Review
Physiological and biochemical responses to high light and temperature stress in plants

https://doi.org/10.1016/j.envexpbot.2017.05.002Get rights and content

Highlights

  • The level of antioxidants depends on the stress severity and duration.

  • The plant’s antioxidants response to light and temperature in a short- and long-term manner (acclimation).

  • Under severe, short stress, the levels of antioxidants tend to decrease.

  • Under acclimation (long-term responses) the levels of antioxidants gradually increase.

Abstract

Light intensity and temperature are primary environmental factors affecting the growth and development of plants. Changes in their intensity, range and duration can lead to acclimatory responses, cellular damage and ultimately to the death of plants. Plants have evolved several efficient protective mechanisms that make it possible for them to survive under unfavorable light and temperature conditions. These mechanisms are linked predominantly to the photosynthetic electron transport chain, xanthophyll cycle and the photorespiratory pathway. Under stress conditions, elevated levels of reactive oxygen species (ROS) are produced, which in addition to deleterious effects also show signalling functions. In response to enhanced ROS formation, different low-molecular antioxidants are synthesized, as well as antioxidant enzymes. Depending on the stress intensity and its duration, the content of synthesized antioxidants varies. Under severe, short light/temperature stress, the contents of low-molecular weight antioxidants, such as ascorbate, glutathione and prenyllipids, tend to decrease, which is correlated with an extra need for ROS scavenging. Under longer exposure of plants to unfavorable light and temperature conditions, the contents of antioxidants gradually increase as a result of acclimation during long-term responses. Studies on plant antioxidant responses indicate that a crucial part of the antioxidant network operates in chloroplasts and their action shows a high level of interdependence. The antioxidant response also depends on plant stress-tolerance, and frequently varies for different species. Therefore studying a wide range of plant species is a fruitful approach to investigating the natural variation in the antioxidant response of plants in relation to excess light and temperature.

Introduction

During their lifetime, plants have to cope with many unfavorable conditions that cause stress. These could be of biotic or abiotic origin. An in-depth understanding of the mechanisms that protect plants against stress conditions should encompass different levels of plant organization: the whole-plant, cellular, biochemical and molecular levels. Furthermore, the multilevel responses of plants to abiotic stresses, such as drought, salinity, low/high temperature, high light etc., are classified as short- and long term responses (Russell et al., 1995, Havaux, 1996, Phee et al., 2004, Biswal et al., 2011, Baxter et al., 2014). The short-term response occurs within hours of the initiation of the stress, whereas extended stress (days, weeks) results in acclimated, long-term responses. Although some processes activated during both responses are similar, many others are different and should be considered separately. Many studies have shown how low molecular weight antioxidants and antioxidant enzymes protect plants against abiotic stresses (Foyer and Noctor, 2009). Under unfavorable abiotic conditions the activities of certain antioxidants are suppressed, while others are up-regulated. In these conditions, the balance between reactive oxygen species (ROS) production and antioxidant activity is essential for the redox signalling (Choudhury et al., 2013, Foyer and Noctor, 2016). Physiological stress is defined as a rapid and direct effect of an external stressor which causes disruption to the homeostasis of the organism (Koolhaas et al., 2011). In contrast, acclimation is the process by which an individual organism adjusts to a gradual change in its environment (i.e. a change in light intensity), allowing it to maintain its performance across a range of environmental conditions (Ruban, 2009). Thus, when we consider the stress response we should be aware which conditions are being analyzed. For example, a rapid, short-time (minutes and hours) increase in light intensity or temperature will induce different mechanisms of antioxidant response than long-term growth in high light (HL) or conditions with a higher temperature (Szymanska and Kruk, 2010, Szymanska et al., 2014, Sgobba et al., 2015).

This review summarizes recent data on the effect of light and temperature stress on the function of plant cells in the context of ROS homeostasis. The aim is to show the differences between the short-term responses to acute stress and the long-term acclimation process in plants.

Many molecular oxygen (O2) derivatives are described as reactive oxygen species (ROS), which include mainly superoxide anion radical (O2 radical dot), hydrogen peroxide (H2O2), hydroxyl radical (radical dotOH), and singlet oxygen (1O2) (for review see e.g. Ślesak et al., 2007, Foyer and Noctor, 2009, Foyer and Noctor, 2016, Choudhury et al., 2016, Mittler, 2017). Local microoxic environments that included O2/ROS together with a rudimentary antioxidant response system may have appeared on Earth as early as ca. 3.0 − 3.5 Ga and have been a permanent associate of aerobic life (Ślesak et al., 2012, Ślesak et al., 2016, Mittler, 2017)

The cell compartments most affected under unfavorable light and temperature conditions are chloroplasts. Stress conditions result in a lowering of the performance of the photosynthetic electron transport chain (PETC). In photosystem II (PSII), excess energy can generate a triplet state of chlorophyll which can pass excitation energy to O2, producing 1O2. Under abiotic stress, over-reduction of photosystem I (PSI) occurs as well, leading to the generation of the O2 and subsequently H2O2 (Asada, 2006, Foyer and Noctor, 2009). The presence of H2O2 gives rise to the formation of the highly radical dotOH (Asada, 2006). When produced in excess amounts, ROS can oxidize lipids and other molecules inside chloroplasts or in the cytosol, into which H2O2 can penetrate from chloroplasts (Borisova et al., 2012). ROS generation affects plant metabolism in two ways, either through the redox signalling pathways or, at an extremal ROS accumulation level, through less specific cytotoxic damage to cellular components (Laloi et al., 2006, Foyer and Noctor, 2009, Foyer and Noctor, 2016, Baxter et al., 2014. Each way determines the transduction and subsequent physiological response. These reactions vary depending on the type of stress, its intensity, duration, and on the species and its life strategy (Lefebvre et al., 2009).

Plants have developed several strategies to cope with oxidative stress and among them antioxidant defense plays a crucial role in plant survival under abiotic stresses. The major components of the antioxidant system include low-molecular weight antioxidants, such as ascorbic acid (Asc), glutathione (GSH), tocochromanols and reduced prenylquinones. Antioxidant enzymes also come into play, such as catalase (CAT), superoxide dismutase (SOD), peroxidase (POX), glutathione reductase (GR), glutathione peroxidase (GPX), peroxiredoxins (PRXs) among others (Choudhury et al., 2013, Choudhury et al., 2016, Awad et al., 2015). Under oxidative stress, the synchronized action of all of these antioxidants leads to ROS-removing and protect plants against oxidative damage.

Among the low-molecular weight antioxidants, Asc plays a crucial role in the hydrophilic cellular environment. Having been synthesized in mitochondria, Asc is transported to other cell compartments (Munné-Bosch et al., 2013). It was estimated that 30–40% of the total Asc of leaves is localized in chloroplasts (Noctor and Foyer, 1998). Apart from its direct antioxidant action, Asc is used as a substrate for ascorbate peroxidase (APX) to detoxify H2O2 to water in the water–water cycle (Asada, 1999, Halliwell, 2006). Asc is also a cofactor of violaxanthine epoxidase, and is involved in the regeneration of α-tocopherol from the α-tocopheroxyl radical (Munné-Bosch and Alegre, 2002, Foyer and Noctor, 2005). GSH, together with Asc, is engaged in the water–water cycle (Noctor and Foyer, 1998). GSH plays a key role in H2O2 decomposition, and the ratio between reduced GSH and its oxidized form (GSSH) under abiotic stress is an indicator of the cellular redox balance (Shao et al., 2008; Foyer and Noctor, 2016; see also below). GSH is synthesized in chloroplasts and cytosol (Szarka et al., 2012) and shows highly compartment-specific changes in plants under abiotic stress, indicating important subcellular roles for plant defense (Zechmann, 2014). In general, GSH accumulates to milimolar concentrations, and very often a higher amount of GSH is found in mitochondria than in plastids, which contain its lowest amounts (Szarka et al., 2012).

Prenyllipids, such as tocochromanols and reduced prenylquinones, are membrane-localized, lipophilic antioxidants that scavenge ROS and inhibit lipid peroxidation (Miret and Munne-Bosch, 2015). Tocochromanols (tocopherols, tocotrienols, plastochromanol) are built of a chromanol head group and a hydrophobic side chain (DellaPenna and Mene-Saffrane, 2011, Kruk et al., 2014). As antioxidants, prenyllipids fulfil their function in thylakoids and are stored in plastoglobuli (Szymanska and Kruk, 2010). One of the functions of tocochromanols is to protect membrane lipids against oxidative damage (DellaPenna and Mene-Saffrane, 2011). Tocochromanols also physically and chemically quench 1O2 and other ROS (Munné-Bosch and Alegre, 2002, Gruszka et al., 2008). Tocochromanols therefore contribute to the preservation of an adequate redox state in chloroplasts and to chloroplast functions during plant development and stress responses (Munné-Bosch and Alegre, 2002, Munné-Bosch, 2005, DellaPenna, 2005, Szymanska and Kruk, 2010).

Antioxidant enzymes such as CAT, SOD, APX, PRX, and GPX act as the main line of defense in cells. These enzymes are involved in the chloroplast detoxification pathway known as the water–water cycle (Asada, 1999, Halliwell, 2006). This name is derived from the fact that water is the source of electrons and is the final product of the pathway. Superoxide anion radicals are dismuted by SOD to O2 and H2O2 (Logan et al., 2006). Then, in the glutathione-ascorbate cycle, APX uses Asc to reduce H2O2 to water. The product of this reaction − monodehydroascorbate (MDHA), can be recycled back to Asc by three different mechanisms: i) by accepting two electrons from the photosynthetic electron transport chain; ii) by reduction through MDHA reductase, or iii) by the non-enzymatic dismutation of ascorbate radicals yielding dehydroascorbate (DHA), which in turn is reduced to Asc by DHA reductase (DHAR). This enzyme utilizes GSH as a reductant. Finally, GR recycles GSH using NADPH as a reductant (Asada, 1999, Logan et al., 2006, Foyer and Noctor, 2009). Moreover, GSH oxidation (GSH  GSSG) may be carried out independently of DHA, i.e. by GPXs, PRXs or methionine sulfoxide reductase. As a result of these reactions catalysed by GPXs/PRXs, the decomposition of H2O2 or organic peroxides into water and alcohol, respectively, also occurs (Foyer and Noctor, 2011). CAT is another important H2O2-removing enzyme under abiotic stress, and can directly convert H2O2 to O2 and water (Van Breusegem et al., 2001).

One of the characteristic features of the antioxidant enzymes mentioned above is their non-homogenous distribution in the plant cell. Most antioxidant enzymes are encoded by multigene families, and they are expressed in various cell compartments (Ślesak et al., 2007, Szechyńska-Hebda and Karpiński, 2013) (Table 1). Moreover, the same cell areas are sources of ROS coupled with intracellular redox signalling pathways (Foyer and Noctor, 2016). An interesting case are CATs which are almost exclusively present in peroxisomes, being a marker of these organelles. However, there are a few reports also on the extraperoxisomal localization of CATs, such as apoplast (cell wall), mitochondria and chloroplasts (for review see: Heinze and Gerhardt, 2002). It should be noted that antioxidant enzymes always occur together with low-weight molecular antioxidants which are coupled to enzyme-related reactions e.g. Asc/APX, GSH/GPX (Table 1). Such a link leads to redox changes in suitable cell compartments, which plays a crucial role in plant responses to various abiotic/biotic stresses (Munné-Bosch et al., 2013, Choudhury et al., 2016, Foyer and Noctor, 2016; see also below).

The survival and reproductive success of plants rely on the molecular basis of the photosynthetic apparatus being efficiently designed and on their adaptability to changing environmental conditions. Plants have developed a number of adaptation mechanisms to cope with light fluctuations. These involve various levels of plant organization. For example, on the level of the whole organism it may be the adjustment of leaf orientation (Koller, 1990), on the cellular level − chloroplast movements (Ruban, 2009, Banaś et al., 2012). Fluctuations in light intensity (i.e. sunlight intensity randomly changing by several orders during the day) predominantly affect those photosynthetic light reactions which take place inside chloroplasts, in thylakoid membranes (Fig. 1, Kirchhoff, 2014). Thus, on the molecular level, plants are able to regulate light absorption by long-term and short-term adaptation mechanisms (Ruban, 2009). Among them, ROS scavenging systems and high energy quenching mechanisms, which convert harvested light energy into heat, are of particular interest (Fig. 1, Noctor and Foyer, 1998, Kirchhoff, 2014).

Excess light (EL) decreases the rate of PETC. In particular, PSII is readily inactivated under strong light and this phenomenon is referred to as the photoinhibition of PSII (for review see: Murata et al., 2007, Roach and Krieger-Liszkay, 2014). The extent of photoinhibition is the result of an imbalance between the rate of photodamage of PSII and its repair. In the “classical” scheme which describes the mechanism of photoinhibition, strong light induces the production of ROS, which directly inactivate the photochemical reaction centre of PSII (Roach and Krieger-Liszkay, 2014). However, other studies have demonstrated that photodamage to PSII is also associated with light absorption by the manganese cluster of the oxygen-evolving complexes (OEC) (Tyystjarvi, 2008). Furthermore, EL energy absorbed by photosynthetic pigments has been shown to accelerate photoinhibition through a mechanism that causes inhibition to the repair of photodamaged PSII rather than through direct photodamage (Nishiyama et al., 2006, Takahashi and Murata, 2008). Ohnishi et al. (2005) proposed that photodamage is initiated by the direct effect of light on the OEC and that ROS inhibit the repair of photodamaged PSII by suppressing primarily the de novo synthesis of proteins. According to this approach, photodamage occurs in a two-stage process. The first step includes the UV and blue light-dependent destruction of the Mn-cluster of the OEC, resulting in the release of manganese ions (Hakala et al., 2005, Takahashi and Murata, 2008, Takahashi and Badger, 2011). The second step is related to the inactivation of the photochemical reaction centre of PSII by light that has been absorbed by photosynthetic pigments at the reaction centre of PSII (Hakala et al., 2005, Ohnishi et al., 2005). The release of manganese ions (Mn2+) from the OEC is accompanied by photodamage to PSII (Hakala et al., 2005, Zsiros et al., 2006), suggesting that disruption of the manganese cluster upon the absorption of light might be a primary element of photodamage. However, it is still unclear whether this model is applicable to photodamage to PSII under visible light, since manganese weakly absorbs visible light. Zavafer et al. (2015) used PSII membrane fragments isolated from spinach leaves to identify the initial site of photodamage to PSII upon illumination by visible light. When the samples were exposed to visible light in the presence of an exogenous electron acceptor, both PSII total activity and PSII reaction centre activity declined due to photodamage. The addition of an electron donor to the PSII reaction centre alleviated the decline of the reaction centre activity but not PSII total activity. These results demonstrate that visible light damages the OEC prior to photodamage to the PSII reaction centre, which is consistent with the two-step photodamage model (Zavafer et al., 2015).

After PSII has been inactivated by light, its activity is efficiently restored by a repair system that involves the degradation and removal of the D1 protein in the photodamaged PSII; de novo synthesis of proteins, in particular the precursor of the D1 protein (pre-D1) and the processing of pre-D1 (Aro et al., 2005). The light-induced inactivation of PSII and its repair occur simultaneously. Photoinhibition of PSII becomes apparent when the rate of photodamage to PSII exceeds the rate of its repair. The rate of photodamage can be studied without the balancing effects of repair using inhibitors of protein synthesis, e.g. lincomycin or chloramphenicol (Tyystjärvi et al., 1992, Wada et al., 1994). PSII repair can be monitored in terms of the recovery of PSII activity after transfer of the plants from HL to relatively low light intensities. The rate of PSII photodamage is proportional to the intensity of incident light and this is consistent with the two-step model of photodamage (Mattoo et al., 1984, Tyystjärvi and Aro, 1996, Nishiyama et al., 2001, Allakhverdiev and Murata, 2004, Chow et al., 2005). Recent studies have revealed that this proportionality is unaffected by environmental stresses, such as oxidative stress (Nishiyama et al., 2001, Nishiyama et al., 2004), cold stress and salt stress (Gombos et al., 1994, Allakhverdiev and Murata, 2004, Allakhverdiev et al., 2002). The rate of repair also depends on the intensity of incident light, reaching its maximum under relatively weak light (Allakhverdiev and Murata, 2004). In contrast to photodamage, repair was severely inhibited by oxidative stress (Nishiyama et al., 2001, Nishiyama et al., 2004, Allakhverdiev and Murata, 2004), salt stress and low-temperature stress (Allakhverdiev and Murata, 2004, Allakhverdiev et al., 2002).

To avoid photoinhibition, plants have developed the diverse photoprotection mechanisms mentioned above (Fig. 1). Moreover, plants are also equipped with other photoprotection mechanisms, such as: i) thermal dissipation of light energy absorbed (see below) and state transitions, ii) cyclic electron flow (CEF) around PSI, iii) the violaxanthin-antheraxanthin-zeaxanthin cycle (VAZ; called also xanthophyll cycle), iv) the photorespiratory pathway and iv) ROS scavenging systems.

Plants are able to dissipate EL energy absorbed by PSII light-harvesting complexes (LHCII) as harmless heat energy (Ahn et al., 2008, Roach and Krieger-Liszkay, 2014). Light energy absorbed by PSII is effectively eliminated by a combination of photochemical and non-photochemical quenching (NPQ) processes (Fig. 1), which can be monitored in terms of chlorophyll fluorescence. NPQ consists of the ΔpH- and PsbS (a chlorophyll-binding protein of PSII)-dependent quenching process (qE), zeaxanthin (a carotenoid involved in the VAZ cycle) formation (qZ), state transition quenching (qT) and photoinhibitory quenching (qI) (Baker, 2008, Li et al., 2009, Kulasek et al., 2016, Ruban, 2016). In general, the NPQ process serves to dissipate excess energy as heat in order to prevent damage to PSII (Niyogi et al., 2005). Recently, however, a link between PsbS, NPQ and the dissipation of EL energy as heat was questioned. It cannot be excluded that 1O2 is involved in EL energy dissipation rather than PsbS (Kulasek et al., 2016). The mechanism responsible for qZ is mainly associated with the VAZ cycle, where the conversion of violaxanthin to zeaxanthin, via antheraxanthin, by the violaxanthin de-epoxidase and the protonation of the PSII protein subunit PsbS in plants or LhcSR3 in green algae, respectively, occurs (Niyogi, 1999, Peers et al., 2009). These reactions are enhanced by a low lumenal pH, which is accompanied by the generation of a ΔpH through linear- and CEF in light (Niyogi, 1999). Another light-inducible response is associated with the phenomenon of state transitions (qT) (Haldrup et al., 2001, Wollman, 2001). State transitions are short-term processes that change the antenna sizes of PSII and PSI. The basis of qT lies in the reversible phosphorylation of LHCII and the movement of phosphorylated LHCII from PSII to PSI. Moreover, the movement of LHCII away from PSII relieves excitation pressure (Tikkanen et al., 2012). The decrease in the PSII antenna size results in less excitation energy in PSII with a corresponding decrease in PSII fluorescence intensity. The contribution of qT to the overall NPQ is rather negligible under HL stress in most plants (Müller et al., 2001). The qT seems to be important only in low light (LL), when it regulates the distribution of excitation energy between PSII and PSI and thereby optimizes photosynthetic reactions. State transitions play a minor role in higher plants, but they are highly important in green algae. In Arabidopsis, where only up to 15–20% of LHCII can be phosphorylated (Bellafiore et al., 2005, Pesaresi et al., 2011), qTare important in acclimation to changing light intensities (Allen, 1992, Roach and Krieger-Liszkay, 2014). In comparison, in Chlamydomonas∼80% of LHCII can disassociate from PSII (Wollman, 2001) but only 20% binds to PSI (Wollman, 2001, Nagy et al., 2014).

CEF around PSI recycles the reducing equivalents produced by PSI in the stroma towards the plastoquinone (PQ) pool and generates ATP without the accumulation of NADPH in chloroplasts. Through the activity of cytochrome b6f, it enhances the generation of ΔpH across the thylakoid membrane and promotes synthesis of ATP (Shikanai, 2007, Shikanai, 2014). The contribution of CEF to the induction of NPQ of Chl fluorescence was demonstrated by Cornic et al. (2000). Illumination of leaves or intact chloroplasts by far-red light, which excites only PSI, induces NPQ with the enhancement of the electrochromic shift and the induction of ΔpH across thylakoid membranes. In addition, CEF activity responds to environmental stress conditions, such as light fluctuations, drought and temperature stress (Rumeau et al., 2007, Kohzuma et al., 2008). Tobacco plants grown under HL showed a higher value of NPQ and enhanced CEF activity when compared to plants grown under lower light intensity. These results suggest that enhancing CEF activity is indispensable for the induction of NPQ (Fig. 1, Miyake et al., 2005).

CEF can occur via both NAD(P)H dehydrogenase (NDH) complex-dependent and ferredoxin (Fd)-dependent electron transport pathways (Shikanai, 2007). The latter occurs directly via Fd and other proteins, such as PGR5 (Munekage et al., 2002) and PGRL1 (Terashima et al., 2012). CEF-induced ΔpH is associated with the Fd-dependent pathway in Arabidopsis (Munekaga et al., 2004), although this might differ in other photosynthetic organisms, such as C4 plants (Takabayashi et al., 2005) and cyanobacteria (Mi et al., 1995).

Although CEF is clearly linked to light stress, the exact regulatory mechanism that switches it on is still being debated. For example, recent studies have revealed components of the NDH- and Fd-dependent pathways (Muraoka et al., 2006, Munekage et al., 2002, DalCorso et al., 2008), but the precise mechanism of CEF activation remains enigmatic. High sensitivity to photoinhibition and bleaching of the photosynthetic pigments under HL was observed in the mutant Nicotiana tabacum ndhB, which lacks a NDH-dependent pathway (Endo et al., 1999). In turn, eliminating the PGR5-dependent pathway by a mutation of pgr5 caused accelerated photoinhibition of PSII in Arabidopsis and Synechocystis (Munekage et al., 2002, Yeremenko et al., 2005). Moreover, in recent studies, a crucial role for PGR5-dependent CEF has been suggested for PSI photoprotection in LL/HL fluctuating conditions (Suorsa et al., 2012).

It has been suggested that the photorespiratory pathway, consisting of the photorespiratory carbon and nitrogen cycles, is important for avoiding the photoinhibition of PSII, especially in C3 plants (Wingler et al., 2000). The photorespiratory pathway is initiated by the oxygenation of ribulose bisphosphate (RuBP) catalysed by Rubisco (D-ribulose 1,5-bisphosphate carboxylase/oxygenase). In this reaction, glycolate-2-phosphate is produced and subsequently metabolized in the photorespiratory carbon cycle to form the Calvin cycle intermediate, glycerate-3-phosphate (Leegood et al., 1995). Moreover, H2O2, the by-product of photorespiration, may be involved in redox processes in the plant cell (Fig. 1, see also below). The impairment of photorespiratory pathways induces symptoms of HL stress, such as photoinhibition and chlorosis, in ambient CO2, but not in conditions that suppress the oxygenase reaction of Rubisco, such as high CO2 and/or low oxygen partial pressures. These results indicate that the enzymes of the photorespiratory pathway are indispensable only under conditions where the oxygenase reaction of Rubisco occurs. It is believed that the consumption of photochemical energy products, such as ATP and NADPH, through the photorespiratory pathway helps to avoid photooxidative damage to PSII (acceptor-side photoinhibition) by highly toxic 1O2 generated via the interaction of oxygen with triplet-excited in PSII reaction center (P680) (Osmond et al., 1997). Thus, the photorespiratory pathway can be regarded as a mechanism for minimizing the damaging effects of EL on PSII (Wingler et al., 2000). Rapid photoinhibition caused by impairment of the photorespiratory pathway in Arabidopsis mutants has been shown to be linked to the inhibition of the repair of photodamaged PSII (but not the acceleration of photodamage to PSII), owing to the suppression of de novo synthesis of the D1 protein on the translation level (Takahashi et al., 2007). For this reason, the photorespiratory pathway might be interpreted as a part of the antioxidant machinery of plant cells (Voss et al., 2013).

It should be emphasized that all so called “antioxidant reactions” that are catalysed by antioxidant enzymes or occur non-enzymatically lead to changes in the content of oxidized and reduced compounds that make specific redox couples (Table 2). These reactions are usually parts or are strictly linked to PETC and the mitochondrial electron transport chain. Some of them are not dependent on chloroplastic/mitochondrial activity, but are associated with other compartments e.g. apoplast, endoplasmic reticulum or vacuole (Foyer and Noctor, 2009, Suzuki et al., 2012, Foyer and Noctor, 2016). Moreover, ROS, mainly H2O2, may directly oxidize thiol (-SH)-containing proteins. Such modifications affect e.g. the transcription factors binding to DNA that alter gene expression (Dietz et al., 2016) or the degradation of proteins like Rubisco that lose their function after oxidative damage (Moreno et al., 2008). As a result, in response to various abiotic/biotic stress factors, the specific redox state in the plant cell compartments is observed (Foyer and Noctor, 2009, Suzuki et al., 2012, Foyer and Noctor, 2016). A balance between the reduced and oxidized pool of redox couples (Table 2), predominantly GSH/GSSG, also has an important function as an antioxidant signal transduction factor linked to calcium signalling and gene expression (Gomez et al., 2004). Recently, the use of transgenic plants with redox-sensitive green fluorescent protein 2 (roGFP2) localized in various organelles showed that the roGFP2 oxidation level is a non-invasive indicator of the H2O2-related redox status of different plant cell compartments (Bratt et al., 2016). For example, HL or drought changed the redox status of chloroplasts or mitochondria respectively. These results indicated a kind of organelle autonomy and multi-organelle redox changes in response to various environmental stresses (Bratt et al., 2016). Therefore, ROS generation and signalling do not occur in the plant cell independently of redox-regulated signal transduction pathways. Thus, these processes are “two sides of the same coin” and, in fact, they should not be analyzed separately.

Stress situations, especially excess (or high) light conditions that are directly linked to PETC, lead to noticeable changes to the content of reduced counterparts in a redox couple (Fig. 1, Table 2). According to the hypothesis of Foyer and Noctor (2016), the generation of ROS and then the activation of ROS-removing machinery is rather a consequence of an increased content of reduced compounds: Fdred, NAD(P)H, thioredoxin, GSH and Asc under light stress. In this scenario, ROS production is a secondary effect after the strong reduction of specific compounds in chloroplasts, including “classical” antioxidants: GSH and Asc (Foyer and Noctor, 2016).

Light intensity also strongly affects the redox state of the PQ-pool in thylakoids and its redox state is supposed to be the key factor that regulates many physiological reactions such as the expression of the psaAB (PSI subunits) and psbA (PSII subunit) genes, and the expression of lhcb1 (subunit of the light harvesting complex of PSII) (Escoubas et al., 1995, Pfannschmidt et al., 2001, Frigerio et al., 2007). The redox state of the PQ-pool also regulates the expression of enzymes involved in carotenoid biosynthesis (Steinbrenner and Linden 2003), and the synthesis of nuclear-encoded antioxidant enzymes, such as APX1 and APX2 (Karpinski et al., 1997), SOD (Ślesak et al., 2002, Ślesak et al., 2003) or nitrate reductase (Giordano et al., 2005). The primary sensor in these responses is cytochrome b6f-associated STN7 kinase in higher plants, which triggers both short-term and long-term responses, although at present its activation mechanisms and signal transduction remain poorly understood (Pesaresi et al., 2011). The PQ-pool undergoes reduction at the light intensities to which plants are adapted (Kruk and Karpinski, 2006), but at high light intensity oxidation of the PQ-pool is observed, mainly due to 1O2 and NPQ (Kruk and Szymańska, 2012).

The primary role of chloroplasts in HL responses has already been postulated, but now it is also extended to other abiotic/biotic stresses (Suzuki et al., 2012; Karpiński et al., 2013). Previous opinions that only interpreted ROS generation by various stress factors as negative side-effect of aerobic metabolism is questioned (Foyer and Noctor, 2009). In this “old-fashioned” model, the role of antioxidants was to eliminate the overproduction of ROS almost completely. Now, ROS are presented in the wider context as an important part of cellular redox homeostasis. An increase in ROS content in a cellular organelle is strictly related to the redox state of many other chemical components. ROS-related redox changes, in appropriate plant cell compartments and plant tissues, but not ROS per se, play a key role in intra- and intercellular signalling that affects plant growth and development. On this view, enzymatic and low-molecular weight antioxidants are kinds of “housekeeping” compounds that integrate plant metabolism in relation to various environmental stimuli (Baxter et al., 2014, Dietz et al., 2016, Foyer and Noctor, 2016, Mittler, 2017).

To control light-induced ROS production in chloroplasts, plants have evolved several antioxidant systems that reduce ROS-mediated side-effects and make it possible to maintain the chloroplast redox balance (Pinto-Marijuan and Munne-Bosch, 2014; see also above). Arabidopsis plants acclimated to very LL (up to 10 μmol photons/m2/s) showed elongated petioles, thinner and smaller leaf blades, changes in grana stacks, and lower chlorophyll and protein content (Oelze et al., 2012). In comparison to normal light-grown plants, those grown under very LL (at 8 μmol photons/m2/s) had a similar stromal APX (sAPX) and higher thylakoid APX (tAPX), DHAR and CuZnSOD protein content. But in most cases, the transcript content in LL plants was lower than in normal-light control plants (Ruckle et al., 2012). The involvement of antioxidant enzymes in time-dependent photoprotection was confirmed by mutant analysis. Single mutants, lacking sAPX or tAPX, or even double mutants, showed no visible symptoms of long-term light stress (1-14 days, 2000 μmol photons/m2/s) (Giacomelli et al., 2007). On the other hand, short-term HL-treated single mutants of sAPX or tAPX accumulated more H2O2, oxidized proteins and GSH when compared to WT plants under stress conditions (Murata et al., 2010). Furthermore, at the early stages of photooxidative stress (1–3 h) the maximum quantum yield of PSII (Fv/Fm) in mutants decreased significantly and this was accompanied by the suppression of the transcript contents of H2O2-responsive genes (APX1, APX2, HsfA2 and HSP18.1-CI) (Murata et al., 2010). These effects were more pronounced for a tAPX than an sAPX mutant, suggesting that in the early stages of photooxidative stress tAPX is not only necessary for the rapid scavenging of H2O2 in the vicinity of thylakoid membranes but also for the regulation of the H2O2-responsive genes (Murata et al., 2010). Under light treatment, the regulation of the antioxidant system at the transcriptional level seems to be crucial in overcoming light stress effects. After the plants were transferred from low to HL, most of the antioxidant defense genes were down-regulated (Szechyńska-Hebda and Karpiński, 2013). When compared to dark/light/dark shifts, in high and EL, a different set of genes seems to be expressed or suppressed. Although similar genes are involved in responses to HL (400 μmol photons/m2/s) and EL intensities (1000–1800 μmol photons/m2/s), under EL the gene expression is more responsive. In particular, under EL, the genes that encode chloroplast enzymes of the water–water cycle are highly expressed in green tissues (Szechyńska-Hebda and Karpiński, 2013). Rapid changes in light intensity when the plant transfers from normal to HL did not affect the transcript content of sAPX within the first 30 min, but later it rapidly increased. The sAPX protein content was upregulated in a similar way. The tAPX transcript (mRNA) also did not change in the early phase, but after 24 h a significant drop in its protein content was observed (Oelze et al., 2012). It should be underlined that besides chloroplastic isoforms of APXs, chloroplast-located PRXs, mainly 2-cysteine peroxiredoxins, are also crucial components of the chloroplastic ROS-removing system and play an essential role in protecting photosynthetic apparatus under HL conditions (Awad et al., 2015).

High SOD activity is linked with stress responses in plants (Mishra et al., 1993). In different cultivars of sweet potato plants, under long-term HL treatment, SOD activity decreased on the first day of treatment, but increased in the following days (Hwang et al., 1999). The same effect was observed for CAT. In contrast, in wheat leaves under HL (600 μmol photons/m2/s) and at two different temperatures (19 and 8 °C) for 20 h there was a gradual increase in SOD and CAT activity. A comparison of the chloroplast protein profiles of Arabidopsis plants subjected to 3 h of EL (1000 μmol photons/m2/s) with LL grown plants (100 μmol photons/m2/s) showed that SOD was one of the most upregulated proteins (Phee et al., 2004).

Asc and GSH accumulation in chloroplasts and the thylakoid lumen was observed under HL stress (Foyer and Noctor, 2005, Heyneke et al., 2013, Zechmann, 2014). Arabidopsis WT were exposed to different light intensities (50, 150, 300, 700 and 1500 μmol photons/m2/s) for short (4 h) and long periods (14 days). Short-term HL treatment induced a drastic increase in the overall GSH and Asc content in WT Arabidopsis. GSH accumulated mainly in chloroplasts, peroxisomes and cytosol reaching the highest value under exposure to 1500 μmol photons/m2/s. Under the same conditions, Asc accumulated mainly in chloroplasts and vacuoles and was detected in the thylakoid lumen (Heyneke et al., 2013). This indicates that these compounds are important antioxidants in chloroplasts and peroxisomes for detoxifying ROS formed after a few hours of HL stress (Karpinski et al., 1997, Tausz et al., 2004, Heyneke et al., 2013). The presence of Asc inside the thylakoid lumen is interesting because of it NPQ value; the violaxanthine deepoxidase, which requires an Asc as a cofactor, is located there (Foyer and Noctor, 2005). When plants were exposed to 300 and 700 μmol photons/m2/s, for a longer time (14 days) Asc and GSH accumulation was observed in all subcellular compartments, whereas under 1500 μmol photons/m2/s these antioxidants decreased (Heyneke et al., 2013). During long-term exposure plants exhibited additional acclimation symptoms, including an increase in leaf thickness, the accumulation of anthocyanins in vacuoles, a decrease in Chl content, and an adjustment of the fine structure of the chloroplast. An increase in the total Asc content and that of GSH in leaves after long-term HL conditions have been reported many times (Muller-Moule et al., 2004, Giacomelli et al., 2006, Haghjou et al., 2009, Havaux et al., 2005, Golan et al., 2006). Asc deficient-mutants (vtc2) were able to grow under HL conditions for 4 weeks, probably because of compensation by other antioxidants and photoprotection mechanisms (Muller-Moule et al., 2004). Mutants, as well as WT plants in these conditions, had increased contents of total GSH content and α-tocopherol, when compared to LL-grown plants. In contrast, when plants were exposed to HL stress − transferred from LL (180 μmol photons/m2/s) to EL/HL (1800 μmol photons/m2/s), (sample were taken after 1, 4, 24, 47, 72, 96, and 120 h) the vtc2 mutants showed much higher sensitivity (Muller-Moule et al., 2003). This is because in the first minutes/hours, the need for ROS scavenging is very strong. In the first 2 h of HL, the content of α-tocopherol and xanthophyll pigments in a vtc2 mutant did not change (Muller-Moule et al., 2003). It might be that under severe stress, in the absence of Asc, tocopherol and other antioxidants take over its scavenging activity, and thus their consumption equals or exceeds their synthesis, thus the content remains at the same level.

It is well established that tocopherols and other chloroplast prenyllipids, such as plastoquinol and plastochromanol, are synthesized in response to high light stress to counteract the elevated ROS content, mainly 1O2, under these conditions (Szymanska and Kruk, 2010, Szymanska et al., 2014, Munné-Bosch and Alegre, 2002, Miret and Munne-Bosch, 2015). As a result of 1O2 being chemically quenched, various oxidation products of prenyllipids are formed (e.g. hydroxy-plastochromanol, plastoquinone-C) that can further fulfill the antioxidant function (Szymanska et al., 2014, Dłużewska et al., 2015, Kruk et al., 2016). Under HL, tocochromanols protect the lipid membrane by quenching/scavenging ROS and by inhibiting lipid peroxidation (Miret and Munne-Bosch, 2015). Changes in the content of tocochromanols are related to light stress intensity (Munné-Bosch and Alegre, 2002, Luschchak and Semchuk, 2012). It is known that the α-tocopherol content tends to decrease when stress is severe and the amount of ROS in chloroplasts increases (Munné-Bosch, 2005). The loss of α-tocopherol is a result of 1O2 chemical scavenging, since most of their oxidation products cannot be recycled back to α-tocopherol (Munné-Bosch, 2005, Munné-Bosch and Alegre, 2002). Stress-tolerant species usually show an increased tocopherol content under stress, while sensitive ones display tocopherol loss, which results in oxidative cell damage (Munné-Bosch, 2005). Munné-Bosch (2005) proposed that changes in α-tocopherol content during the plant stress response can be divided into two phases. The first involves an increase in tocopherol synthesis, followed by a second phase of net tocopherol loss (Munné-Bosch, 2005). The first stage is associated with protection by ROS scavenging and the inhibition of lipid peroxidation and can be related to moderate stress and to the acclimation process. This phase is typical of stress-tolerant plants. Plants in the second phase undergo severe stress, and then tocopherol degradation exceeds its synthesis and their content decreases (Munné-Bosch, 2005). This phase is observed in stress-sensitive plants. This mechanism can also be expanded to other antioxidants. The data obtained by our group (Szymanska and Kruk, 2010, Szymanska et al., 2014) are consistent with it. During acclimation to HL (5 weeks, 380 μmol photons/m2/s) in Arabidopsis plants the content of α-tocopherol, and that of plastoquinol increased markedly when compared to LL-grown plants. In the absence of α-tocopherol, in vte4 mutants, γ-tocopherol accumulated in HL subjected plants (Szymanska and Kruk, 2010). Similar results were obtained when plants were exposed to 3 days of HL. However, when Arabidopsis plants were illuminated by strong light (2000 μmol photons/m2/s) for a short-time (1 and 2 h), the α-tocopherol content, as well as γ-tocopherol in the vte4 mutant, gradually decreased (Szymanska et al., 2014). The same effect was observed by Golan et al. (2006). When compared to LL-grown plants, Arabidops is acclimated to 1800 μmol/photons/m2/s for 5 weeks showed a 4-fold increase in α-tocopherol content, accompanied by a significant rise in Asc, GSH and xanthophylls content (Golan et al., 2006). Over a period of 15 days, the tocopherol content increased 18-fold in plants subjected to HL stress combined with nutrient deficiency and low temperature (Collakova and DellaPenna, 2003). The increase in tocopherol content under long-term HL stress has been observed in many studies (Tanaka et al., 1999, Havaux et al., 2005, Trebst et al., 2002). In contrast, detached maize leaves exposed to short-term HL at a low temperature showed a 50% decrease in α-tocopherol content (Liepner et al., 2000). In Synechocystis sp. PCC6803, after 3 and 20 h of HL treatment, the content of tocopherol diminished by 20% (Maeda et al., 2005).

The response of plants to low- or high temperature stress depends on its level, its duration and the plant species. In general, temperature fluctuations limit plant growth and development (Lobell and Asner, 2003).

At elevated temperatures or heat (usually ≥30 °C), both developmental and growth parameters are affected, including seed germination, reproduction as well as crop yield (Hasanuzzaman et al., 2013). On the cellular and molecular level, membranes and the cytoskeleton, proteins, enzymes and RNA are the most affected (Ruelland and Zachowski, 2010, Suzuki et al., 2012, Hasanuzzaman et al., 2013). Photosynthesis is one of the processes most sensitive to temperature stress. Therefore, if the stress is extreme, like in EL conditions, photosynthesis inhibition occurs within minutes (Fig. 2). For example, inhibition of photosynthesis occurs at temperatures only slightly higher than those optimal for growth (Allakhverdiev et al., 2008, Yamamoto et al., 2008). Under elevated temperatures (≥30 °C), photochemical reactions and the carbon metabolism are the most prone to injury (Wang et al., 2009). Heat stress markedly affects the water status in leaves and intracellular CO2 concentration which is an effect of stomata closure (Greer and Weedon, 2012, Allakhverdiev et al., 2008). All of these changes lead to a reduction in the photosynthetic rate. The mechanism of photosynthetic inhibition under heat stress remains unclear. One mechanism suggested is the inhibition of the RuBP carboxylation rate (Kurek et al., 2007). Another suggests the inhibition of photosynthetic electron transport and the decrease in Rubisco activity (Cen and Sage, 2005; Makino and Sage, 2007 Makino and Sage, 2007). Of the photosynthetic electron transport chain components, PSII has been considered the most temperature-sensitive (Havaux, 1996). Within chloroplasts, under elevated temperature the most affected are the PSII, Rubisco and ATP synthase (Asthir, 2015).

Recent studies have suggested that elevated temperature, like HL, inhibits the repair system of PSII, rather than damaging it (Fig. 2; Sharkey, 2005, Allakhverdiev et al., 2008). Damage to the inhibition of the repair of PSII is strongly related to the temperature level. It is well known that strong heat stress inactivates the OEC directly (Nash et al., 1985). However, moderate heat stress, which does not directly inactivate the OEC, stimulates the photoinhibition of PSII (Allakhverdiev et al., 1997, Allakhverdiev and Murata, 2004). It was shown that moderate heat stress also increases the extent of photoinhibition in higher plants and inhibits the repair of photodamaged PSII but does not affect the extent of photodamage to PSII in transgenic tobacco with the ability to accumulate glycinebetaine (Yang et al., 2007). This increased tolerance to heat was associated with an improvement in the thermostability of the OEC and the reaction centre of PSII. The enhanced tolerance was caused by an acceleration of the repair of PSII from heat-enhanced photoinhibition, which might be due to a lower accumulation of ROS in transgenic plants (Yang et al., 2007). Moreover, it was found that heat stress caused oxidation of the PQ-pool in young 4-day-old barley leaves, inhibition of the linear electron flow due to partial impairment of the water oxidizing complex and the increase in the extent of QA (primary quinone) reoxidation by Tyrz (tyrosine Z) in thylakoids (Pshybytko et al., 2008). In 11-day-old leaves, heat treatment limited both photosynthetic electron flow and oxygen evolution. The decrease in size of the photoactive PQ-pool and a change in the proportions of oxidized and reduced PQ in the older leaves under heat treatment were also shown (Pshybytko et al., 2008). Based on these studies, it was concluded that a thermo-induced change in the redox state of the PQ-pool and a redistribution of PQ molecules between photoactive and non-photoactive pools are the mechanisms which reflect and regulate the response of the photosynthetic apparatus under heat stress conditions (Fig. 2).

Low temperature (0–15 °C) is common in natural conditions and leads to cellular damage in many plant species, limiting plants’ productivity and distribution (Theocharis et al., 2012). In non-tolerant plants, this damage occurs in the first hours of stress. While short exposure to low temperatures may only trigger transitory changes, prolonged exposure to stress causes plant necrosis or death. On the other hand, tolerant plants have the ability to re-organize their molecular and physiological parameters to counteract the destructive effects of the cold. This phenomenon, known as cold acclimation, is the central factor for plant cold tolerance (Theocharis et al., 2012).

Low temperature stress also inhibits the repair of PSII. There are many reports confirming that a low temperature stress inhibits the repair of PSII but does not affect the photodamage to PSII (Wada et al., 1994, Moon et al., 1995, Allakhverdiev and Murata, 2004). For example the labelling of proteins in Synechocystis cells demonstrated that the de novo synthesis of the D1 protein is suppressed at low temperatures (Allakhverdiev and Murata, 2004). Low-temperature stress also inhibits the process of the D1 precursor which is necessary for the assembly of the active PSII complex and the repair of PSII (Kanervo et al., 1997).

One of the major consequences of temperature stress is the excess generation of ROS, leading to oxidative stress (Munné-Bosch and Alegre, 2002). To some extent, plants are able to overcome the side-effects of temperature stress (Janska et al., 2010). As mentioned above, these processes cover all levels of plant organization. By metabolic alterations, plants protect proteins and cellular structures, can sustain cell turgor by osmotic adjustments or modify the antioxidant system to maintain the redox balance and cellular homeostasis (Janska et al., 2010, Hasanuzzaman et al., 2013). At the molecular level, temperature treatment alters the expression of the genes involved in protection against temperature stress (Shinozaki and Yamaguchi-Shinozaki, 2007, Semenov and Halford, 2009). Under temperature stress, the modulation of transcriptional activity seems to be critical for plant survival (Xiong and Zhu, 2001).

To reduce the temperature-dependent perturbations, plants improve their membrane thermostability and antioxidant capacity (Xu et al., 2006, Hameed et al., 2012). Within the temperature range 0–50 °C, antioxidant enzymes are severely affected. For example CAT, SOD and APX activity increased in a temperature-dependent manner up to 50 °C, with a subsequent decrease (Chakraborty and Pradhan, 2011). In contrast, POX and GR activities decreased between 20 and 50 °C. In temperature-sensitive plant varieties, total antioxidant activity was maximal at 30°C, whereas for tolerant varieties at 35–40°C (Suzuki and Mittler, 2006; Goyal and Asthir, 2010; Ahmad et al., 2010Ahmad et al., 2010Suzuki and Mittler, 2006; Goyal and Asthir, 2010; Ahmad et al., 2010 Ahmad et al., 2010). Increased activity of antioxidant enzymes is also correlated with freeze tolerance. In contrast to cold-sensitive tea plants, those that were cold-resistant showed a much higher activity of SOD and CAT (Luo et al., 2001). Thus, an improvement of antioxidant enzyme activity is also one of the effective ways to acquire cold resistance in plants. The introduction of the manganese SOD gene into the mitochondria and chloroplasts of alfalfa plants or copper-zinc SOD into tobacco, resulted in an improvement of freeze tolerance (McKersie et al., 1993, Chen et al., 2014a, Chen et al., 2014b). Investigations on cold-resistant plants have shown the high activity of antioxidant enzymes (Scebba et al., 1999). For example, higher CAT activity was observed in wheat under cold stress (Zhang et al., 2010).

The increased activity of antioxidant enzymes is not only correlated with temperature-tolerance, but predominantly with the stress response. At low temperatures, ROS production is enhanced and the activity of the antioxidant system declines, leading to lipid peroxidation (Maeda et al., 2005). Among the primary processes influenced by low temperature stress, photosynthesis is the main one (Allen and Ort, 2001). Many studies have shown that cellular membranes, including thylakoids, are the primary site of chill injury in plants (Zhang and Tian, 2009, Zhang et al., 2013, Khan et al., 2015). Membrane damage is an effect of the disruption of lipid structure, protein denaturation, and the leakage of solutes and free electrons, which is accompanied by ROS generation (Khan et al., 2015). In different plant species, the antioxidant response to low temperature stress depends on the time of exposure, and the temperature value. Pepper plants exposed to 8°C for 3 days showed oxidative stress symptoms and lipid peroxidation for the first 24 h (Ariaki et al., 2012). CAT and APX were induced, and the Asc and GSH content was increased. During the second and third days of low temperature treatment the pepper plants adjusted their antioxidant metabolism and diminished the oxidative stress observed during the early hours (Ariaki et al., 2012). When exposed to a range of low temperatures, Lycopersicon esculatum, showed a higher content of antioxidant enzymes (SOD, CAT and POX) and a decrease in lycopene and β-carotene content in fruits (Khan et al., 2015). Exposure to low temperature treatment caused a significant increase in H2O2 content (Khan et al., 2015).

Time- and range-related antioxidant responses have also been reported for elevated temperatures (above 30 °C) and heat. For example tobacco Bright-Yellow 2 cells at 35 °C were not affected, while 55 °C induced programmed cell death and 60 °C caused necrosis (Vacca et al., 2004; Locato et al., 2008). Rice seedlings exposed to heat (42 °C for 24 h) before low temperature treatment (5 °C for 7 d) did not develop temperature-dependent injury, but showed a higher level of APX activity and the induction of the expression of its gene. On the other hand, CAT activity decreased, while no significant difference in SOD activity was observed (Sato et al., 2001). Differences between temperature stress and acclimation were also shown by Sgobba et al. (2015). They exposed tobacco plants to short-term heat stress (6 h at 35 °C) and long-term high temperature stress (7 days at 35 °C). After the short-term stress, the antioxidant system was enhanced. In contrast, 3–5 days of long-term exposure caused a decrease in CAT and APX activity, with lower values for their activity than those in the control plants. In addition, H2O2 content increased and lipid peroxidation was observed (Sgobba et al., 2015). These data concur with the results obtained for radish plants (Chen et al., 2014a, Chen et al., 2014b). Three lines of Raphanus sativus plants with different heat resistances were subjected to elevated temperatures (40 °C day/30 °C night) for 9 days. The increase in H2O2 content, as well in SOD, APX and GR activity were observed after 1 day of exposure, and rose within 3 days. After that time, their activity decreased to the level observed in non-stressed plants by the 9th day (Chen et al., 2014a, Chen et al., 2014b). All these plants accumulated a lipid peroxidation product, i.e. malondialdehyde (MDA), gradually during the stress period. Li et al. (2015) subjected wheat plants to winter warming temperature, which was achieved by increasing the air temperature for 35 days, followed by 5 days of low temperature treatment. In chloroplasts, during the winter warming period, the H2O2 concentration was not affected and the activity of SOD and APX slightly increased. Under winter warming, CAT activity even decreased. The changes in enzyme activity under high temperature treatment indicate that these antioxidants are a part of the primary response mechanisms. This is also supported by an analysis of 45 Arabidopsismutants for basal and acquired thermotolerance. This showed that antioxidant enzyme mutants were more impaired in basal than in acquired thermotolerance (Larkindale et al., 2005) and indicates that survival at high temperatures requires the activation of several protective mechanisms, of which the maintenance of redox homeostasis seems to be most crucial for survival under elevated temperatures (Larkindale et al., 2005).

Recently, much attention has been paid to the role of low-molecular weight antioxidants, such as tocochromanols under temperature stress. Studies of cause-and-effect have produced differing results, but the response seems to be quite similar to those observed for antioxidant enzymes. It was shown that tocopherols play a crucial role in plant low-temperature acclimation (Havaux et al., 2005; Maeda et al., 2005). Arabidopsisplants exposed to 4 °C for 5 days had a slightly higher tocopherol content, whereas heat stress caused a 5-fold increase (Bermuller et al., 2003). An increase in α-tocopherol content has been reported in maize exposed to a long-term low temperature (Leipner et al., 2000). In contrast, in Eucalyptus sp. after 24 h of chilling conditions, the α-tocopherol content decreased (Kayal et al., 2006). In addition, the incubation of tomato plants at 2 °C for 72 h led to a decline in α-tocopherol content (Walker and McKersie, 1993). The same effect was observed for the Asc and GSH content in these plants. When subjected to 2 °C for 2 days, Arabidopsisshowed an initial increase in Asc and GSH content (after 12 h of chilling) followed by a decrease in both of them after 24 and 48 h (Wang et al., 2012). Cultivating Arabidopsisplants at elevated, but non-stress, temperatures led to an increase in Asc content and in APX activity (Panchuk et al., 2002). Long-term cultivation of ArabidopsisWT plants at elevated temperatures (34 °C) resulted in a gradual increase in Asc content, whereas short-term subjection to 37 °C and 44 °C caused a significant Asc decline (Panchuk et al., 2002).

The differences in antioxidant response, including both acclimation and the short-term effect of light or temperature, were studied in Arabidopsis thaliana accessions. They are perfect for studying natural variation in many physiological and molecular processes, including stress and antioxidant responses. This is because Arabidopsis thaliana is widely distributed and covers the Northern hemisphere from the equator to the Arctic circle (Alonso-Blanco and Koornneef, 2000). Hundreds of accessions have been collected over the last century throughout this geographical area. Accessions show significant genetic variability, allowing investigations into genotype and environment interactions (Alonso-Blanco and Koornneef, 2000). Recently, much attention has been paid to the highly different antioxidant responses of Arabidopsis thaliana accessions to light and temperature (Szymanska et al., 2015, Gabruk et al., 2016), which are known to have a tremendous effect on plant growth and development in terms of geographic latitude and longitude. Arabidopsis thaliana accessions collected from their natural environments exhibit natural variations in antioxidant response (Des Marais and Juenger, 2010, Zuther et al., 2012). A set of 25 accessions originating from a variety of climate conditions were grown for 5 weeks in different light and temperature combinations: 16 °C/LL, 23 °C/LL, 16 °C/LL and 23 °C/HL conditions (for LL and HL intensity was 100 and 380 μmol photons/m2/s, respectively) (Gabruk et al., 2016). It was shown that temperature, more so than light intensity, affects tocochromanol content and the expression of their biosynthetic genes (Szymanska et al., 2015, Gabruk et al., 2016). The same light and temperature conditions were applied to the study of the physiological and antioxidant responses of two accessions, Lov-5 and Sha (Szymanska et al., 2015). The results also showed pronounced differences in stress response between these two accessions. Distelbarth et al. (2013) compared H2O2 concentration, the activity of antioxidant enzymes and the extent of lipid peroxidation in four Arabidopsis thaliana accessions from the north to south range of this species grown under HL and cold conditions. While under HL all accessions showed oxidative stress symptoms, the effect of low temperature was not uniform for the accessions examined (Distelbarth et al., 2013).

A comparative analysis of temperature and developmental responses in seven northern Arabidopsis thaliana accessions showed that some of them regulate the chloroplast antioxidant system more on the level of polysomal RNA, whereas the Columbia-0 (Col-0) accession accumulated mRNA (Juszczak et al., 2012). These mechanisms led to effective antioxidant defense strategies in some accessions, whereas others were more susceptible and accumulated a high ROS content. Comparing the expressions of CuZnSOD and APX have shown high variation among accessions, which indicate that these plants use different strategies for antioxidant adjustments and protection (Juszczak et al., 2012).

In most stress-related experiments, the biological samples are treated in a specific way, and conclusions are often formulated based on transcript level (mRNA), an abundance of proteins, enzyme activity or any metabolite level (e.g. Oelze et al., 2012, Szechyńska-Hebda and Karpiński, 2013). In fact, a simple correlation between mRNA and protein content for a particular gene is often not obvious in plants (Fig. 3, Vélez-Bermúdez and Schmidt, 2014). The whole process of gene expression, from mRNA to a functional protein, is quite complicated and the mechanisms controlling their regulation are not entirely recognized (Liu et al., 2016). In this context, highly dynamic processes like short-term stress responses, which have lasted from a few to tens of minutes, may led to a strong shift between protein content/biological activity and their coding mRNAs (Fig. 3). In such cases, accurate conclusions about a decrease or an increase in mRNA/protein content may be incorrect. Even current technologies e.g. RNA-sequencing and high-resolution mass spectrometry do not yet allow us to draw precise conclusions that concern mRNA/protein abundance when stress-related experiments are performed in short timescales (Liu et al., 2016). Moreover, apart from determining changes at the molecular level, a response at the whole plant or even natural plant population level which includes e.g. photosynthesis intensity and seeds production is required in order for us to understand plant reactions to stress situations properly. For example, advances in non-destructive image-based phenotyping technologies are enabling parallel studies of plant growth and photosynthetic performance over time (Munns et al., 2010, Dhondt et al., 2013) by the use of RGB and chlorophyll fluorescence (ChlF) imaging (Brown et al., 2014). Therefore, we should bear this knowledge in mind and critically look at our own and other results.

Section snippets

Conclusions

Plants experience many environmental stress factors, of which light and temperature are of particular interest. Fluctuations in their intensity and range mainly affect photosynthesis. Thus, efficient protection is essential for plant survival and reproductive success. Plants are equipped with several protective mechanisms. These include CEF, the VAZ cycle, the photorespiratory pathway and ROS scavenging systems. Studies on plant antioxidant responses indicate the existence of a broad

Acknowledgements

AGH-University of Science and Technology and Jagiellonian University are partners of the Leading National Research Center (KNOW) supported by the Ministry of Science and Higher Education.

This work has been supported by the grant SonataUMO-2015/19/D/NZ9/00060 obtained by Renata Szymanska from National Science Centre. Jerzy Kruk acknowledges financial support from the grant 2015/19/B/NZ9/00422 obtained from the National Science Centre.

References (204)

  • D. DellaPenna et al.

    Vitamin E

    Adv. Bot. Res.

    (2011)
  • T. Endo et al.

    The role of chloroplastic NAD(P)H dehydrogenase in photoprotection

    FEBS Lett.

    (1999)
  • S. Frigerio et al.

    Photosynthetic antenna size in higher plants is controlled by the plastoquinone redox state at the post-transcriptional rather than transcriptional level

    J. Biol. Chem.

    (2007)
  • S.S. Gill et al.

    Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations

    Plant Physiol. Biochem.

    (2013)
  • J. Gruszka et al.

    Tocochromanols, plastoquinol and other biological prenyllipids as singlet oxygen quenchers −determination of singlet oxygen quenching rate constants and oxidation products

    Free Radic. Biol. Med.

    (2008)
  • M. Hakala et al.

    Evidence for the role of the oxygen evolving manganase complex in photoinhibition of photosystem II

    Biochim. Biophys. Acta

    (2005)
  • A. Haldrup et al.

    Balance of power: a view of the mechanism of photosynthetic state transitions

    Trends Plant Sci.

    (2001)
  • J.M. Koolhaas et al.

    Stress revisted: a critical evaluation of the stress concept

    Neurosci. Biobehav. Rev.

    (2011)
  • J. Kruk et al.

    An HPLC-based method of estimation of the total redox state of plastoquinone in chloroplasts, the size of the photochemically active plastoquinone-pool and its redox state in thylakoids of Arabidopsis

    BBA −Bioenergetics

    (2006)
  • J. Kruk et al.

    Singlet oxygen and non-photochemical quenching contribute to oxidation of the plastoquinone-pool under high-light stress in Arabidopsis

    BBA −Bioenergetics

    (2012)
  • J. Kruk et al.

    Plastochromanol-8: fifty years of research

    Phytochemistry

    (2014)
  • Y. Liu et al.

    On the dependency of cellular protein levels on mRNA abundance

    Cell

    (2016)
  • P. Ahmad et al.

    Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress

    Crit. Rev. Biotechnol.

    (2010)
  • T. Ahn et al.

    Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein

    Science

    (2008)
  • R.G. Alscher et al.

    Role of superoxide dismutases (SODs) in controlling oxidative stress in plants

    J. Exp. Bot.

    (2002)
  • S.I. Allakhverdiev et al.

    Bicarbonate is an essential constituent of the wateroxidizing complex of photosystem II

    Proc. Natl. Acad. Sci. U. S. A.

    (1997)
  • S.I. Allakhverdiev et al.

    Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis

    Plant Physiol.

    (2002)
  • S.I. Allakhverdiev et al.

    Heat stress: an overview of molecular responses in photosynthesis

    Photosynth. Res.

    (2008)
  • E.M. Aro et al.

    Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes

    J. Exp. Bot.

    (2005)
  • K. Asada

    The Water–Water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (1999)
  • K. Asada

    Production and scavenging of reactive oxygen species in chloroplasts and their functions

    Plant Physiol.

    (2006)
  • B. Asthir

    Protective mechanisms of heat tolerance in crop plants

    J. Plant Int.

    (2015)
  • J. Awad et al.

    2-cysteine peroxiredoxins and thylakoid ascorbate peroxidase create a water–water cycle that is essential to protect the photosynthetic apparatus under high light stress conditions

    Plant Physiol.

    (2015)
  • N.R. Baker

    Chlorophyll fluorescence: a probe of photosynthesis in vivo

    Annu. Rev. Plant Biol.

    (2008)
  • A.K. Banaś et al.

    Blue light signalling in chloroplast movements

    J. Exp. Bot.

    (2012)
  • A. Baxter et al.

    ROS as key players in plant stress signalling

    J. Exp. Bot.

    (2014)
  • S. Bellafiore et al.

    State transitions and light adaptation require chloroplast thylakoid protein kinase STN7

    Nature

    (2005)
  • B. Biswal et al.

    Photosynthesis, a global sensor of environmental stress in green plants: stress signalling and adaptation

    Curr. Sci. India

    (2011)
  • M.M. Borisova et al.

    Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins

    Biochim. Biophys. Acta

    (2012)
  • A. Bratt et al.

    Organelle redox autonomy during environmental stress

    Plant Cell Environ.

    (2016)
  • U. Chakraborty et al.

    High temperature-induced oxidative stress in Lens culinaris, role of antioxidants and amelioration of stress by chemical pre-treatments

    J. Plant Interact.

    (2011)
  • L.-J. Chen et al.

    An overview of cold resistance in plants

    J. Agro Crop Sci.

    (2014)
  • S. Choudhury et al.

    Reactive oxygen species in plants under abiotic stress

    Plant Signal. Behav.

    (2013)
  • F.K. Choudhury et al.

    Reactive oxygen species, abiotic stress and stress combination

    Plant J.

    (2016)
  • W.S. Chow et al.

    Photoinactivation of photosystem II in leaves

    Photosynth. Res.

    (2005)
  • E. Collakova et al.

    The role of homogentisate phytyltransferase and other tocopherol pathway enzymes in the regulation of tocopherol synthesis during abiotic stress

    Plant Physiol.

    (2003)
  • G. Cornic et al.

    Flexible coupling between light dependent electron and vectorial proton transport in illuminated leaves of C3 plants. Role of photosystem I-dependent proton pumping

    Plants

    (2000)
  • F.J. Corpas et al.

    Immunological evidence for the presence of peroxiredoxin in pea leaf peroxisomes and response to oxidative stress conditions

    Acta Physiol. Plant

    (2017)
  • G. Dąbrowska et al.

    Characteristics of the plant acrorbate peroxidase family

    Acta Biol. Cracov. Bot.

    (2007)
  • D. Des Marais et al.

    Pleiotropy, plasticity and the evolution of plant abiotic stress tolerance

    Ann. N. Y. Acad. Sci.

    (2010)
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