADPH oxidase. These enzymes are considered as major ROS producers in the plasma membrane (PM), but proteomic studies have documented the presence of these enzymes in the tonoplast as well (Carter et al., 2004; Whiteman et al., 2008). Consistently, O2·–, the first product generated by this enzyme, has been detected in the tonoplast (Romero-Puertas et al., 2004). Taken together, it can be hypothesized that a tonoplastic NADPH oxidase might use the cytoplasmic NADPH to transfer electrons across the membrane to form O2·–, as described in lysosomes (Chen, 2002) and phagocytic vacuoles in animal cells (Behe and Segal, 2007). This O2·– could be transformed to the less toxic H2O2 spontaneously or via tonoplast-associated superoxide dismutase (SOD) (Shi et al., 2007).
After generation by membrane-bound oxidases and peroxidases, ROS present a great danger for these membranes (lipid peroxidation). Fructans can protrude deep into membranes (deeper than sucrose) as described (Valluru and Van den Ende, 2008), contributing to membrane stabilization. It is hypothesized that these membrane-associated fructans might also be ideally positioned to react with these radicals, to form OFFRs, in this way preventing lipid peroxidation (Fig. 2). However, these OFFRs might be rapidly reduced again to fructans by the ‘classical’ antioxidant ASC or by other vacuolar antioxidants (PCs and anthocyanins). Such an ‘NADPH oxidase/Prx/fructan/PC’ system within the tonoplast (NADPH oxidase), associated with the inner side of the tonoplast (Prx/fructan/PC), and present in the vacuolar lumen (fructan/PC) could be elegantly linked with the cytoplasmic redox systems (Fig. 2). It may operate as a unique scavenging and salvaging system, preventing lipid degradation, in this way ensuring membrane stabilization and contributing to cell survival by removing excess H2O2 that is formed in or diffused into vacuoles. Indeed, it has been shown that plant cell viability depends on the functional status of the vacuole and intact vesicular trafficking (Surpin and Raikhel, 2004). A similar scavenging system has also been proposed before for phenoxy radicals (Mehlhorn et al., 1996; Takahama, 2004). Recently, a role for trehalose in protection against ROS was also demonstrated (Nery et al., 2008).
Regeneration of OFFRs into fructans might be an important aspect for efficient quenching of ROS. Vacuolar compounds such as flavonoids (e.g. anthocyanins) might be involved in reduction of OFFRs into fructans. Indeed, flavonoids may also act as antioxidants (Kytridis and Manetas, 2006; Pourcel et al., 2007) and a strong correlation was found between flavonoid content and freezing tolerance (Korn et al., 2008). Previous knock-out experiments revealed that raffinose alone could not account for the observed freezing tolerance (Zuther et al., 2004). It is proposed here that perhaps the combination of sugars and (different) flavonoids might be essential to establish freezing tolerance in this species. Indeed, conjugated flavonoid compounds have been shown to have a stronger scavenging effect on ROS than their respective monomers, and thus seem to moderate the pro-oxidant properties of antioxidants (Kang, 2007). As a new concept, it can be hypothesized that both sugars and phenolic compounds form part of an integrated redox system, quenching ROS and contributing to freezing tolerance (see further Fig. 2).
It should be noted that under stress, a tonoplast vesicle-derived exocytosis (TVE) (Valluru et al., 2008) might be operating as an efficient system to carry fructans (and sucrose) from the vacuole to the PM in plants (Fig. 2). A similar vesicular transport from lysosomes to the cell surface was described in animal cells (Wubbolts et al., 1996). Therefore, and perhaps even more importantly, a very similar system involving PM-localized NADPH oxidase and soluble sugars such as fructans (and perhaps Prx: Mika and Lúthje, 2003) might fulfil significant roles in preserving PM stability. Such a system might greatly contribute to stress tolerance and signalling pathways controlling apoplastic H2O2 concentrations, regulating defence responses (Orozco-Cardenas et al., 2001) as well as growth and development by cell wall modifications (Passardi et al., 2004).
The model depicted in Fig. 2 depends on high sucrose concentrations (as a substrate for fructan biosynthesis by FTs), oxygen availability, and on the presence of PCs. Consistent with the present model, much higher fructan levels are generated under hypoxia (Albrecht et al., 2004), to keep OFFR levels high despite the reduced OH· generation. However, the model cannot work under complete anoxia. Indeed, it was found that fructans are totally degraded under these circumstances (Albrecht et al., 2004). Consistent with the model, H2O2 seems to accumulate in vascular tissues such as leaf veins (Fryer et al., 2002; Slesak et al., 2008). Strikingly, phloem-associated tissues typically form a major site of storage for several sugar compounds, including sucrose and fructans (Wang and Nobel, 1998; Van den Ende et al., 2000).
The relevance of the concept might be validated from the studies carried out on transgenic non-fructan tobacco plants carrying FTs (SacB gene, Konstantinova et al., 2002; Parvanova et al., 2004; 1-SST, Li et al., 2007) which showed more resistance to frost. Closer observations elucidated that transformants are able to maintain oxidative compounds such as malondialdehyde–an end-product of lipid peroxidation and H2O2–within the controlled range to cope with oxidative damage (Parvanova et al., 2004; Li et al., 2007).
So far, the reasons behind the partial degradation of fructans in cold-induced (0–5 °C) autumn chicory roots, a very well studied physiological response (Van Laere and Van den Ende, 2002), remained obscure. Indeed, these growth-arrested plants do not need carbon skeletons or osmotic adjustments. According to the hypothesis presented here, it is now proposed that the partial degradation of longer DP fructans increases the total number of molecules (fructose, sucrose, and lower DP fructans) to increase scavenging capacities and deal with the increased oxidative stress under chilling. Indeed, longer DP fructans might be too extended, part of these molecules being too far away from the tonoplast, the actual place of ROS generation. Similarly, the introduction of yeast invertase in potato increased the sugar concentration, contributing to chilling tolerance (Deryabin et al., 2007). Supporting the same idea, the breakthrough manuscript of Kawakami et al. (2008), introducing wheat 1-SST in the non-fructan plant rice, convincingly demonstrated that transgenic rice plants became more tolerant to chilling. The stabilizing effect of fructans on membranes might be of crucial importance during freezing (subzero temperatures) but probably not during chilling. Therefore, the proposed ROS-scavenging concept could probably explain the chilling tolerance observed in transgenic rice. Strikingly, both 1-SST introduction (Kawakami et al., 2008) and heat shock-mediated APX expression (Sato et al., 2001) can protect rice plants against chilling injury.
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Conclusions and perspectives |
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TopAbstractIntroductionSOS: a role in...Links between oxidative stress...Conclusions and perspectivesReferences |
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Exposure to environmental stress often results in increased production of ROS in plants. The plant's capacity to delineate these toxic compounds depends on the metabolic responsiveness of defensive mechanisms. Both enzymatic and non-enzymatic defence pathways can detoxify ROS. Sucrose and SOS (including fructans and RFOs) fulfil various functional roles in plant metabolism. SOS might either directly detoxify ROS in chloroplasts and vacuoles or indirectly stimulate the classic antioxidative defence systems. As a new concept, it can be hypothesized that the synergistic interaction of SOS and phenolic compounds forms part of an integrated redox system, quenching ROS and contributing to stress tolerance, especially in tissues with high soluble sugar concentrations. However, the exact chemical identity and stability of the SOS radicals remain obscure and need further exploration. Furthermore, it can be expected that SOS-related scavenging mechanisms would affect ROS signalling pathways. How such signalling cascades control the survival, or death, of plants would be a fascinating perspective.
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Acknowledgements |
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The authors thank Professor A. Van Laere for critically reviewing this manuscript. RV is funded by the University of Hohenheim and Baden-Wurttemberg state, Germany. WVdE is supported by grants from FSR Flanders.
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