Next Article in Journal
Polyphenols in Almond Skins after Blanching Modulate Plasma Biomarkers of Oxidative Stress in Healthy Humans
Next Article in Special Issue
On the Origin and Fate of Reactive Oxygen Species in Plant Cell Compartments
Previous Article in Journal
Effect of the Phosphodiesterase 5 Inhibitor Sildenafil on Ischemia-Reperfusion-Induced Muscle Mitochondrial Dysfunction and Oxidative Stress
Previous Article in Special Issue
Amelioration of the Oxidative Stress Generated by Simple or Combined Abiotic Stress through the K+ and Ca2+ Supplementation in Tomato Plants
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

The Role of the Plant Antioxidant System in Drought Tolerance

Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Universitätsstr. 25, 33615 Bielefeld, North Rhine Westphalia, Germany
Author to whom correspondence should be addressed.
Submission received: 14 March 2019 / Revised: 30 March 2019 / Accepted: 2 April 2019 / Published: 8 April 2019
(This article belongs to the Special Issue Oxidative Stress in Plant)


Water deficiency compromises plant performance and yield in many habitats and in agriculture. In addition to survival of the acute drought stress period which depends on plant-genotype-specific characteristics, stress intensity and duration, also the speed and efficiency of recovery determine plant performance. Drought-induced deregulation of metabolism enhances generation of reactive oxygen species (ROS) and reactive nitrogen species (RNS) which in turn affect the redox regulatory state of the cell. Strong correlative and analytical evidence assigns a major role in drought tolerance to the redox regulatory and antioxidant system. This review compiles current knowledge on the response and function of superoxide, hydrogen peroxide and nitric oxide under drought stress in various species and drought stress regimes. The meta-analysis of reported changes in transcript and protein amounts, and activities of components of the antioxidant and redox network support the tentative conclusion that drought tolerance is more tightly linked to up-regulated ascorbate-dependent antioxidant activity than to the response of the thiol-redox regulatory network. The significance of the antioxidant system in surviving severe phases of dehydration is further supported by the strong antioxidant system usually encountered in resurrection plants.

1. Introduction

During their ontogenesis, plants face a dynamically changing environment defined by abiotic factors (e.g., light/dark, temperature, nutrient and water availability, and toxic compounds such as heavy metals) and biotic interactions (e.g., beneficial and pathogenic microbes, fungi, insects, other herbivores) [1]. Environmental perturbations which significantly disturb metabolism, development and yield, are considered as stress situations and cause stress responses in biological system. Such imposed stress is commonly accompanied by an increase in the production of reactive oxygen species (ROS) and reactive nitrogen species (RNS) that lead to an imbalance between their production and scavenging. Despite their reactive and thus toxic nature, ROS and RNS are also key components of signal transduction pathways that trigger stress responses. Furthermore, ROS and RNS are involved in plant developmental processes [2,3,4] and plant-microbe interactions [5,6]. However, excessive ROS and RNS production must be counteracted by the antioxidant system to prevent damage development and cell death.
Drought stress severely impacts plant development, growth and fertility. Drought triggers water loss and a decrease in water potential, which concomitantly leads to a reduction in cell turgor (Figure 1). Among the fastest processes induced by drought is the abscisic acid (ABA)-mediated closure of stomata [7]. Prolonged drought stress and increased stress intensity lead to further acclimation reactions. These responses include osmotic adjustment [8,9], decreased shoot-root ratio [10], cell wall modifications [11,12], reprogramming of metabolism [13], and activation of the antioxidant system [14,15]. Many of these modifications are measurable and are used to characterize the severity of drought stress. Measurable traits are, for example, the stomatal and mesophyll conductance, net photosynthesis, photorespiration, abundance of osmoprotectants, tissue water potential, ABA content and membrane integrity. Drought avoidance includes morphological adaptations, like leaf curling and increased wax deposition on the leaf surface [16] (Figure 1).
During evolution, plants developed mechanisms to acclimate to drought or even to withstand dry periods. Extensive research has unraveled the molecular mechanisms of drought and desiccation tolerance. Figure 2 summarizes characteristic features of drought-sensitive, drought-tolerant and desiccation-tolerant plants. Tolerant plants are equipped with higher levels of both osmolytes and non-protein antioxidants, reprogram their metabolism and enhance their antioxidant capacity. Interestingly, sensitive species also activate their antioxidant system. Nevertheless, despite this apparent contradiction, drought tolerance seems to be a function of the antioxidant capacity realized in response to drought. Furthermore, the antioxidant activity not only is important during acute drought stress, but also interferes with recovery from water limitation and resurrection from dehydration.
In the beginning of the review we will recall the classification of drought and how drought stress conditions are experimentally induced. This is important information to relate the production of ROS and RNS to the applied stress later in this review. Our review centers on the sites of production and roles of ROS and RNS during dehydration and their detoxification by the antioxidant system. Where possible we will correlate the activation of the antioxidative system to drought tolerance. Furthermore, we will evaluate which antioxidants are involved in drought response in particular. The last section describes the role of the antioxidative system in resurrection plants as an intriguing case of exceptional drought tolerance.

2. Classification and Application of Drought Stress

Drought is classified in mild, moderate and severe stages of stress (Table 1). The transition between the different stages occurs steadily and reflects the progression of drought stress severity both in duration and dehydration strength. Hence, an absolute value of dehydration cannot be assigned to the individual stages of drought stress. The stages are rather categorized in certain ranges. Various units have been used to describe water limitations (Table 1). The overall consensus is that the relative water content (RWC) in mild drought stress ranges between 60–70% compared to the control of ≥90%, in moderate stress between 40–60% and in severe stress between 0–40% (Table 1, Figure 1). Interestingly, these classifications are quite consistent between different species, even though the length of the applied stress to reach these states differs considerably (Table 1). Severe drought stress conditions can be reached rapidly within a week in soils with low water holding capacity. Mild stress conditions, corresponding to a soil field capacity (SFC) of 70%, are already reached after two days, severe (SFC < 50%) and very severe wilting (SFC < 30%) after five and eight days, respectively, as determined for 25 day-old soybeans grown in a sand-vermiculite mixture [17]. A time period of 1–2 weeks without watering was shown to be the most suitable condition for testing both drought tolerance and recovery of various mesophytic species grown on soil (Table 2). Drought stress can be induced either by withholding water in the case of soil-grown plants or by polyethylene glycol (PEG) in both agar-plates and liquid cultures [18]. The use of PEG-infused agar systems allows generating a defined water potential in the substrate [19]. However, the majority of these systems were only applicable for seedlings for a long time. Recently, Frolov and colleagues [20] established an agar-based polyethylene glycol infusion drought model for six-to-eight-week-old Arabidopsis plants. This system is extremely valuable as it allows analyzing the response of adult plants and thus a more appropriate developmental stage in terms of agricultural application.
The occurrence and severity of drought-induced injury varies between different developmental stages of the plant and also depends on duration and strength of the applied stress.

3. ROS and RNS Generation during Dehydration and Its Combination with Other Stresses

Stress-induced production of ROS and RNS occurs in different cell compartments [45]. They are used to transmit signals to the nucleus and other compartments to reprogram cell performance including gene expression [46,47]. The underlying mechanisms are known as retrograde and anterograde signaling pathways [1,48]. This paragraph focuses on the sources of ROS and RNS, and their accumulation in response to drought stress.

3.1. ROS during Drought

The first response of plants to drought is the closure of stomata in order to minimize water loss due to transpiration. Because of ongoing photosynthesis in the light, the increased gas diffusion barrier facilitates depletion of the intercellular carbon dioxide (CO2) concentration. Decreased availability of CO2 stimulates ribulose–1,5–bisphosphate oxygenation and, thus, photorespiratory hydrogen peroxide (H2O2) production in the peroxisomes. This effect has been studied in detail and was frequently summarized, e.g., with respect to drought and H2O2 production in wheat and potato as C3 field crops [49]. Insufficient availability of the electron acceptor CO2 slows down the oxidation of nicotinamide adenine dinucleotide phosphate (NADPH) in the Calvin–Benson cycle. Lack of NADP+ causes a backlog of electrons and over-reduction of the photosynthetic electron transport which in turn increases the reduction rate of oxygen as alternative electron acceptor in the Mehler reaction at photosystem I (PSI) and enhanced release of superoxide anion (O2) and hydrogen peroxide (H2O2). Hence, chloroplasts are primary targets of excess light and CO2 starvation in drought. In addition, photorespiration produces NADH in the mitochondrion.
A highly reduced chloroplast NADPH-pool via thioredoxin (TRX) reduction activates the NADPH-dependent malate dehydrogenase and, thereby, the malate valve for export of reducing equivalents to the cytosol and mitochondrion. The disequilibrium between electron supply and consumption in photosynthesis is efficiently transmitted to the respiratory electron transport chain (ETC) in the mitochondrion. Activation of alternative oxidase (AOX) and induction of aox gene expression are hallmarks of drought response [50,51,52]. Even under normal conditions, 1–2% of oxygen is consumed to produce ROS due to an over-reduction at complex I and III in the oxidative phosphorylation [53]. Under drought, the capacities of AOX, plant uncoupling proteins (PUCPs) and ATP-sensitive potassium channels are stimulated to dissipate excess electron flow in ETC [54]. Respiratory functions are inhibited by about two-thirds in drought-stressed plants as reviewed by Atkin and Macherel [55]. These studies included dehydration regimes of various intensities and on different time scales. The authors commented that the missing response in tolerant species might be due to enhanced antioxidant defense. Additionally, ROS are produced at the apoplast. Interestingly, the production of apoplastic ROS is coupled to calcium signaling [56]. Respiratory burst oxidase homolog (RBOH) proteins in the plasma membrane are calcium and phosphorylation-sensitive enzymes generating superoxide anions in the apoplast in response to drought, but also many other stresses [57,58]. Cell wall-associated kinases (WAKs) are members of the receptor-like kinase (RLK) family and participate in the perception of turgor pressure changes during drought probably linking ROS bursts with phosphorylation of RBOHs [59]. Apoplastic ROS also induce lipid peroxidation giving rise to malondialdehyde (MDA) as an indicator for membrane damage especially during drought. After dismutation of superoxide to H2O2 in the apoplast, transfer of H2O2 from the apoplast to the cytosol may also contribute to the intracellular ROS signature.
Table 3 summarizes changes of ROS and RNS amounts in response to drought stress. Maize growing in soil at 20% water saturation deficit accumulated twice the H2O2 amount of well-watered control plants [60]. Likewise, H2O2 reached thrice the contents of control rice if exposed to 200 mmol/L mannitol for two days [61,62] and in Ailanthus altissima plants that were kept unirrigated for 14 days [63], respectively. Thus, accumulation of ROS under drought is a prototypic case of stress-induced responses.

3.2. ROS, Oxidative Post-Translational Modifications and Redox Signalling

Within proteins, the thiol groups of both cysteine (Cys) and methionine (Met) are the major sites of oxidative post-translational modifications (PTMs) [90]. Thiols are prone to successive oxidation to sulfenic (R-SOH), sulfinic (R-SO2H), and sulfonic (R-SO3H) acids [91]. Cys oxidation and reduction efficiently regulates enzyme activities. A well-established system is the redox system of chloroplasts in which the redox input is provided by ferredoxin (Fd), NADPH and glutathione (GSH), redox signals are transmitted on target proteins by TRX, NADPH-thioredoxin reductase (NTRC) and glutaredoxins (GRX) [92]. Peroxiredoxins (PRX) are thought to sense the redox state of the cell and act in signaling instead of ROS detoxification [92]. Oxidative PTMs and the role of PRX in plant redox signaling are subjects of recent reviews and, thus, are not discussed in detail here [92,93].

3.3. RNS during Drought

Reactive nitrogen species are less diverse than ROS. Nitric oxide (NO) is a gaseous signaling molecule involved in germination, development, hormone regulation, and stress management. While homologues of animal NO synthase are absent from plants [94], the described mechanisms for NO production include (i) nitrate reductase (enzymatic, cytosol/plasma membrane), (ii) xanthine oxidoreductase (enzymatic, peroxisome), (iii) NO-associated proteins (enzymatic, mitochondria/plastids), (iv) nitrite: NO reductase (enzymatic, plasma membrane), (v) electron transport chain (non-enzymatic, mitochondria/chloroplast), and (vi) a poorly understood mechanism using arginine, polyamine or hydroxylamine [95,96,97]. The bioactive NO concentration is influenced by the nitrogen nutrient supply, the concentration of the storage compound nitrosoglutathione (GSNO), the activity of the GSNO reductase, and turnover mechanisms including the interaction with hemoglobins [98,99,100].
Osmotic stress, established by exposing rice roots to 200 mmol/L mannitol, increased the NO amount threefold within 24 h in rice leaves [61]. The same increase in NO was observed in rice after withholding irrigation for nine days, while a significant increase was undetected after three days [86]. Since both studies focused on leaves, the large time scale difference is striking and may reflect the time span needed to establish similar stress levels. This interpretation is supported by the fact that an osmotic shock treatment with 210 mmol/L mannitol corresponds to an applied osmotic potential of approximately −1.1 MPa [101], while an equivalent osmotic potential after withholding water was reached only at days 4 and 5 [86]. The data also point to changes in drought sensitivity during development. Most plants respond more sensitive to dehydration in early developmental stages. Therefore, one explanation for the discrepancies between the above mentioned studies might be attributed to differences in the plant growth stages of 16 [61] versus 42 days [86], leaving juvenile leaves more sensitive to drought. In this context, it should be mentioned that the ratio of developing to mature cell in the leaf lamina changes significantly during the early phase of development. Furthermore, the antioxidant response to paraquat was compromised in young Arabidopsis leaves [102]. Mature leaves were able to compensate ROS accumulation much more efficiently due to an increase in APX activity. The authors suggested different photoprotective regulatory mechanisms in the two leaf types. Furthermore, it was concluded that the redox-state of plastoquione A (QA) is the determinant of tolerance to paraquat-induced oxidative stress [102]. A similar observation was made in Fagus sylvatica L. Here, resistance to paraquat-induced oxidative stress was mediated by an increase in SOD activity in mature leaves [103]. In the tea plant (Camellia sinensis), cold-sensitivity of young leaves is correlated with inhibited expression of genes related to cell membranes, carotenoid metabolism, photosynthesis and the antioxidative system [104]. In contrast, transcripts belonging to the gene ontology groups of chloroplasts, cell membranes, redox processes, glutathione metabolism and photosynthesis were increased in mature leaves in response to cold. Hence, the antioxidative system plays an important role in establishing acclimation and hardening to stress.
In tree species like Ailanthus altissima, NO amounts increased three-fold after withholding water for 14 days [63]. NO is reported as an important positive regulator for Crassulacean acid metabolism (CAM) in pineapple leaves as described by Freschi et al. [79]. Emission of NO gradually increased from 40 to 140 pmol.h−1g−1 dry weight upon treatment with 30% PEG 6000 for 5 days. Of PEG, 30% corresponds to a water potential of −1.03 MPa [105] and, thus, is similar to osmotic stress induced by 200 mmol/L mannitol [87]. NO quantification was mostly achieved by using fluorescence probes like diaminofluorescein (DAF) or diaminorhodamine (DAR) derivates. To overcome drawbacks related to limited specificity, new probes are presently engineered to improve sensitivity and specificity [106]. Nevertheless, cell- and tissue-imaging with DAF-2 diacetate in dehydrating pineapples localized NO in chlorenchyma, trichoma and epithelial cells but did not resolve subcellular compartmentation.
NO also plays a significant role in regulating germination during drought in grasses like wheat and rice [87,107]. Endogenous NO counteracts programmed cell death and vacuolization induced by gibberellic acid. The NO amount in aleurone layers drops by 75% after 24 h of osmotic stress compared to controls (20% PEG-6000). Exogenous application of NO donors alleviates the effect and delays germination. Thus, a synergistic effect of NO is seen with ABA allowing postponing germination until growth conditions improve. Under such conditions, germination is inhibited and resumed only after growth conditions have improved. Expression of rat neuronal NO synthase (nNOS) in plants constitutively increases NO levels twofold in A. thaliana [80] and 1.5-fold in O. sativa [61]. These nNOS-plants accumulate more biomass and less H2O2 after withholding water for 14 d (A. thaliana) or upon treating rice with 200 mmol/L mannitol. These results assign a significant role to NO in shaping the acclimation to drought. They also show that the NO effect partly antagonizes the effects of ROS in this process.
In general, information on plant specific endogenous RNS signaling is still scarce. The production of NO occurs in similar subcellular compartments as ROS but our knowledge on its induction, regulation of enzyme activities, and substrates emerges only slowly. Hence, many groups use NO donors to artificially expose plants to RNS. Currently, research focuses on synergistic versus antagonistic effects of RNS and ROS, especially in the field of abiotic stress, and promises a more integrative concept. Experiments on genetic model systems are needed which link the dynamics of specific markers for RNS signaling with proteomic and transcriptomic analyses.

3.4. Nitrosylation by ONOO and GSNO

Antagonistic and synergistic effects relate to reaction products of RNS and ROS and antioxidants, respectively. Thus, GSNO forms by reaction of NO with reduced glutathione, while peroxynitrite (ONOO) forms at sites of simultaneous formation of O2 and NO. GSNO triggers S-nitrosylation, while ONOO causes tyrosine nitration. Several targets of these reactions are part of the antioxidant defense system like PRX, ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) and catalase (CAT) [108,109]. Especially during drought in Lotus japonicus NO amounts doubled in roots, but interestingly not in leaves [84]. S-nitrosylation of proteins is promoted in roots. The authors hypothesized that roots are prone to nitrosative stress, and leaves to oxidative stress.
Higher NO concentrations in roots compared to leaves were also reported in sugarcane [89] and bluegrass [110] and support this rule of thumb. One function of NO in roots concerns root patterning as described for pea, tomato, tobacco, and cucumber facing drought conditions [82,111,112,113]. Such differential effects have also been reported for pollen development and stigma function which respond preferentially to either RNS or ROS, respectively. Apparently, ROS and RNS play unique roles in developmental signaling which should be explored further [114]. Furthermore, GSNO serves as a mobile carrier of NO allowing for long distance signaling. In contrast, ONOO is highly reactive and characterized by a short half-life of 10 to 20 ms, and thus is discussed as a linker between ROS and RNS signaling [115]. Moreover, specific analyses are needed to clarify the NO-related effects on metabolism and to see whether RNS signaling is exclusively transmitted by ONOO and GSNO.

3.5. ROS/RNS in Stress Combinations with Drought

Responses to drought are accentuated if dehydration is combined with other abiotic stresses. Exceptions from this rule concern drought combined with ozone and high CO2. The antagonising effect is traced back to stomata closure triggered by ozone [116] or high CO2 [117]. Iyer and collegues [116] described this phenomenon in Medicago truncatula. Here, ROS levels increase in response to drought and ozone by 2-fold and 2.8-fold, respectively, compared to the well-watered condition. However, ROS levels in response to combined drought and ozone stress are indistinguishable from the control (well-watered plants). In contrast, NO levels are elevated only in response to drought by approximately 2-fold, while ozone has no effect. Simultaneous application of the two stresses again did not lead to significant changes. Interestingly, jasmonic acid and salicylic acid synthesis are induced after application of NO-donors in A. thaliana which might explain the mitigating effect of ozone in combination with drought [118]. Again, both reports vary in species and treatment, but indicate that RNS signaling is directly involved in stress response and alters the ROS effects.
In the natural environment, dry periods often coincide with high temperature and high light. Malondialdehyde (MDA) is an indicator for lipid peroxidation and oxidative damage and significantly increases in green tissue of citrus cultivars exposed to a combination of drought and heat (10 d, 40 °C). The increase is absent in single stress applications [119]. The stronger effect of a drought/heat combination is also seen in maize. Here, MDA levels increase by 225%, while the single applications elevated MDA levels by only 45% (−0.7 MPa PEG for 8 h) or 92% (2 °C/h increase from 28 to 42 °C for 8 h), respectively [120]. In cotton cultivars, no significant differences in H2O2 levels are observed for drought and combined drought/heat stress [121].
Combining heat (42 °C) and drought in succulent purslane for seven days doubles MDA content, while single stress treatments increase the MDA amount only by 20%. Interestingly, O2 amount raises 2.5-fold under heat and combined stress, but not in plants exposed to drought [122]. Surprisingly, the leaf H2O2 level decreases in grapevine upon deprivation from water for four days followed by treatment with heat (1 h, 42 °C) or high light (1 h, 2000 µmol quanta.s−1m−2) [123]. None of the double or triple stress treatments including drought alters the H2O2 amounts above the levels measured during control treatments. Significant variations between cultivars are only seen in single treatments and a heat/high light treatment.
These examples support the theory by Suzuki and colleagues [1] that the response to a combined stress is unique and cannot be simply extrapolated from the responses to single stresses. For instance, the response to stress combinations on signaling pathways and responses can be synergistic, antagonistic or independent. Antagonistic and, thus, positive interactions are observed for the combination of drought and high CO2 [124]. However, combined stress often leads to negative interactions, and the consequences are synergistic rather than additive [1]. This is also true for high light and drought [125]. Both, high light and drought realize an over-reduced state of photosynthetic ETC. With respect to high light the over-reduction is caused by an excess of light energy, while the over-reduction following drought is caused by a limited CO2 availability after stomatal closure and the concomitant inhibition of the Calvin–Benson cycle. Consequently, in both cases ROS and RNS are generated, but the ROS/RNS signatures differ in both cases [126].
The described examples demonstrate the importance to investigate plant responses and signaling pathways in combined stress. However, most laboratory studies on plant stress responses consider one stress at a time, whereas plants in the field usually are exposed to different stresses simultaneously. For example, drought stress is often accompanied by heat and high light intensities [117,127]. Therefore, it has to be kept in mind that any treatment applied under controlled growth chamber conditions fails to reflect field conditions. Ecotypes of the same plant species adopt distinct adaptive responses to acclimate to their local habitats. Such naturally occurring biodiversity in terms of sensitivity vs. tolerance of closely related species, the extreme adaptability of specialists and the special case of crop plant monocultures cannot be treated in this review focusing on ROS and RNS-dependent signaling.

4. Response of the Redox Network under Drought

The activation of the antioxidant system via retrograde signaling is a key process in plant acclimation to oxidative stress. Thus, the upregulation of antioxidant enzymes represents an important marker for drought stress. In the cell, the production and scavenging of ROS and RNS is strictly controlled and the equilibrium can be perturbed by several biotic and abiotic stresses [128]. Plants have evolved complex redox signaling networks in which ROS and RNS are used as signals to regulate normal and stress-related physiological processes including antioxidant mechanisms to combat the toxic effects of ROS and RNS [129,130]. Plants keep ROS under control by an efficient and versatile scavenging system. The antioxidant defense comprises low molecular weight compounds such as GSH, ascorbate (ASC), α-tocopherol, carotenoids, and enzymes including CAT, SOD, and the thiol peroxidases of the PRX and glutathione peroxidase (GPX) type [131].
Thiol peroxidases are linked to the NADPH-thioredoxin reductase (NTR), ferredoxin-dependent TRX reductase (FTR) and GSH/GRX systems [132,133]. Mechanism of ROS production and their scavenging by high antioxidant capacity has been associated with tolerance of plants to abiotic stresses [128]. Recently, a new function was assigned to thiol peroxidases in redox regulation, namely as TRX oxidases [134]. This mechanism allows for reading out the balance between reductive electron input and oxidative electron drainage and tunes the redox and activity state of target proteins.

4.1. Effect of Drought Stress on the Antioxidant System and Redox Homeostasis

During drought stress, up-regulation of antioxidant systems occurs at both the transcriptional and post-transcriptional level. Table 4 gives examples for quantitative drought responses of antioxidative enzymes and enzymes involved in regeneration of non-protein antioxidants. APX, catalase (CAT) and GPX represent the principal ROS scavengers in plants. Among these three, APX appears to be induced most strongly on post-transcriptional level (Table 4). In contrast to CAT and GPX, APX is also regulated on transcriptional level based on the data summarized in Table 4. Cytosolic, chloroplastic and peroxisomal APX activities are commonly enhanced in all species of the plant kingdom. The activity of cytosolic APX is increased during drought in pea [135]. The alx8 mutant (altered expression of APX2) of Arabidopsis reveals improved drought tolerance [136,137]. Over-expression of peroxisomal or cytosolic APX from poplar in transgenic tobacco increases plant performance under drought [138,139]. CAT is a tetrameric, heme-containing enzyme that catalyzes the dismutation of H2O2 into H2O and O2 in the peroxisome. CAT2 plays a crucial role when the plant is exposed to a severe drought stress [140]. Compared to APX activation, stimulation of CAT is moderate (Table 4). Even though CAT activation seems predominantly taking place on post-transcriptional level, there are examples for complex regulation of CAT activity under severe drought which involves gene expression, translation and protein turnover [141].
Besides APX, other components of the ASC-GSH cycle, namely MDHAR, DHAR, glutathione-S-transferase (GST) and glutathione reductase (GR), work synergistically in different cell compartments. MDHAR, DHAR, GST and GR transcripts and activity are predominantly induced under drought stress (Table 4). Among these four enzymes, GR is activated strongest. GR activation can be compared to the one observed for CAT. In general, upregulation of the ASC-GSH metabolism and associated enzymes efficiently scavenge H2O2 under drought stress as observed in wheat [167].
Moreover, PRXs are also up-regulated and accumulated in cotton [150], date palm [151] and wheat [161] upon drought (Table 4). This indicates that plants activate compensatory mechanisms to counteract enhanced H2O2 production in response to drought stress. In addition to their reductive function in detoxifying H2O2, alkyl hydroperoxide and ONOO, PRX play a role in redox signaling and transmit information on the cell ROS state to target proteins [134,168].
SODs are a class of metalloenzymes that catalyze the dismutation of two molecules of O2 into molecular oxygen and H2O2. The activation of SOD isoforms (Mn-SOD, Fe-SOD, Cu,Zn-SOD) is interpreted as a measure to counteract O2 accumulation in diverse cell compartments under drought in e.g., Arabidopsis [158], blue grass [160], citrus [147], Coffea canephora [148], date palm [151], fescue [160], pea [135], poplar [153], tepary bean [145] and wheat [159]. Apparently, SOD is a critical component of the ROS-scavenging system likely by minimizing the reaction of O2 with, e.g., NO to form ONOO, unsaturated fatty acids for peroxidation or with proteins. In line with this assumption transgenic plants overexpressing Cu,Zn-SOD are more tolerant to drought stress [168].
A set of other important proteins belonging to the TRX superfamily is usually highly activated under drought stress. In general, TRXs are induced under different environmental stresses including dehydration, salinity, heat or cold [169]. Under several stresses, atypical and canonical TRX have the capacity to reduce oxidized antioxidant enzymes in the chloroplast, cytosol and mitochondria [170,171]. TRXs are localized in cytosol, chloroplast, mitochondrion, endoplasmic reticulum and nucleus [132]. Strongly responding oxidoreductases are represented by atypical chloroplastic TRX (CDSP32 and CDSP34), cytosolic or mitochondrial NADPH-TRX reductase (NTRA or B), endoplasmic reticulum-associated protein disulfide isomerase (PDI) and canonical cytosolic TRX (TRX h). NTRA-overexpressing plants exhibit extreme drought tolerance with high survival rates, low water loss and reduced ROS accumulation compared to wildtype and ntra-knock out plants [144]. However, TRX transcripts and activity measurements in date palm [151] and wheat [161] also indicate a down-regulation of some TRX members in response to drought stress.

4.2. Distinct Patterns of Antioxidative Sytem Activation in Sensitive and Tolerant Species

As summarized in Figure 2, drought-sensitive species also activate their antioxidative system. The data given in Table 4 confirm this assumption. However, they point out that not only the magnitude of activation might be decisive but also which enzymes are activated. For instance, the activation of the major scavenger APX and CAT is stronger in tolerant species compared to their sensitive counterparts. In contrast, sensitive species activate GPX more than tolerant species. Changes in the activation of the antioxidant system between sensitive and tolerant species are visualized in Figure 3. Obviously, sensitive plants predominantly activate the glutathione-dependent scavenging system, while the ascorbate-dependent system is only induced moderately or are even down-regulated (Figure 3). On the other hand, tolerant species showed a stronger activation of ascorbate-dependent scavenging system compared to the glutathione-dependent system. Moreover, inactivation is only apparent for the TRX-dependent scavenging system in tolerant species. Because drought stress leads to an over-reduction of the electron transport chain, down-regulation of TRX may counteract excessive reduction of target proteins. On the other hand, TRX-dependent reduction of PRX is compromised under this condition. However, PRX can be regenerated by other enzymes like GRX and NTRC [92]. Moreover, drought conditions necessitate a high capacity of detoxifying enzymes such as APX and CAT to suppress ROS accumulation. Furthermore, PRX are involved in redox-signaling [92] which might be their predominant function under drought stress.
There is not much information on drought tolerance and NO signaling. However, a recent study investigated root extracellular and leaf intracellular NO contents in drought-tolerant and –sensitive sugarcane genotypes. Here, drought tolerance was correlated with an increased extracellular NO concentration due to an increased nitrate reductase (NR) activity [89]. Furthermore, the simultaneous decrease in S-nitrosoglutathione reductase (GSNOR) implicates that tolerant plants possess a higher GSNO reservoir. As mentioned before, GSNO is a mobile carrier of NO allowing long distance transport. As observed for roots, likewise, the leaf intracellular NO content was elevated in the tolerant species when compared to the sensitive [89].
When evaluating the role of the ascorbate- and glutathione-dependent pathways in drought tolerance, it must be taken into consideration that the basal levels of the different antioxidants in sensitive and tolerant species were not compared. However, Arabidopsis plants lacking the cytosolic APX1 show a collapse in the entire chloroplast-located H2O2-scavenging system, which is accompanied with increased H2O2 levels and protein oxidation, respectively [172]. In a direct comparison with TRX-dependent peroxidase activity, APX activity was 7-fold and 2-fold higher in leaf extracts and chloroplasts, respectively [173]. Thus, a predominant role of the ascorbate-dependent antioxidative system should be assumed. At this point, a deeper screen through the literature may not be helpful to test the hypothesis since most studies only present data on changes of selected antioxidant enzymes in a few tolerant and sensitive species. Future investigations should explicitly address the hypothesized role of the ascorbate-dependent ROS defense in drought tolerance in tolerant and sensitive genotypes within plant families. If the hypothesis can be confirmed, the ascorbate-dependent scavenging system can be a target for improving plant tolerance towards drought in biotechnological application.

5. The Role of the Antioxidative System in Desiccation Tolerance

Drought stress induces major transcriptional reprogramming in plants via ABA-dependent and ABA-independent pathways regardless whether a plant is sensitive or tolerant to drought. This is also true for resurrection plants. Research has shown that resurrection plants use similar mechanisms and strategies to respond and adapt to drought as sensitive species. However, if processes like perception, signaling and responses are as similar as assumed, which specific features provoke the tolerance to desiccation of vegetative tissues? The major difference to drought-sensitive plants is that the protective machinery of resurrection plants is held in an activated, ‘primed’ state. To achieve this, the basal levels of osmolytes like sugars and polyamines, non-enzymatic and enzymatic antioxidants are often increased in desiccation tolerant plants. High levels of sugars like trehalose, sucrose and raffinose prevent protein denaturation, stabilize membranes and act as ROS scavengers [174,175]. In addition, unique sugars such as the C8-sugar octulose also accumulate to up to 90% of the soluble sugars in photosynthetically active leaves [176]. Despite this, Djilianov and colleagues [177] found that the initial Suc/Fru ratio is increased in the desiccation-tolerant plant H. rhodopensis compared to the sensitive species C. eberhardtii. The differences and similarities between drought sensitivity, and drought and desiccation tolerance are compiled in Figure 3.
Significant evidence indicates that the strong antioxidant status is a prerequisite of desiccation tolerance in resurrection plants. Thus, glutathione is suggested to be an important player in the dehydration response [178]. The non-enzymatic antioxidants ascorbate and glutathione turn more oxidized during dehydration [177,179], while the total glutathione content increases. The increase in GSSG remains elevated during desiccation of the tolerant species H. rhodopensis. In addition, activities of antioxidant enzymes like SOD, peroxidase POD), CAT and GR increase in response to drought in the fern Selaginella tamariscina [180]. Resurrection plants are well equipped with genes encoding antioxidant enzymes. For instance, H. rhodopensis contains more genes encoding SOD, CAT, MDHAR and GR than the model plant A. thaliana [181]. The H. rhodopensis genome encodes eight catalase genes and, thus, five more than the Arabidopsis genome [181]. Expression of specific Cat genes is upregulated following drought/desiccation. The importance of CAT activity during desiccation is shown by an experiment in which leaves were sprayed with the catalase inhibitor 3-aminotriazole (0.1 mmol/L 3-AT). Plants that were treated by 3-AT never recover completely from desiccation and die within a month after the treatment [181]. The increased sensitivity of dehydrating plants to CAT inhibitors is interpreted as indication of enhanced photorespiration due to stomatal closure, lack of intercellular CO2, enhanced oxygenation of RUBISCO and therefore stimulated release of H2O2 by glycolate oxidase in the peroxisome. CAT is needed to detoxify the released H2O2 and therefore inhibited CAT disturbs redox and ROS homeostasis under drought.
Wang and colleagues [180] compiled drought/dehydration-responsive proteins from both resurrection and common plants [180]. The comparison of tolerant with sensitive phenotypes highlights the role of the antioxidant system in drought tolerance. For instance, CAT, APX and SOD levels are up-regulated in the drought-tolerant CE704 genotype (maize), while CAT and APX levels decreased in the drought-sensitive genotype 2023 [182]. In wheat, TRX-h and glutathione S-transferase are selectively upregulated in the drought-tolerant genotype Khazar-1 [161].
It should be noted that dehydration tolerance depends on additional features of the plants apart from adjusting metabolism including the antioxidant system. Massive water loss usually causes mechanical disruption in hygrophytic and mesophytic plants, e.g., the rupture of the tonoplast/plasmamembrane/cell wall junctions. Such irreversible mechanical damage is prevented in resurrection plants such as Craterostigma plantagineum where the tissue shrinks proportionally to the water loss. Thus, special anatomical properties like leaf curling and structurally flexible vessels are important features of dehydration tolerance [183,184].

6. Conclusion and Perspective

Drought tolerance depends on conditional activation of the acclimation program during initial phases of water loss. This also applies for thallophytic and cormophytic resurrection plants which need a hardening period for full expression of the tolerance trait [183,185]. As pointed out in this review, different drought stress regimes and time points of analysis result in distinct states of the ROS and RNS network and the antioxidant defense system. In the initial phases of dehydration, the activation of the hardening program decisively involves the generation of ROS and RNS which assist in activating the redox regulatory network and appropriate gene expression and protein accumulation. It was out of focus of this review to describe the intimate link between ROS, RNS and hormone signaling like salicylic acid and abscisic acid [186]. In the end ROS and RNS define a regulatory framework of the cell and contribute to link the stress impact to gene expression and whole plant performance [187].
At present our knowledge on specific subcellular ROS, RNS and redox patterns still falls short of the requirements for understanding the drought acclimation response in its entirety. Cell imaging with roGFP for glutathione redox state [188] and Hyper for H2O2 [189] will provide important insight on subcellular responses. In addition, in depth redox proteomics detecting the redox state of also low abundant proteins will provide a global view with subcellular resolution.
There is a need to assess the various PTMs in the proteome simultaneously. This is a challenge for current proteomics which for technical reasons often focuses on single or few PTMs only [190]. As functional readout of ROS and RNS, such approaches will realize the necessary temporal and spatial resolution since ROS and RNS partly antagonize each other. Nevertheless, the presence of both reactive species is necessary for full drought acclimation. Additionally, the reaction of NO with O2 generates the highly reactive ONOO which directly nitrates proteins. Cysteine oxidation and tyrosine nitrations are PTMs that change the activity of its target enzymes. Proteomics may tackle this challenge.
Along with the activation of the antioxidative system, other stress markers often increase during periods of progressive dehydration, e.g., H2O2 as indicator of redox imbalance, MDA as lipid oxidation product, glyoxylate linked to photorespiration, glutathione as antioxidant, glutamate and proline as precursor and compatible solute, and zeaxanthin with its role in photoprotection. The consensus of what defines drought tolerance is that many traits are needed to prevent biochemical or physiological impairment during water deficit. Several traits contribute to drought tolerance and include reduced water loss, build-up of osmotic potential, synthesis of compatible solutes, dissipation of excess energy, activation of antioxidant defense and repair systems, generation of sclerenchymatic tissue, strengthening the plasmamembrane-cell wall interaction and other mechanisms of growth adjustment such as differentiation of smaller leaves. The recovery from water depletion is affected by light intensity with often negative interference, i.e., slower recovery at high light.
Taken together, strategies to improve drought tolerance in crops need to target several metabolic pathways at the same time. Certainly, the activation of the antioxidative system following drought is one important goal. Attention should also be drawn to the pathways that are selected to increase drought tolerance. In the first instance, overexpressing of certain enzymes can lead to a beneficial increase in drought tolerance, but may delay germination and development for months and, thus, interfere with the growing season. Thus, biotechnological approaches should take into account the temporal and spatial signaling aspect in drought stress acclimation.

Author Contributions

Each author wrote a specific section of this review and commented on the whole manuscript. M.L.(Miriam Laxa) (Section 1, Section 2, Section 4.2, Section 5; manuscript editing, coordination and formatting); M.L.(Michael Liebthal) (Section 3); W.T. and K.C. (Section 4); K.J.-D. (abstract; Section 6; manuscript editing).


Support of the own work by the Deutsche Forschungsgemeinschaft is gratefully acknowledged (Di 364/17-2; SPP 1710). The publication of this article was funded by the Open Access Fund of Bielefeld University.

Conflicts of Interest

The authors declare no conflict of interest.


ABAabscisic acid;
AOXalternative oxidase;
APXascorbate peroxidase;
CAMcrassulacean acid metabolism,
CO2carbon dioxide;
DHARdehydroascorbate reductase;
ELIPearly light inducible protein;
Suc/Frusucrose to fructose ratio;
ETCelectron transport chain;
FTRferredoxin-dependent TRX reductase;
GPXglutathione peroxidase;
GPXglutathione peroxidase;
GRglutathione reductase;
GSNORS-nitrosoglutathione reductase;
GSTglutathione-S transferase;
H2O2hydrogen peroxide;
HSHoagland solution;
HSPheat shock protein;
LEAlate embryogenesis abundant protein;
MDHARmonodehydroascorbate reductase;
MWHCmaximum water holding capacity;
NAD+/NADHoxidized/reduced nicotinamide adenine dinucleotide;
NADP+/NADPHoxidized/reduced nicotinamide adenine dinucleotide phosphate;
NOnitric oxide;
NRnitrate reductase;
NTRNADPH–thioredoxin reductase;
NTRCNADPH-dependent thioredoxin reductase C;
O2molecular oxygen;
O2superoxide anion;
PDIprotein disulfide isomerase;
PEGpolyethylene glycol;
PTMposttranslational modification;
PSIphotosystem I;
PUCPsplant uncoupling proteins;
RBOHrespiratory burst oxidase homolog;
RLKreceptor-like kinase;
RNSreactive nitrogen species;
ROSreactive oxygen species;
RWCrelative water content;
SFCsoil field capacity;
SODsuperoxide dismutase;
SWCsoil water content;
WAKscell wall-associated kinases


  1. Suzuki, N.; Rivero, R.M.; Shulaev, V.; Blumwald, E.; Mittler, R. Abiotic and biotic stress combinations. New Phytol. 2014, 203, 32–43. [Google Scholar] [CrossRef] [PubMed]
  2. Corpas, F.J.; Barroso, J.B. Functions of nitric oxide (NO) in roots during development and under adverse stress conditions. Plants 2015, 4, 240–252. [Google Scholar] [CrossRef] [PubMed]
  3. Sanz, L.; Albertos, P.; Mateos, I.; Sánchez-Vicente, I.; Lechón, T.; Fernández-Marcos, M.; Lorenzo, O. Nitric oxide (NO) and phytohormones crosstalk during early plant development. J. Exp. Bot. 2015, 66, 2857–2868. [Google Scholar] [CrossRef]
  4. Mhamdi, A.; Van Breusegem, F. Reactive oxygen species in plant development. Development 2018, 145. [Google Scholar] [CrossRef]
  5. Maier, J.; Hecker, R.; Rockel, P.; Ninnemann, H. Role of nitric oxide synthase in the light-induced development of sporangiophores in Phycomyces blakesleeanus. Plant Physiol. 2001, 126, 1323–1330. [Google Scholar] [CrossRef] [PubMed]
  6. Segal, L.M.; Wilson, R.A. Reactive oxygen species metabolism and plant-fungal interactions. Fungal Genet. Biol. 2018, 110, 1–9. [Google Scholar] [CrossRef] [PubMed]
  7. Pirasteh-Anosheh, H.; Saed-Moucheshi, A.; Pakniyat, H.; Pessarakli, M. Stomatal responses to drought stress. In Water Stress and Crop Plants: A Sustainable Approach; Wiley Blackwell: Oxford, UK, 2016; Volume 1. [Google Scholar]
  8. An, Y.; Zhang, M.; Liu, G.; Han, R.; Liang, Z. Proline accumulation in leaves of Periploca sepium via both biosynthesis up-regulation and transport during recovery from severe drought. PLoS ONE 2013, 8, e69942. [Google Scholar] [CrossRef] [PubMed]
  9. Blum, A. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ. 2017, 40, 4–10. [Google Scholar] [CrossRef]
  10. Silva, D.D.; Kane, M.E.; Beeson, R.C. Changes in root and shoot growth and biomass partition resulting from different irrigation intervals for Ligustrum japonicum Thunb. Hortic. Sci. 2012, 47, 1634–1640. [Google Scholar] [CrossRef]
  11. Cho, S.K.; Kim, J.E.; Park, J.A.; Eom, T.J.; Kim, W.T. Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett. 2006, 580, 3136–3144. [Google Scholar] [CrossRef]
  12. Lü, P.; Kang, M.; Jiang, X.; Dai, F.; Gao, J.; Zhang, C. RhEXPA4, a rose expansin gene, modulates leaf growth and confers drought and salt tolerance to Arabidopsis. Planta 2013, 237, 1547–1559. [Google Scholar] [CrossRef]
  13. Zhang, J.Y.; Cruz de Carvalho, M.H.; Torres-Jerez, I.; Kang, Y.; Allen, S.N.; Huhman, D.V.; Tang, Y.; Murray, J.; Sumner, L.W.; Udvardi, M.K. Global reprogramming of transcription and metabolism in Medicago truncatula during progressive drought and after rewatering. Plant Cell Environ. 2014, 37, 2553–2576. [Google Scholar] [CrossRef] [PubMed]
  14. Ajithkumar, I.P.; Panneerselvam, R. ROS scavenging system, osmotic maintenance, pigment and growth status of Panicum sumatrense roth. under drought stress. Cell Biochem. Biophys. 2014, 68, 587–595. [Google Scholar] [CrossRef] [PubMed]
  15. He, F.; Sheng, M.; Tang, M. Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Front. Plant Sci. 2017, 8, 183. [Google Scholar] [CrossRef] [PubMed]
  16. Kim, K.S.; Park, S.H.; Jenks, M.A. Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit. J. Plant Physiol. 2007, 164, 1134–1143. [Google Scholar] [CrossRef] [PubMed]
  17. Ramos, M.L.G.; Gordon, A.J.; Minchin, F.R.; Sprent, J.I.; Parson, R. Effect of water stress on nodule physiology and biochemistry of a drought tolerant cultivar of Common Bean (Phaseolus vulgaris L.). Ann. Bot. 1999, 83, 57–63. [Google Scholar] [CrossRef]
  18. Osmolovskaya, N.; Shumilina, J.; Kim, A.; Didio, A.; Grishina, T.; Bilova, T.; Keltsieva, O.A.; Zhukov, V.; Tikhonovich, I.; Tarakhovskaya, E.; et al. Methodology of drought stress research: Experimental setup and physiological characterization. Int. J. Mol. Sci. 2018, 19, 4089. [Google Scholar] [CrossRef] [PubMed]
  19. Van der Weele, C.M.; Spollen, W.G.; Sharp, R.E.; Baskin, T. Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. J. Exp. Bot. 2000, 51, 1555–1562. [Google Scholar] [CrossRef]
  20. Frolov, A.; Bilova, T.; Paudel, G.; Berger, R.; Balcke, G.U.; Birkemeyer, C.; Wessjohann, L.A. Early responses of mature Arabidopsis thaliana plants to reduced water potential in the agar-based polyethylene glycol infusion drought model. J. Plant Physiol. 2017, 208, 70–83. [Google Scholar] [CrossRef]
  21. Guo, Y.; Zhao, S.; Zhu, C.; Chang, X.; Yue, C.; Wang, Z.; Lin, Y.; Lai, Z. Identification of drought-responsive miRNAs and physiological characterization of tea plant (Camellia sinensis L.) under drought stress. BMC Plant Biol. 2017, 17, 211. [Google Scholar] [CrossRef]
  22. Clauw, P.; Coppens, F.; De Beuf, K.; Dhondt, S.; Van Daele, T.; Maleux, K.; Storme, V.; Clement, L.; Gonzalez, N.; Inzé, D. Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol. 2015, 167, 800–816. [Google Scholar] [CrossRef]
  23. Ma, X.; Sukiran, N.L.; Ma, H.; Su, Z. Moderate drought causes dramatic floral transcriptomic reprogramming to ensure successful reproductive development in Arabidopsis. BMC Plant Biol. 2014, 14, 164. [Google Scholar] [CrossRef]
  24. Vicente, C.S.L.; Pérez-Fernández, M.A.; Pereira, G.; Tavares-de-Sousa, M.M. Biological nitrogen fixation of Biserrula pelecinus L. under water deficit. Plant Soil Environ. 2012, 58, 360–366. [Google Scholar] [CrossRef]
  25. Qiang, M.; Fei, L.; Liu, Y. Regulated deficit irrigation promoting growth and increasing fruit yield of jujube trees. Trans. Chin. Soc. Agric. Eng. 2015, 31, 91–96. [Google Scholar]
  26. Németh-Zámbori, É.; Pluhár, Z.; Szabó, K.; Malekzadeh, M.; Radácsi, P.; Inotai, K.; Komáromi, B.; Seidler-Lozykowska, K. Effect of water supply on growth and polyphenols of lemon balm (Melissa officinalis L.) and thyme (Thymus vulgaris L.). Acta Biol. Hung. 2016, 67, 64–74. [Google Scholar] [CrossRef]
  27. Liang, B.; Gao, T.; Zhao, Q.; Ma, C.; Chen, Q.; Wie, Z.; Li, C.; Li, C.; Ma, F. Effects of exogenous dopamine on the uptake, transport, and resorption of apple ionome under moderate drought. Front. Plant Sci. 2018, 9, 755. [Google Scholar] [CrossRef]
  28. Wang, C.; Liu, S.; Dong, Y.; Zhao, Y.; Geng, G.; Xia, X.; Yin, W. PdEPF1 regulates water-use efficiency and drought tolerance by modulating stomatal density in poplar. Plant Biotechnol. J. 2016, 14, 849–860. [Google Scholar] [CrossRef]
  29. Ribas-Carbo, M.; Taylor, N.L.; Giles, L.; Busquets, S.; Finnegan, P.M.; Day, D.A.; Lambers, H.; Medrano, H.; Berry, J.A.; Flexas, J. Effects of water stress on respiration in soybean leaves. Plant Physiol. 2005, 139, 466–473. [Google Scholar] [CrossRef]
  30. Sánchez-Rodríguez, E.; Rubio-Wilhelmi, M.D.; Cervilla, L.M.; Blasco, B.; Rios, J.J.; Leyva, R.; Romero, L.; Ruiz, J.M. Study of the ionome and uptake fluxes in cherry tomato plants under moderate water stress conditions. Plant Soil 2010, 335, 339–347. [Google Scholar] [CrossRef]
  31. Mustafavi, S.H.; Shekari, F.; Hatami-Maleki, H.; Nasiri, Y. Effect of water stress on some quantitative and qualitative traits of Valerian (Valeriana officinalis L.) plants. Bull. UASVM Hortic. 2016, 73, 1–8. [Google Scholar] [CrossRef]
  32. Wang, X.; Vignjevic, M.; Jiang, D.; Jacobsen, S.; Wollenweber, B. Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J. Exp. Bot. 2014, 65, 6441–6456. [Google Scholar] [CrossRef]
  33. Olsovska, K.; Kovar, M.; Brestic, M.; Zivcak, M.; Slamka, P.; Shao, H.B. Genotypically identifying wheat mesophyll conductance regulation under progressive drought stress. Front. Plant Sci. 2016, 7, 1111. [Google Scholar] [CrossRef]
  34. Fang, Y.; Du, Y.; Wang, J.; Wu, A.; Qiao, S.; Xu, B.; Zhang, S.; Siddique, K.H.M.; Chen, Y. Moderate drought stress affected root growth and grain yield in old, modern and newly released cultivars of winter wheat. Front. Plant Sci. 2017, 8, 672. [Google Scholar] [CrossRef] [PubMed]
  35. Tschaplinski, T.J.; Abraham, P.E.; Jawdy, S.S.; Gunter, L.E.; Martin, M.Z.; Engle, N.L.; Yang, X.; Tuskan, G.A. The nature of the progression of drought stress drives differential metabolomic responses in Populus deltoids. Ann. Bot. 2019. [Google Scholar] [CrossRef]
  36. Nayyar, H.; Gupta, D. Differential sensitivity of C3 and C4 plants to water deficit stress: Association with oxidative stress and antioxidants. Environ. Exp. Bot. 2006, 58, 106–113. [Google Scholar] [CrossRef]
  37. Li, X.; Li, G.; Li, Y.; Kong, X.; Zhang, L.; Wang, J.; Li, X.; Yang, Y. ABA receptor subfamily III enhances abscisic acid sensitivity and improves the drought tolerance of Arabidopsis. Int. J. Mol. Sci. 2018, 19, 1938. [Google Scholar] [CrossRef]
  38. Nakabayashi, R.; Mori, T.; Saito, K. Alternation of flavonoid accumulation under drought stress in Arabidopsis thaliana. Plant Signal. Behav. 2014, 9, e29518. [Google Scholar] [CrossRef]
  39. Ge, H.; Li, X.; Chen, S.; Zhang, M.; Liu, Z.; Wang, J.; Li, X.; Yang, Y. The expression of CARK1 or RCAR11 driven by synthetic promoters increases drought tolerance in Arabidopsis thaliana. Int. J. Mol. Sci. 2018, 19, 1945. [Google Scholar] [CrossRef] [PubMed]
  40. Gao, Y.; Wu, M.; Zhang, M.; Jiang, W.; Ren, X.; Liang, E.; Zhang, D.; Zhang, C.; Xiao, N.; Li, Y.; et al. A maize phytochrome-interacting factors protein ZmPIF1 enhances drought tolerance by inducing stomatal closure and improves grain yield in Oryza sativa. Plant Biotechnol. J. 2018, 16, 1375–1387. [Google Scholar] [CrossRef]
  41. Augustine, S.M.; Narayan, A.J.; Syamaladevi, D.P.; Appunu, C.; Chakravarthi, M.; Ravichandran, V.; Tuteja, N.; Subramonian, N. Overexpression of EaDREB2 and pyramiding of EaDREB2 with the pea DNA helicase gene (PDH45) enhance drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Cell Rep. 2015, 34, 247–263. [Google Scholar] [CrossRef]
  42. Xia, Z.; Xu, Z.; Wie, Y.; Wang, M. Overexpression of the maize sulfite oxidase increases sulfate and GSH levels and enhances drought tolerance in transgenic tobacco. Front. Plant Sci. 2018, 9, 298. [Google Scholar] [CrossRef] [PubMed]
  43. Zhu, M.; Chen, G.; Zhang, J.; Zhang, Y.; Xie, Q.; Zhao, Z.; Pan, Y.; Hu, Z. The abiotic stress-responsive NAC-type transcription factor SlNAC4 regulates salt and drought tolerance and stress-related genes in tomato (Solanum lycopersicum). Plant Cell Rep. 2014, 33, 1851–1863. [Google Scholar] [CrossRef] [PubMed]
  44. Xing, L.; Di, Z.; Yang, W.; Liu, J.; Li, M.; Wang, X.; Cui, C.; Wang, X.; Wang, X.; Zhang, R.; et al. Overexpression of ERF1-V from Haynaldia villosa can enhance the resistance of wheat to powdery mildew and increase the tolerance to salt and drought stresses. Front. Plant Sci. 2017, 8, 1948. [Google Scholar] [CrossRef] [PubMed]
  45. Del Río, L.A. ROS and RNS in plant physiology: An overview. J. Exp. Bot. 2015, 66, 2827–2837. [Google Scholar] [CrossRef]
  46. Choudhury, S.; Panda, P.; Sahoo, L.; Panda, S.K. Reactive oxygen species signaling in plants under abiotic stress. Plant Signal. Behav. 2013, 8, e23681. [Google Scholar] [CrossRef]
  47. Hossain, M.A.; Bhattacharjee, S.; Armin, S.M.; Qian, P.; Xin, W.; Li, H.Y.; Burritt, D.J.; Fujita, M.; Tran, L.S. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: Insights from ROS detoxification and scavenging. Front. Plant Sci. 2015, 6, 420. [Google Scholar] [CrossRef]
  48. Kleine, T.; Leister, D. Retrograde signaling: Organelles go networking. Biochim. Biophys. Acta 2016, 1857, 1313–1325. [Google Scholar] [CrossRef]
  49. Noctor, G.; Veljovic-Jovanovic, S.; Driscoll, S.; Novitskaya, L.; Foyer, C.H. Drought and oxidative load in the leaves of C3 plants: A predominant role for photorespiration? Ann. Bot. 2002, 89, 841–850. [Google Scholar] [CrossRef]
  50. Pastore, D.; Trono, D.; Laus, M.N.; Di Fonzo, N.; Passarella, S. Alternative oxidase in durum wheat mitochondria. Activation by pyruvate, hydroxypyruvate and glyoxylate and physiological role. Plant Cell Physiol. 2001, 42, 1373–1382. [Google Scholar] [CrossRef]
  51. Bartoli, C.G.; Gomez, F.; Gergoff, G.; Guiamét, J.J.; Puntarulo, S. Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J. Exp. Bot. 2005, 56, 1269–1276. [Google Scholar] [CrossRef]
  52. Selinski, J.; Scheibe, R.; Day, D.A.; Whelan, J. Alternative oxidase is positive for plant performance. Trends Plant Sci. 2018, 23, 588–597. [Google Scholar] [CrossRef] [PubMed]
  53. De Carvalho Cruz, M.H. Drought stress and reactive oxygen species: Production, scavenging and signaling. Plant Signal. Behav. 2008, 3, 156–165. [Google Scholar] [CrossRef]
  54. Barreto, P.; Yassitepe, J.E.; Wilson, Z.A.; Arruda, P. Mitochondrial uncoupling protein 1 overexpression increases yield in Nicotiana tabacum under drought stress by improving source and sink metabolism. Front. Plant Sci. 2017, 8, 1836. [Google Scholar] [CrossRef] [PubMed]
  55. Atkin, O.K.; Macherel, D. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 2009, 103, 581–597. [Google Scholar] [CrossRef]
  56. Gilroy, S.; Suzuki, N.; Miller, G.; Choi, W.G.; Toyota, M.; Devireddy, A.R.; Mittler, R. A tidal wave of signals: Calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci. 2014, 19, 623–630. [Google Scholar] [CrossRef]
  57. Evans, M.J.; Choi, W.G.; Gilroy, S.; Morris, R.J. A ROS-assisted calcium wave dependent on AtRBOHD and TPC1 propagates the systemic response to salt stress in Arabidopsis roots. Plant Physiol. 2016, 171, 1771–1784. [Google Scholar] [CrossRef]
  58. Sierla, M.; Waszczak, C.; Vahisalu, T.; Kangasjärvi, J. Reactive oxygen species in the regulation of stomatal movements. Plant Physiol. 2016, 171, 1569–1580. [Google Scholar] [CrossRef]
  59. Osakabe, Y.; Osakabe, K.; Shinozaki, K.; Tran, L.S.P. Response of plants to water stress. Front Plant Sci. 2014, 5, 86. [Google Scholar] [CrossRef] [PubMed]
  60. Avramova, V.; AbdElgawad, H.; Zhang, Z.; Fotschki, B.; Casadevall, R.; Vergauwen, L.; Knapen, D.; Taleisnik, E.; Guisez, Y.; Asard, H.; et al. Drought induces distinct growth response, protection and recovery mechanisms in the maize leaf growth zone. Plant Physiol. 2015, 169, 1382–1396. [Google Scholar] [CrossRef]
  61. Cai, W.; Liu, W.; Wang, W.S.; Fu, Z.W.; Han, T.T.; Lu, Y.T. Overexpression of rat neurons nitric oxide synthase in rice enhances drought and salt tolerance. PLoS ONE 2015, 10, e0131599. [Google Scholar] [CrossRef]
  62. Shehab, G.G.; Ahmed, O.K.; El-Beltagi, H.S. Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.). Notulae Botanicae Horti Agrobotanici Cluj-Napoca 2010, 38, 139–148. [Google Scholar]
  63. Filippou, P.; Bouchagier, P.; Skotti, E.; Fotopoulos, V. Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ. Exp. Bot. 2014, 97, 1–10. [Google Scholar] [CrossRef]
  64. Ben Rejeb, K.; Vos, L.D.; Le Disquet, I.; Leprince, A.S.; Bordenave, M.; Maldiney, R.; Jdey, A.; Abdelly, C.; Savouré, A. Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol. 2015, 208, 1138–1148. [Google Scholar] [CrossRef] [PubMed]
  65. Hasanuzzaman, M.; Nahar, K.; Hossain, M.S.; Anee, T.I.; Parvin, K.; Fujita, M. Nitric oxide pretreatment enhances antioxidant defense and glyoxalase systems to confer PEG-induced oxidative stress in rapeseed. J. Plant Interact. 2017, 12, 323–331. [Google Scholar] [CrossRef]
  66. Sarkar, J.; Ray, A.; Chakraborty, B.; Chakraborty, U. Antioxidative changes in Citrus reticulata L. induced by drought stress and its effect on root colonization by arbuscular mycorrhizal fungi. Eur. J. Biol. Res. 2016, 6, 1–13. [Google Scholar]
  67. Uzilday, B.; Turkan, I.; Sekmen, A.H.; Ozgur, R.; Karakaya, H.C. Comparison of ROS formation and antioxidant enzymes in Cleome gynandra (C4) and Cleome spinosa (C3) under drought stress. Plant Sci. 2012, 182, 59–70. [Google Scholar] [CrossRef] [PubMed]
  68. Batista, P.F.; Costa, A.C.; Müller, C.; de Oliveira Silva-Filho, R.; da Silva, F.B.; Merchant, A.; Mendes, G.C.; Nascimento, K.J.T. Nitric oxide mitigates the effect of water deficit in Crambe abyssinica. Plant Physiol. Biochem. 2018, 129, 310. [Google Scholar] [CrossRef] [PubMed]
  69. Gunes, A.; Pilbeam, D.J.; Inal, A.; Coban, S. Influence of silicon on sunflower cultivars under drought stress, I: Growth, antioxidant mechanisms, and lipid peroxidation. Commun. Soil Sci. Plant Anal. 2008, 39, 1885–1903. [Google Scholar] [CrossRef]
  70. Baloğlu, M.C.; Kavas, M.; AYDIN, G.; ÖKTEM, H.A.; Yücel, A.M. Antioxidative and physiological responses of two sunflower (Helianthus annuus) cultivars under PEG-mediated drought stress. Turk. J. Bot. 2012, 36, 707–714. [Google Scholar]
  71. Antoniou, C.; Chatzimichail, G.; Xenofontos, R.; Pavlou, J.J.; Panagiotou, E.; Christou, A.; Fotopoulos, V. Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. J. Pineal Res. 2017, 62, e12401. [Google Scholar] [CrossRef]
  72. Sharma, P.; Dubey, R.S. Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul. 2005, 46, 209–221. [Google Scholar] [CrossRef]
  73. Guo, Y.Y.; Tian, S.S.; Liu, S.S.; Wang, W.Q.; Sui, N. Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica 2018, 56, 861–872. [Google Scholar] [CrossRef]
  74. Hajihashemi, S.; Sofo, A. The effect of polyethylene glycol-induced drought stress on photosynthesis, carbohydrates and cell membrane in Stevia rebaudiana grown in greenhouse. Acta Physiol. Plant. 2018, 40, 142. [Google Scholar] [CrossRef]
  75. Gong, H.; Zhu, X.; Chen, K.; Wang, S.; Zhang, C. Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci. 2005, 169, 313–321. [Google Scholar] [CrossRef]
  76. Tian, X.; Lei, Y. Nitric oxide treatment alleviates drought stress in wheat seedlings. Biol. Plant. 2006, 50, 775–778. [Google Scholar] [CrossRef]
  77. Gong, H.J.; Chen, K.M.; Zhao, Z.G.; Chen, G.C.; Zhou, W.J. Effects of silicon on defense of wheat against oxidative stress under drought at different developmental stages. Biol. Plant. 2008, 52, 592–596. [Google Scholar] [CrossRef]
  78. Zhang, J.; Kirkham, M.B. Lipid peroxidation in sorghum and sunflower seedlings as affected by ascorbic acid, benzoic acid, and propyl gallate. J. Plant Physiol. 1996, 149, 489–493. [Google Scholar] [CrossRef]
  79. Freschi, L.; Rodrigues, M.A.; Domingues, D.S.; Purgatto, E.; Van Sluys, M.A.; Magalhaes, J.R.; Kaiser, W.M.; Mercier, H. Nitric oxide mediates the hormonal control of Crassulacean acid metabolism expression in young pineapple plants. Plant Physiol. 2010, 152, 1971–1985. [Google Scholar] [CrossRef] [PubMed]
  80. Shi, H.T.; Li, R.J.; Cai, W.; Liu, W.; Wang, C.L.; Lu, Y.T. Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance. Plant Cell Physiol. 2012, 53, 344–357. [Google Scholar] [CrossRef] [PubMed]
  81. Ziogas, V.; Tanou, G.; Filippou, P.; Diamantidis, G.; Vasilakakis, M.; Fotopoulos, V.; Molassiotis, A. Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol. Biochem. 2013, 68, 118–126. [Google Scholar] [CrossRef]
  82. Arasimowicz-Jelonek, M.; Floryszak-Wieczorek, J.; Kubiś, J. Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. Plant Growth Regul. 2009, 28, 177–186. [Google Scholar] [CrossRef]
  83. Montilla-Bascón, G.; Rubiales, D.; Hebelstrup, K.H.; Mandon, J.; Harren, F.J.M.; Cristescu, S.M.; Mur, L.A.J.; Prats, E. Reduced nitric oxide levels during drought stress promote drought tolerance in barley and is associated with elevated polyamine biosynthesis. Sci. Rep. 2017, 17, 13311. [Google Scholar] [CrossRef] [PubMed]
  84. Signorelli, S.; Corpas, F.J.; Borsani, O.; Barroso, J.B.; Monza, J. Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus. Plant Sci. 2013, 201, 137–146. [Google Scholar] [CrossRef] [PubMed]
  85. Filippou, P.; Antoniou, C.; Fotopoulos, V. Effect of drought and rewatering in the cellular status and antioxidant response of Medicago truncatula plants. Plant Signal. Behav. 2011, 6, 270–277. [Google Scholar] [CrossRef] [PubMed]
  86. Xiong, J.; Zhang, L.; Fu, G.; Yang, Y.; Zhu, C.; Tao, L. Drought-induced proline accumulation is uninvolved with increased nitric oxide, which alleviates drought stress by decreasing transpiration in rice. J. Plant Res. 2012, 125, 155–164. [Google Scholar] [CrossRef] [PubMed]
  87. Wu, H.; Zheng, Y.; Liu, J.; Zhang, H.; Chen, H. Heme oxygenase-1 delays gibberellin-induced programmed cell death of rice aleurone layers subjected to drought stress by interacting with nitric oxide. Front. Plant Sci. 2016, 6, 1267. [Google Scholar] [CrossRef]
  88. Fan, Q.J.; Liu, J.H. Nitric oxide is involved in dehydration/drought tolerance in Poncirus trifoliata seedlings through regulation of antioxidant systems and stomatal response. Plant Cell Rep. 2012, 31, 145–154. [Google Scholar] [CrossRef]
  89. Silveira, N.M.; Hancock, J.T.; Frungillo, L.; Siasou, E.; Marcos, F.C.; Salgado, I.; Machado, E.C.; Ribeiro, R.V. Evidence towards the involvement of nitric oxide in drought tolerance of sugarcane. Plant Physiol. Biochem. 2017, 115, 354–359. [Google Scholar] [CrossRef] [PubMed]
  90. Davies, M.J. Protein oxidation and peroxidation. Biochem. J. 2016, 473, 805–825. [Google Scholar] [CrossRef]
  91. Dietz, K.J. Peroxiredoxins in plants and cyanobacteria. Antioxid. Redox Signal. 2011, 15, 1129–1159. [Google Scholar] [CrossRef]
  92. Liebthal, M.; Maynard, D.; Dietz, K.J. Peroxiredoxins and Redox Signaling in Plants. Antioxid. Redox Signal. 2018, 28, 609–624. [Google Scholar] [CrossRef] [PubMed]
  93. Waszczak, C.; Akter, S.; Jacques, S.; Huang, J.; Messens, J.; Van Breusegem, F. Oxidative post-translational modifications of cysteine residues in plant signal transduction. J. Exp. Bot. 2015, 66, 2923–2934. [Google Scholar] [CrossRef] [PubMed]
  94. Jeandroz, S.; Wipf, D.; Stuehr, D.J.; Lamattina, L.; Melkonian, M.; Tian, Z.; Zhu, Y.; Carpenter, E.J.; Wong, G.K.; Wendehenne, D. Occurrence, structure, and evolution of nitric oxide synthase—Like proteins in the plant kingdom. Sci. Signal. 2016, 9, re2. [Google Scholar] [CrossRef]
  95. Corpas, F.J.; Chaki, M.; Fernandez-Ocana, A.; Valderrama, R.; Palma, J.M.; Carreras, A.; Begara-Morales, J.C.; Airaki, M.; del Río, L.A.; Barroso, J.B. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 2008, 49, 1711–1722. [Google Scholar] [CrossRef]
  96. Corpas, F.J.; Palma, J.M.; Del Río, L.A.; Barroso, J.B. Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol. 2009, 184, 9–14. [Google Scholar] [CrossRef]
  97. Gupta, K.J.; Fernie, A.R.; Kaiser, W.M.; van Dongen, J.T. On the origins of nitric oxide. Trends Plant Sci. 2011, 16, 160–168. [Google Scholar] [CrossRef] [PubMed]
  98. Díaz, M.; Achkor, H.; Titarenko, E.; Martínez, M.C. The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Lett. 2003, 543, 136–139. [Google Scholar] [CrossRef]
  99. Igamberdiev, A.U.; Bykova, N.V.; Shah, J.K.; Hill, R.D. Anoxic nitric oxide cycling in plants: Participating reactions and possible mechanisms. Physiol. Plant. 2010, 138, 393–404. [Google Scholar] [CrossRef] [PubMed]
  100. Chamizo-Ampudia, A.; Sanz-Luque, E.; Llamas, A.; Galvan, A.; Fernandez, E. Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci. 2017, 22, 163–174. [Google Scholar] [CrossRef]
  101. Tholakalabavi, A.; Zwiazek, J.J.; Thorpe, T.A. Effect of mannitol and glucose-induced osmotic stress on growth, water relations, and solute composition of cell suspension cultures of poplar (Populus deltoides var. Occidentalis) in relation to anthocyanin accumulation. In Vitro Cell. Dev. Biol. Plant 1994, 30, 164–170. [Google Scholar] [CrossRef]
  102. Moustaka, J.; Tanou, G.; Adamakis, I.D.; Eleftheriou, E.P.; Moustakas, M. Leaf age-dependent photoprotective and antioxidative response mechanisms to paraquat-induced oxidative stress in Arabidopsis thaliana. Int. J. Mol. Sci. 2015, 16, 13989–14006. [Google Scholar] [CrossRef]
  103. Polle, A.; Schwanz, P.; Rudolf, C. Developmental and seasonal changes of stress responsiveness in beech leaves (Fagus sylvatica L.). Plant Cell Environ. 2001, 24, 821–829. [Google Scholar] [CrossRef]
  104. Li, N.N.; Yue, C.; Cao, H.L.; Qian, W.J.; Hao, X.Y.; Wang, Y.C.; Wang, L.; Ding, C.Q.; Wang, X.C.; Yang, Y.J. Transcriptome sequencing dissection of the mechanisms underlying differential cold sensitivity in young and mature leaves of the tea plant (Camellia sinensis). J. Plant Physiol. 2018, 224–225, 144–155. [Google Scholar] [CrossRef]
  105. Mohammadkhani, N.; Heidari, R. Water stress induced by polyethylene glycol 6000 and sodium chloride in two maize cultivars. Pak. J. Biol. Sci. 2008, 11, 92–97. [Google Scholar] [CrossRef] [PubMed]
  106. Csonka, C.; Páli, T.; Bencsik, P.; Görbe, A.; Ferdinandy, P.; Csont, T. Measurement of NO in biological samples. Brit. J. Pharmacol. 2015, 172, 1620–1632. [Google Scholar] [CrossRef] [PubMed]
  107. Wu, C.; Wang, Q.; Xie, B.; Wang, Z.; Cui, J.; Hu, T. Effects of drought and salt stress on seed germination of three leguminous species. Afr. J. Biotechnol. 2011, 10, 17954–17961. [Google Scholar]
  108. Begara-Morales, J.C.; Sánchez-Calvo, B.; Chaki, M.; Valderrama, R.; Mata-Pérez, C.; Padilla, M.N.; Corpas, F.J.; Barroso, J.B. Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front. Plant Sci. 2016, 7, 152. [Google Scholar] [CrossRef]
  109. Mata-Pérez, C.; Begara-Morales, J.C.; Chaki, M.; Sánchez-Calvo, B.; Valderrama, R.; Padilla, M.N.; Corpas, F.J.; Barroso, J.B. Protein tyrosine nitration during development and abiotic stress response in plants. Front. Plant Sci. 2016, 7, 1699. [Google Scholar] [CrossRef] [PubMed]
  110. Bian, S.; Jiang, Y. Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci. Hortic. 2009, 120, 264–270. [Google Scholar] [CrossRef]
  111. Leshem, Y.Y.; Kuiper, P.J.C. Is there a GAS (general adaptation syndrome) response to various types of environmental stress? Biol. Plant. 1996, 38, 1. [Google Scholar] [CrossRef]
  112. Correa-Aragunde, N.; Graziano, M.; Lamattina, L. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 2004, 218, 900–905. [Google Scholar] [CrossRef]
  113. Kolbert, Z.; Bartha, B.; Erdei, L. Generation of nitric oxide in roots of Pisum sativum, Triticum aestivum and Petroselinum crispum plants under osmotic and drought stress. Acta Biol. 2005, 49, 13–16. [Google Scholar]
  114. McInnis, S.M.; Desikan, R.; Hancock, J.T.; Hiscock, S.J. Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: Potential signalling crosstalk? New Phytol. 2006, 172, 221–228. [Google Scholar] [CrossRef] [PubMed]
  115. Molassiotis, A.; Fotopoulos, V. Oxidative and nitrosative signaling in plants: Two branches in the same tree? Plant Signal. Behav. 2001, 6, 210–214. [Google Scholar] [CrossRef]
  116. Iyer, N.J.; Tang, Y.; Mahalingam, R. Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant Cell Environ. 2013, 36, 706–720. [Google Scholar] [CrossRef] [PubMed]
  117. Zandalinas, S.I.; Mittler, R.; Balfagón, D.; Arbona, V.; Gómez-Cadenas, A. Plant adaptations to the combination of drought and high temperatures. Physiol. Plant. 2018, 162, 2–12. [Google Scholar] [CrossRef] [PubMed]
  118. Ahlfors, R.; Brosché, M.; Kollist, H.; Kangasjärvi, J. Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J. 2009, 58, 1–12. [Google Scholar] [CrossRef]
  119. Zandalinas, S.I.; Balfagón, D.; Arbona, V.; Gómez-Cadenas, A.; Inupakutika, M.A.; Mittler, R. ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J. Exp. Bot. 2016, 67, 5381–5390. [Google Scholar] [CrossRef]
  120. Zhao, F.; Zhang, D.; Zhao, Y.; Wang, W.; Yang, H.; Tai, F.; Li, C.; Hu, X. The difference of physiological and proteomic changes in maize leaves adaptation to drought, heat, and combined both stresses. Front. Plant Sci. 2016, 7, 1471. [Google Scholar] [CrossRef] [PubMed]
  121. Sekmen, A.H.; Ozgur, R.; Uzilday, B.; Turkan, I. Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environ. Exp. Bot. 2014, 99, 141–149. [Google Scholar] [CrossRef]
  122. Jin, R.; Wang, Y.; Liu, R.; Gou, J.; Chan, Z. Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Front. Plant Sci. 2016, 6, 1123. [Google Scholar] [CrossRef] [PubMed]
  123. Carvalho, L.C.; Coito, J.L.; Goncalves, E.F.; Chaves, M.M.; Amancio, S. Differential physiological response of the grapevine varieties Touriga Nacional and Trincadeira to combined heat, drought and light stresses. Plant Biol. 2016, 18, 101–111. [Google Scholar] [CrossRef]
  124. Brouder, S.M.; Volenec, J.J. Impact of climate change on crop nutrient and water use efficiencies. Physiol. Plant. 2008, 133, 705–724. [Google Scholar] [CrossRef] [PubMed]
  125. Giraud, E.; Ho, L.H.; Clifton, R.; Carroll, A.; Estavillo, G.; Tan, Y.F.; Howell, K.A.; Ivanova, A.; Pogson, B.J.; Millar, A.H.; et al. The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 2008, 147, 595–610. [Google Scholar] [CrossRef]
  126. Choudhury, F.K.; Rivero, R.M.; Blumwald, E.; Mittler, R. Reactive oxygen species, abiotic stress and stress combination. Plant J. 2017, 90, 856–867. [Google Scholar] [CrossRef] [PubMed]
  127. Correia, B.; Hancock, R.D.; Amaral, J.; Gomez-Cadenas, A.; Valledor, L.; Pinto, G. Combined drought and heat activates protective responses in Eucalyptus globulus that are not activated when subjected to drought or heat stress alone. Front. Plant Sci. 2018, 9, 819. [Google Scholar] [CrossRef]
  128. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef] [PubMed]
  129. Mittler, R.; Vanderauwera, S.; Suzuki, N.; Miller, G.; Tognetti, V.B.; Vandepoele, K.; Gollery, M.; Shulaev, V.; Van Breusegem, F. ROS signaling: The new wave? Trends Plant Sci. 2011, 16, 300–309. [Google Scholar] [CrossRef] [PubMed]
  130. Tognetti, V.B.; Mühlenbock, P.; Van Breusegem, F. Stress homeostasis—The redox and auxin perspective. Plant Cell Environ. 2012, 35, 321–333. [Google Scholar] [CrossRef]
  131. Hussain, T.; Tan, B.; Yin, Y.; Blachier, F.; Tossou, M.C.; Rahu, N. Oxidative stress and inflammation: What polyphenols can do for us? Oxid. Med. Cell Longev. 2016, 2016, 7432797. [Google Scholar] [CrossRef]
  132. Chibani, K.; Wingsle, G.; Jacquot, J.P.; Gelhaye, E.; Rouhier, N. Comparative genomic study of the thioredoxin family in photosynthetic organisms with emphasis on Populus trichocarpa. Mol. Plant 2009, 2, 308–322. [Google Scholar] [CrossRef]
  133. Sevilla, F.; Camejo, D.; Ortiz-Espín, A.; Calderón, A.; Lázaro, J.J.; Jiménez, A. The thioredoxin/peroxiredoxin/sulfiredoxin system: Current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J. Exp. Bot. 2015, 66, 2945–2955. [Google Scholar] [CrossRef]
  134. Vaseghi, M.J.; Chibani, K.; Telman, W.; Liebthal, M.F.; Gerken, M.; Mueller, S.M.; Dietz, K.J. The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism. BioRxiv 2018. [Google Scholar] [CrossRef] [PubMed]
  135. Mittler, R.; Zilinskas, B.A. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J. 1994, 5, 397–405. [Google Scholar] [CrossRef]
  136. Wilson, P.B.; Estavillo, G.M.; Field, K.J.; Pornsiriwong, W.; Carroll, A.J.; Howell, K.A.; Woo, N.S.; Lake, J.A.; Smith, S.M.; Millar, H.A.; et al. The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J. 2009, 58, 299–317. [Google Scholar] [CrossRef] [PubMed]
  137. Estavillo, G.M.; Crisp, P.A.; Pornsiriwong, W.; Wirtz, M.; Collinge, D.; Carrie, C.; Giraud, E.; Whelan, J.; David, P.; Javot, H.; et al. Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 2011, 23, 3992–4012. [Google Scholar] [CrossRef] [PubMed]
  138. Li, Y.J.; Hai, R.L.; Du, X.H.; Jiang, X.N.; Lu, H. Over-expression of a Populus peroxisomal ascorbate peroxidase (PpAPX) gene in tobacco plants enhances stress tolerance. Plant Breed 2009, 128, 404–410. [Google Scholar] [CrossRef]
  139. Cao, S.; Du, X.H.; Li, L.H.; Liu, Y.D.; Zhang, L.; Pan, X.; Li, Y.; Li, H.; Lu, H. Overexpression of Populus tomentosa cytosolic ascorbate peroxidase enhances abiotic stress tolerance in tobacco plants. Russ. J. Plant Physiol. 2017, 64, 224–234. [Google Scholar] [CrossRef]
  140. Sofo, A.; Scopa, A.; Nuzzaci, M.; Vitti, A. Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int. J. Mol. Sci. 2015, 16, 13561–13578. [Google Scholar] [CrossRef]
  141. Luna, C.M.; Pastori, G.M.; Driscoll, S.; Groten, K.; Bernard, S.; Foyer, C.H. Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. J. Exp. Bot. 2005, 56, 417–423. [Google Scholar] [CrossRef]
  142. Rubio, M.C.; González, E.M.; Minchin, F.R.; Webb, K.J.; Arrese-Igor, C.; Ramos, J.; Becana, M. Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol. Plant. 2002, 115, 531–540. [Google Scholar] [CrossRef] [PubMed]
  143. Koussevitzky, S.; Suzuki, N.; Huntington, S.; Armijo, L.; Sha, W.; Cortes, D.; Shulaev, V.; Mittler, R. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem. 2008, 283, 34197–34203. [Google Scholar] [CrossRef]
  144. Cha, J.Y.; Kim, J.Y.; Jung, I.J.; Kim, M.R.; Melencion, A.; Alam, S.S.; Yun, D.J.; Lee, S.Y.; Kim, M.G.; Kim, W.Y. NADPH-dependent thioredoxin reductase A (NTRA) confers elevated tolerance to oxidative stress and drought. Plant Physiol. Biochem. 2014, 80, 184–191. [Google Scholar] [CrossRef] [PubMed]
  145. Turkan, I.; Bor, M.; Ozdemir, F.; Koca, H. Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris subjected to polyethylene glycol mediated water stress. Plant Sci. 2005, 168, 223–231. [Google Scholar] [CrossRef]
  146. Balfagón, D.; Zandalinas, S.I.; Baliño, P.; Muriach, M.; Gómez-Cadenas, A. Involvement of ascorbate peroxidase and heat shock proteins on citrus tolerance to combined conditions of drought and high temperatures. Plant Physiol. Biochem. 2018, 127, 194–199. [Google Scholar] [CrossRef] [PubMed]
  147. Zandalinas, S.I.; Balfagón, D.; Arbona, V.; Gómez-Cadenas, A. Modulation of antioxidant defense system is associated with combined drought and heat stress tolerance in Citrus. Front. Plant Sci. 2017, 8, 953. [Google Scholar] [CrossRef] [PubMed]
  148. Lima, A.L.S.; DaMatta, F.M.; Pinheiro, H.A.; Totola, M.R.; Loureiro, M.E. Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit conditions. Environ. Exp. Bot. 2002, 47, 239–247. [Google Scholar] [CrossRef]
  149. Ratnayaka, H.H.; Molin, W.T.; Sterling, T.M. Physiological and antioxidant responses of cotton and spurred anoda under interference and mild drought. J. Exp. Bot. 2003, 54, 2293–2305. [Google Scholar] [CrossRef]
  150. Zhang, H.; Ni, Z.; Chen, Q.; Guo, Z.; Gao, W.; Su, X.; Qu, Y. Proteomic responses of drought-tolerant and drought-sensitive cotton varieties to drought stress. Mol. Genet. Genom. 2016, 291, 1293–1303. [Google Scholar] [CrossRef]
  151. Safronov, O.; Kreuzwieser, J.; Haberer, G.; Alyousif, M.S.; Schulze, W.; Al-Harbi, N.; Arab, L.; Ache, P.; Stempfl, T.; Kruse, J.; et al. Detecting early signs of heat and drought stress in Phoenix dactylifera (date palm). PLoS ONE 2017, 12, e0177883. [Google Scholar] [CrossRef]
  152. Jiang, M.; Zhang, J. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 2002, 53, 2401–2410. [Google Scholar] [CrossRef] [PubMed]
  153. Lei, Y.; Yin, C.; Li, C. Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii. Physiol. Plant. 2006, 127, 182–191. [Google Scholar] [CrossRef]
  154. Guo, Z.; Ou, W.; Lu, S.; Zhong, Q. Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol. Biochem. 2006, 44, 828–836. [Google Scholar] [CrossRef] [PubMed]
  155. Badawi, G.H.; Kawano, N.; Yamauchi, Y.; Shimada, E.; Sasaki, R.; Kubo, A.; Tanaka, K. Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol. Plant. 2004, 121, 231–238. [Google Scholar] [CrossRef] [PubMed]
  156. Rizhsky, L.; Liang, H.; Mittler, R. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 2002, 130, 1143–1151. [Google Scholar] [CrossRef] [PubMed]
  157. Shan, C.; Zhang, S.; Ou, X. The roles of H2S and H2O2 in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress. Protoplasma 2018, 255, 1257–1262. [Google Scholar] [CrossRef]
  158. Jung, S. Variation in antioxidant metabolism of young and mature leaves of Arabidopsis thaliana subjected to drought. Plant Sci. 2004, 166, 459–466. [Google Scholar] [CrossRef]
  159. Cheng, L.; Wang, Y.; He, Q.; Li, H.; Zhang, X.; Zhang, F. Comparative proteomics illustrates the complexity of drought resistance mechanisms in two wheat (Triticum aestivum L.) cultivars under dehydration and rehydration. BMC Plant Biol. 2016, 16, 188. [Google Scholar] [CrossRef] [PubMed]
  160. Fu, J.; Huang, B. Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ. Exp. Bot. 2001, 45, 105–114. [Google Scholar] [CrossRef]
  161. Hajheidari, M.; Eivazi, A.; Buchanan, B.B.; Wong, J.H.; Majidi, I.; Salekdeh, G.H. Proteomics uncovers a role for redox in drought tolerance in wheat. J. Prot. Res. 2007, 6, 1451–1460. [Google Scholar] [CrossRef]
  162. Broin, M.; Cuiné, S.; Peltier, G.; Rey, P. Involvement of CDSP 32, a drought-induced thioredoxin, in the response to oxidative stress in potato plants. FEBS Lett. 2000, 467, 245–248. [Google Scholar] [CrossRef]
  163. Dhindsa, R.S. Drought stress, enzymes of glutathione metabolism, oxidation injury, and protein synthesis in Tortula ruralis. Plant Physiol. 1991, 95, 648–651. [Google Scholar] [CrossRef] [PubMed]
  164. Loggini, B.; Scartazza, A.; Brugnoli, E.; Navari-Izzo, F. Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol. 1999, 119, 1091–1099. [Google Scholar] [CrossRef] [PubMed]
  165. Contour-Ansel, D.; Torres-Franklin, M.L.; Cruz, D.E.; Carvalho, M.H.; D’Arcy-Lameta, A.; Zuily-Fodil, Y. Glutathione reductase in leaves of cowpea: Cloning of two cDNAs, expression and enzymatic activity under progressive drought stress, desiccation and abscisic acid treatment. Ann. Bot. 2006, 98, 1279–1287. [Google Scholar] [CrossRef] [PubMed]
  166. Zhu, C.; Luo, N.; He, M.; Chen, G.; Zhu, J.; Yin, G.; Li, X.; Hu, Y.; Li, J.; Yan, Y. Molecular characterization and expression profiling of the protein disulfide isomerase gene family in Brachypodium distachyon L. PLoS ONE 2014, 18, e94704. [Google Scholar] [CrossRef]
  167. Lou, L.; Li, X.; Chen, J.; Li, Y.; Tang, Y.; Lv, J. Photosynthetic and ascorbate-glutathione metabolism in the flag leaves as compared to spikes under drought stress of winter wheat (Triticum aestivum L.). PLoS ONE 2018, 13, e0194625. [Google Scholar] [CrossRef] [PubMed]
  168. Wu, J.; Zhang, J.; Li, X.; Xu, J.J.; Wang, L. Identification and characterization of a PutCu/Zn-SOD gene from Puccinellia tenuiflora (Turcz.) Scribn. et Merr. Plant Growth Regul. 2016, 79, 55–64. [Google Scholar] [CrossRef]
  169. Kosová, K.; Vítámvás, P.; Urban, M.O.; Prášil, I.T.; Renaut, J. Plant abiotic stress proteomics: The major factors determining alterations in cellular proteome. Front. Plant Sci. 2018, 9, 122. [Google Scholar] [CrossRef] [PubMed]
  170. Meyer, Y.; Reichheld, J.P.; Vignols, F. Thioredoxins in Arabidopsis and other plants. Photosynth. Res. 2005, 86, 419–433. [Google Scholar] [CrossRef]
  171. Chibani, K.; Couturier, J.; Selles, B.; Jacquot, J.P.; Rouhier, N. The chloroplastic thiol reducing systems: Dual functions in the regulation of carbohydrate metabolism and regeneration of antioxidant enzymes, emphasis on the poplar redoxin equipment. Photosynth. Res. 2010, 104, 75–99. [Google Scholar] [CrossRef]
  172. Davletova, S.; Rizhsky, L.; Liang, H.; Shengqiang, Z.; Oliver, D.J.; Coutu, J.; Shulaev, V.; Schlauch, K.; Mittler, R. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 2005, 17, 268–281. [Google Scholar] [CrossRef]
  173. Dietz, K.J.; Jacob, S.; Oelze, M.L.; Laxa, M.; Tognetti, V.; de Miranda, S.M.; Baier, M.; Finkemeier, I. The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 2006, 57, 1697–1709. [Google Scholar] [CrossRef] [PubMed]
  174. Ghasempour, H.R.; Gaff, D.F.; Williams, R.P.W.; Gianello, R.D. Content of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regul. 1998, 24, 185–191. [Google Scholar] [CrossRef]
  175. Almeida, A.M.; Cardoso, L.A.; Santos, D.M.; Torne, J.M.; Fevereiro, P.S. Trehalose and its applications in plant biotechnology. In Vitro Cell. Dev. Biol.-Plant 2007, 43, 167–177. [Google Scholar] [CrossRef]
  176. Bianchi, G.; Gamba, A.; Murelli, C.; Salamini, F.; Bartels, D. Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. Plant J. 1991, 1, 355–359. [Google Scholar] [CrossRef] [PubMed]
  177. Djilianov, D.; Ivanov, S.; Moyankova, D.; Miteva, L.; Kirova, E.; Alexieva, V.; Joudi, M.; Peshev, D.; Van den Ende, W. Sugar ratios, glutathione redox status and phenols in the resurrection species Haberlea rhodopensis and the closely related non-resurrection species Chirita eberhardtii. Plant Biol. 2011, 13, 767–776. [Google Scholar] [CrossRef]
  178. Toldi, O.; Tuba, Z.; Scott, P. Vegetative desiccation tolerance: Is it a goldmine for bioengineering crops? Plant Sci. 2009, 176, 187–199. [Google Scholar] [CrossRef]
  179. Kranner, I.; Beckett, R.P.; Wornik, S.; Zorn, M.; Pfeifhofer, H.W. Revival of a resurrection plant correlates with its antioxidant status. Plant J. 2002, 31, 13–24. [Google Scholar] [CrossRef] [PubMed]
  180. Wang, X.; Chen, S.; Zhang, H.; Shi, L.; Cao, F.; Guo, L.; Xie, Y.; Wang, T.; Yan, X.; Dai, S. Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J. Proteome Res. 2010, 9, 6561–6577. [Google Scholar] [CrossRef] [PubMed]
  181. Gechev, T.S.; Benina, M.; Obata, T.; Tohge, T.; Sujeeth, N.; Minkov, I.; Hille, J.; Temanni, M.R.; Marriott, A.S.; Bergström, E.; et al. Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cell Mol. Life Sci. 2013, 70, 689–709. [Google Scholar] [CrossRef]
  182. Benešová, M.; Holá, D.; Fischer, L.; Jedelský, P.L.; Hnilička, F.; Wilhelmová, N.; Rothová, O.; Kočová, M.; Procházková, D.; Honnerová, J.; et al. The physiology and proteomics of drought tolerance in maize: Early stomatal closure as a cause of lower tolerance to short-term dehydration? PLoS ONE 2012, 7, e38017. [Google Scholar] [CrossRef] [PubMed]
  183. Hartung, W.; Schiller, P.; Dietz, K.J. The physiology of poikilohydric plants. Prog. Bot. 1997, 59, 299–327. [Google Scholar]
  184. Rascio, N.; La Rocca, N. Resurrection plants: The puzzle of surviving extreme vegetative desiccation. CRC Crit. Rev. Plant Sci. 2005, 24, 209–225. [Google Scholar] [CrossRef]
  185. Hellwege, E.M.; Dietz, K.J.; Volk, O.H.; Hartung, W. Abscisic acid and the induction of desiccation tolerance in the extremely xerophilic liverwort Exormotheca holstii. Planta 1994, 194, 525–531. [Google Scholar] [CrossRef]
  186. La, V.H.; Lee, B.R.; Islam, M.T.; Park, S.H.; Jung, H.I.; Bae, D.W.; Kim, T.H. Characterization of salicylic acid-mediated modulation of the drought stress responses: Reactive oxygen species, proline, and redox state in Brassica napus. Environ. Exp. Bot. 2019, 157, 1–10. [Google Scholar] [CrossRef]
  187. Chaves, M.M.; Maroco, J.P.; Pereira, J.S. Understanding plant responses to drought—From genes to the whole plant. Funct. Plant Biol. 2003, 30, 239–264. [Google Scholar] [CrossRef]
  188. Meyer, A.J.; Brach, T.; Marty, L.; Kreye, S.; Rouhier, N.; Jacquot, J.P.; Hell, R. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J. 2007, 52, 973–986. [Google Scholar] [CrossRef] [PubMed]
  189. Belousov, V.V.; Fradkov, A.F.; Lukyanov, K.A.; Staroverov, D.B.; Shakhbazov, K.S.; Terskikh, A.V.; Lukyanov, S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 2006, 3, 281–286. [Google Scholar] [CrossRef] [PubMed]
  190. Mock, H.P.; Dietz, K.J. Redox proteomics for the assessment of redox-related posttranslational regulation in plants. Biochim. Biophys. Acta 2016, 1864, 967–973. [Google Scholar] [CrossRef]
Figure 1. Physiological and biochemical processes triggered by drought.
Figure 1. Physiological and biochemical processes triggered by drought.
Antioxidants 08 00094 g001
Figure 2. Characteristic features of drought-sensitive, drought-tolerant and desiccation-tolerant plants. The figure summarizes properties related to metabolism, antioxidant defense, and recovery which often are associated with the physiological traits. Red arrow: reactive oxygen species (ROS)/reactive nitrogen species (RNS) gain prevalence; green arrow: status is preserved following drought. Fond size correlates with the strength of stress responses measured. ROS, reactive oxygen species; RNS, reactive nitrogen species; HSP, heat shock protein; LEA, late embryogenesis abundant protein; ELIP, early light-inducible protein; Suc/Fru, sucrose to fructose ratio; CAT, catalase; APX, ascorbate peroxidase; SOD, superoxide dismutase; ASC, ascorbate; GSH, glutathione.
Figure 2. Characteristic features of drought-sensitive, drought-tolerant and desiccation-tolerant plants. The figure summarizes properties related to metabolism, antioxidant defense, and recovery which often are associated with the physiological traits. Red arrow: reactive oxygen species (ROS)/reactive nitrogen species (RNS) gain prevalence; green arrow: status is preserved following drought. Fond size correlates with the strength of stress responses measured. ROS, reactive oxygen species; RNS, reactive nitrogen species; HSP, heat shock protein; LEA, late embryogenesis abundant protein; ELIP, early light-inducible protein; Suc/Fru, sucrose to fructose ratio; CAT, catalase; APX, ascorbate peroxidase; SOD, superoxide dismutase; ASC, ascorbate; GSH, glutathione.
Antioxidants 08 00094 g002
Figure 3. Changes in the activation of the antioxidative system in sensitive and tolerant species. Orange, downregulation, blue, upregulation, grey, no significant changes, no color, no data. APX, ascorbate peroxidase; CAT, catalase; DHAR, dehydroascorbate reductase; Fd, ferredoxin; GPX, glutathione peroxidase; GR, glutathione reductase; MDHAR, monodehydroascorbate reductase; PRX, peroxiredoxin; SOD, superoxide dismutase; TRX, thioredoxin.
Figure 3. Changes in the activation of the antioxidative system in sensitive and tolerant species. Orange, downregulation, blue, upregulation, grey, no significant changes, no color, no data. APX, ascorbate peroxidase; CAT, catalase; DHAR, dehydroascorbate reductase; Fd, ferredoxin; GPX, glutathione peroxidase; GR, glutathione reductase; MDHAR, monodehydroascorbate reductase; PRX, peroxiredoxin; SOD, superoxide dismutase; TRX, thioredoxin.
Antioxidants 08 00094 g003
Table 1. Classification of drought stress by different units that describe the water availability for different species at the various stages of drought stress.
Table 1. Classification of drought stress by different units that describe the water availability for different species at the various stages of drought stress.
Plant SpeciesUnitControlMildModerateSevereVery SevereLength of Stress Application Reference
Camellia sinensis (Tea)Soil moisture content [%]19.515.210.175.54 week(s)[21]
Arabidopsis thalianaWater content [g water/g dry soil]2.21.2 0.7 weeks[22]
Arabidopsis thalianaRelative soil water content [%]85–90 45–5030–35 week(s)[23]
Biserrula pelecinusWater holding capacity70–9040–60 20–40 month[24]
Common beanSoil field capacity [%]9070 5030weeks[17]
Jujube treeRelative soil moisture [%]80706040 [25]
Lemon balm and thymeRelative soil water content [%]70 4025 months[26]
Malus hupehensisSoil field capacity [%]75–85 45–55 months[27]
PoplarRelative soil water content [%]7045 20 month[28]
Soybeangs intervals [mol H2O m−2s−1]>0.20.1–0.2 <0.1 week[29]
TomatoSoil field capacity [%]100 50 weeks[30]
Valeriana officinalesAvailable water content/relative water content (%)100/77.370/67.2 65.1/5051.4/30months[31]
WheatRelative soil water content [%]80–9035–43 20–25 week[32]
WheatRelative water content [%]80–10060–80 40–60 weeks[33]
WheatSoil field capacity [%]85 55 months[34]
Populus deltoidesWater potential [MPa]−0.1−0.5 −1.26 week[35]
Wheat and maize Water potential [MPa] in the presence of PEG6000 −0.4−0.8−1.5 week[36]
g: gram(s).
Table 2. Exemplary experimental design for testing drought tolerance in different plant species.
Table 2. Exemplary experimental design for testing drought tolerance in different plant species.
Plant SpeciesDrought Stress (Age of Plants, Duration, Re-Watering)MediumReference
Arabidopsis thaliana2-weeks-old, 13 d no water, re-hydration for 2 dsoil[37]
Arabidopsis thaliana2-weeks-old, 5 d no waterMS medium[38]
Arabidopsis thaliana2-weeks-old, 12 d no water, re-hydration for 4 dayssoil[39]
Rice2-weeks-old, 4 d 20% PEG-6000, 1–10 d re-wateringhydroponics[40]
Rice40-days-old, 7 d no water, 1–10 d re-wateringsoil[40]
Sugarcane120-days-old, 10 d no water, re-wateringsoil[41]
Tobacco14 d without water, 3 d re-wateringsoil[42]
Tomato8-weeks old, up to 21 d no watersoil[43]
Wheat3-leaves stage, 72 h 20% PEG-6000 in 1/2 Hoagland solution (HS), 1 d re-watering with 1/2 HShydroponics[44]
d, day(s); h, hour(s); MS medium, Murashige–Skoog medium; PEG, polyethylene glycol.
Table 3. Changes in reactive oxygen species (ROS) and nitric oxide (NO) amounts upon drought or osmotic stress treatment in various plant species. Data originate from green leaf tissue if not indicated otherwise. Increase in percent was chosen due to different detection methods with different units. Effects were estimated from graphs, figures and tables if not directly given in the text or supplements.
Table 3. Changes in reactive oxygen species (ROS) and nitric oxide (NO) amounts upon drought or osmotic stress treatment in various plant species. Data originate from green leaf tissue if not indicated otherwise. Increase in percent was chosen due to different detection methods with different units. Effects were estimated from graphs, figures and tables if not directly given in the text or supplements.
ROS/RNS SpeciesPlant SpeciesStress ApplicationObserved Change in ROS/RNS Concentration (% Relative to Control)Reference
H2O2Ailanthus altissimaNo water for 14 d+166[63]
Arabidopsis thaliana200 mmol/L mannitol for 6 h+50[64]
Brassica rapus10% PEG for 2 d
20% PEG for 2 d
Citrus reticulataNo water for 3 d
No water for 6 d
No water for 9 d
Cleome spinosaNo water for 10 d+25[67]
Crambe abyssinica50% MWHC for 32 h
50% MWHC for 136 h
Helianthus annuus cultivars40% SFC for 21 dVariable, see literature[69]
Helianthus annuus Aydin

Helianthus annuus Musala
10% PEG for 5 d
20% PEG for 5 d
10% PEG for 5 d
20% PEG for 5 d
Medicago sativaNo water for 7 d+490[71]
Oryza sativa200 mmol/L mannitol for 2 d+200[61]
Oryza sativa callus5% PEG for 28 d
10% PEG for 28 d
15% PEG for 28 d
20% PEG for 28 d
Oryza sativa
roots and leaves
−0.5 MPa for 1 d
−2.0 MPa for 1 d
Age dependent, see literature[72]
Sorghumbicolor M-81E
Sorghum bicolor Roma
No water for 7 d
No water for 7 d
Stevia rebaudiana15% PEG for 30 d+220[74]
Triticum aestivum50% RWC for 12 d+40[75]
Triticum aestivum seedlings15% PEG for 2 d
15% PEG for 4 d
15% PEG for 6 d
Triticum aestivum (booting)
Triticum aestivum (filling)
No water for 52 d
No water for 69 d
Zea mays growth zones20 % less SWC till 3 d after 5th leafDoubled across all zones[60]
O2Crambe abyssinica50% MWHC for 32 h+18[68]
Helianthus annuus10 % PEG for 1 d−60[78]
Oryza sativa
roots and leaves
−0.5 MPa for 1 d
−2.0 MPa for 1 d
Age dependent, see literature[72]
Sorghum bicolor10% PEG for 1 d−22.5[78]
NOAilanthus altissimaNo water for 14 d+125[63]
Ananas comosus30% PEG for 25 dVariable emission, see literature[79]
Arabidopsis thalianaNo water for 4 d+150 [80]
Citrus aurantium13% PEG for 12 d+150[81]
Cucumis sativusRoot aeration for 5, 10, 15 h plus rewateringVariable, see literature[82]
Hordeum vulgareNo water for 18 dDoubled production rate[83]
Lotus japonicus
roots and leaves
No water for 5 d+80
Medicago truncatula
roots and leaves
No water for 3, 9, 11 d plus rewateringVariable, see literature[85]
Oryza sativa200 mmol/L mannitol for 1, 6, 24 hVariable, see literature[61]
Oryza sativaNo water for 9 d+200[86]
Oryza sativa seeds20% PEG for 1d−75[87]
Poncirus trifoliateNo water 6 h+200[88]
Saccharum spp.
roots and leaves
−0.4 MPa (PEG) for 1 dVariable, see literature[89]
MWHC, maximum water holding capacity; RWC, relative water content; SWC, soil water content; SFC, soil field capacity; d, day(s); h, hour(s.).
Table 4. Antioxidant enzymes regulated in plants under drought.
Table 4. Antioxidant enzymes regulated in plants under drought.
Antioxidative EnzymePlant SpeciesTranscriptional RegulationPost-Transcriptional RegulationReference
Ascorbate peroxidase
Alfalfa only severe: 15%[142]
Arabidopsis thalianaAPX1 1.66-fold 800%[143]
Arabidopsis thalianaAPX1 ns [144]
Arabidopsis thalianaAPX3 2-fold [143]
Antioxidants 08 00094 i001 Antioxidants 08 00094 i002[145]
Carrizo citrange APX2 5.5-fold 50%[146]
Carrizo citrange cAPX 2-fold Total ns [147]
Cleopatra mandarinAPX2 10-fold 50%[146]
Cleopatra mandarincAPX 0.5-fold Total ns [147]
Antioxidants 08 00094 i003 Antioxidants 08 00094 i004[148]
Cotton (tol) up to 50%[149]
Antioxidants 08 00094 i005 Antioxidants 08 00094 i006[150]
Date PalmAPX-46 4-fold [151]
Date PalmAPX-1 4-fold [151]
Maize 25%[152]
PeacAPX1 3-fold (not log2-fold)cAPX1 50%[136]
Antioxidants 08 00094 i007 Antioxidants 08 00094 i008[153]
TobaccoAPXI 299 % 300%[155]
TobaccothyAPX and strAPX ns [156]
Wheat2.29-fold (rel. expression)35%[157]
Catalase (CAT)Alfalfa 100 % (moderate)[142]
Alfalfa ns (severe)[142]
Arabidopsis thaliana 30%[158]
Carrizo citrange 1.5-foldns[147]
Cleopatra mandarin 1.5-foldns[147]
Antioxidants 08 00094 i009 Antioxidants 08 00094 i010[148]
Maize 50%[152]
Pea 100%[136]
Antioxidants 08 00094 i011 Antioxidants 08 00094 i012[154]
TobaccoCAT1-2 ns [156]
TobaccoCAT3 2.4-fold (rel. expression)45%[155]
Antioxidants 08 00094 i013 Antioxidants 08 00094 i014[159]
Cotton up to 50%[149]
Fescue 33%[160]
reductase (DHAR)
Date PalmDHAR-25 1.4 fold [151]
Date PalmDHAR-2 1.4-fold [151]
Wheat2.3-fold (rel. expression)44%[157]
Antioxidants 08 00094 i015 Antioxidants 08 00094 i016[161]
Glutathione peroxidase
Alfalfa ns[142]
Antioxidants 08 00094 i017 Antioxidants 08 00094 i018[153]
Potato2.9-fold (rel. expression) [162]
Tortula 50%[163]
Antioxidants 08 00094 i019 Antioxidants 08 00094 i020[164]
Glutathione reductase
Arabidopsis thaliana 65%[158]
Carrizo citrange2-fold90%[147]
Cleopatra mandarin2-fold50%[147]
Cottonup to 80%[149]
Antioxidants 08 00094 i0213.5-fold (rel. expression)
4-fold (rel. expression)
Antioxidants 08 00094 i022[165]
Maize 33%[152]
Antioxidants 08 00094 i023 Antioxidants 08 00094 i024[153]
Tobacco1.6-fold (rel. expression) [156]
Tobacco 35%[155]
Tortula 100%[163]
Wheat2.1-fold (rel. expression)30%[157]
Antioxidants 08 00094 i025 Antioxidants 08 00094 i026[164]
Glutathione S-transferase (GST)Tortula 40%[163]
Antioxidants 08 00094 i027 Antioxidants 08 00094 i028[161]
Monodehydroascorbate reductase (MDHAR)Wheat2.3-fold (rel. expression)65%[157]
Tobacco1.6-fold (rel. expression) [156]
Protein disulphide isomerase (PDI)Stiff bromeBdPDIL1-1 > 1-fold (rel. expression) [166]
Stiff bromeBdPDIL1-2 0.67-fold, [166]
Stiff bromeBdPDIL7-2 0.33-fold [166]
Stiff bromeBdPDIL2-1 > 1-fold (rel. expression)[166]
Stiff bromeBdPDIL3-1, BdPDIL5-1 and BdPDIL8-1 (between 0.33 and 1-fold)[166]
Peroxiredoxin (PRX)Date PalmPRXR-18 1.1-fold [151]
Date PalmPRXR-1 1.5.fold[151]
Date PalmPRXR-2 4.3-fold[151]
Superoxide dismutase (SOD) Alfalfa Total SOD ns [142]
Alfalfa MnSOD 30%[142]
Arabidopsis thaliana 100%[158]
Arabidopsis thalianans [144]
Antioxidants 08 00094 i029 Antioxidants 08 00094 i030[145]
Carrizo citrange CuZnSOD 2-foldns[147]
Cleopatra mandarinFeSOD 1.5-fold100%[147]
Antioxidants 08 00094 i031 Antioxidants 08 00094 i032[148]
Date Palm up to 450%[151]
Blue Grass 100% (25 d of stress)[160]
Fescue 30% (25 d of stress)[160]
MaizeSOD-13 1.2-fold20%[152]
MaizeSOD-11 1.26-fold [152]
Pea 100% (chloroplast and cytosol)[136]
Antioxidants 08 00094 i033 Antioxidants 08 00094 i034 [153]
Antioxidants 08 00094 i035 Antioxidants 08 00094 i036[154]
Antioxidants 08 00094 i037 Antioxidants 08 00094 i038[159]
Thioredoxin (TRX)Date Palm
TRX-40 1.1-fold
TRX-44 1.3-fold
TRX -37 1.3-fold
TRX -16 1.3-fold
TRX -31 1.3-fold
TRX -12 1.1-fold
Date Palm [151]
Date Palm [151]
Date Palm [151]
Date Palm [151]
Date Palm [151]
Antioxidants 08 00094 i039 Antioxidants 08 00094 i040[161]
APX, ascorbate peroxidase; CAT, catalase; DHAR, dehydroascorbate reductase; GPX, glutathione peroxidase; GR, glutathione reductase; GST, glutathione-S transferase; MDHAR, monodehydroascorbate reductase; PDI, protein disulfide isomerase; PRX, peroxiredoxin; SOD, superoxide dismutase; TRX, thioredoxin. Black color, up-regulation; red color, down-regulation; ns, not significantly changed.

Share and Cite

MDPI and ACS Style

Laxa, M.; Liebthal, M.; Telman, W.; Chibani, K.; Dietz, K.-J. The Role of the Plant Antioxidant System in Drought Tolerance. Antioxidants 2019, 8, 94.

AMA Style

Laxa M, Liebthal M, Telman W, Chibani K, Dietz K-J. The Role of the Plant Antioxidant System in Drought Tolerance. Antioxidants. 2019; 8(4):94.

Chicago/Turabian Style

Laxa, Miriam, Michael Liebthal, Wilena Telman, Kamel Chibani, and Karl-Josef Dietz. 2019. "The Role of the Plant Antioxidant System in Drought Tolerance" Antioxidants 8, no. 4: 94.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop