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Article

Hydrogen Peroxide Mitigates Cu Stress in Wheat

by
Bushra Ahmed Alhammad
1,
Mahmoud F. Seleiman
2,3,* and
Matthew Tom Harrison
4
1
Biology Department, College of Science and Humanity Studies, Prince Sattam Bin Abdulaziz University, Al Kharj Box 292, Riyadh 11942, Saudi Arabia
2
Plant Production, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, Saudi Arabia
3
Department of Crop Sciences, Faculty of Agriculture, Menoufia University, Shibin El-kom 32514, Egypt
4
Tasmanian Institute of Agriculture, University of Tasmania, Newnham Drive, Launceston 7248, Australia
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(4), 862; https://doi.org/10.3390/agriculture13040862
Submission received: 5 March 2023 / Revised: 11 April 2023 / Accepted: 12 April 2023 / Published: 13 April 2023
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Abstract

:
Abiotic stress imposed by heavy metals (HMs) adversely influences plant growth. In crop plants, such stresses penalize grain yield and ultimately could have enduring connotations for sustainable food security. Although copper (Cu) is an essential micronutrient for crop life, excessive availability of copper impairs plant growth and/or reproductive performance. Anecdotal evidence suggests that hydrogen peroxide (H2O2) is produced in plants under either biotic or abiotic stresses to mitigate oxygen-derived cell toxicity, although the influence of H2O2 remains to be definitively quantified. Here, our aim was to investigate the effects of hydrogen peroxide (H2O2) on the growth, grain yield, and yield components, as well as copper uptake of stressed wheat grown in sandy soil. We found that applications rates of 150 or 300 mg Cu kg−1 soil significantly reduced net photosynthesis, leaf area, chlorophyll, and grain yield. Foliar application of H2O2 to plants grown under 150 and 300 mg Cu kg−1 soil had improved growth, physiological, and yield traits. For instance, foliar application of H2O2 Cu-stressed plants grown under 300 mg Cu kg−1 soil reduced detrimental effects of Cu toxicity by −12% in terms of grains per spike and −7% for 1000-grain weight in comparison to the control treatment. Foliar application of H2O2 on wheat grown under copper stress reduced accumulation of other heavy metals such as cadmium. We suggest that the potential for foliar application of H2O2 in mitigating heavy metal stress in crop plants has large global potential; however, further work is required to elucidate the environmental conditions and application rates required to attain optimal benefit.

1. Introduction

Agricultural practices such as irrigating crops with wastewater, sludge application, pesticide, and fertilization can increase heavy metal (HM) soil concentrations [1,2,3,4,5]. Unlike organic contaminants, HM contaminants are efficiently transferred from the soil to plant organs [6,7,8,9,10]. Abiotic stresses—such as those due to sub- or supraoptimal temperature, or water deficit [11,12,13] adversely affect plant growth and grain yield, which ultimately have negative connotations for agri-food sustainability [7,8,9,14,15,16,17,18]. Ionic toxicity caused by HMs impairs functional processes, including the active sites of enzymes, polynucleotides, cellular structural proteins, and biological molecules essential for transportation of nutrients. Similar to other stressors, effects caused by HMs may impair biochemical activities, physiological processes, and ultimately plant growth and development [1,17,19,20]. Toxic thresholds of HMs not only reduce rhizosphere microbial activity and crop yield, but cascade through the food chain to threaten human health [9,21]. For example, high prevalence of stomach cancer was related to the food products contaminated with excessive quantities of cadmium (Cd), Pb (lead), Cr (chromium), and Cu (copper) that were ingested by vegetables and fruits [22]. It is therefore crucial to diminish the HM applications onto agricultural soils but also lessen the impacts of existing HMs on crop production and yield [23].
Copper is considered one of the most health-hazardous HMs for food and fodder consumers. Although Cu is necessary in key metabolic enzymes and proteins as a cofactor [24,25], excessive Cu concentrations in the soil can be toxic [26]. Among essential micronutrients for plants, Cu is vital for optimum functioning in agricultural crops, with Cu being an active redox transition metal required in several biochemical and physiological functional processes. In soil and biological systems, the metal occurs as monovalent (Cu1+) and divalent (Cu2+), often bound with other biological molecules [27]. However, beyond permissible concentrations, Cu is harmful, potentially destabilizing cellular membranes, impairing photosynthetic activity and enzymic function, and causing detrimental effects on both plant growth and yield [28,29]. Copper is recognized as a “soil pollutant” and has attracted scientific attention due to recent anthropogenic activities. Agricultural and industrial practices, and improper disposal of Cu-containing compounds are contributing to excessive accumulations of Cu in agricultural lands [27,28,29]. Excessive concentrations of Cu in the rhizosphere can cause oxidative stress by promoting the generation of reactive oxygen species (ROS) [30], which may negatively impact seed germination [31], essential nutrient uptake [30], chlorophyll synthesis, and mineral ion balance [31].
Abiotic stress caused by HMs can enhance ROS production in plants. Hydrogen peroxide (H2O2) is considered one of the ROS produced in plants grown under either biotic or abiotic stresses, playing a vital role against O2−-derived cell toxicity [31,32,33,34]. A recent investigation reported that application of H2O2 at low concentrations (16 and 30 mM) acted as a signaling molecule for mediating plant physiological and biochemical responses to stresses, although H2O2 in some cases damaged plant cells if accumulated in cellular compartments [35]. From these observations, we hypothesize that exogenous application of H2O2 may mimic internal biosynthesis of H2O2, relieve stress caused by excessive Cu, and enable homeostatic growth functioning typically seen over the long-term [19].
Wheat (Triticum aestivum L.) is considered one of the most important crops for maintenance of food security for a burgeoning global population [36,37,38,39,40,41,42]. In 2018, wheat crops were harvested over 214.3 M ha [43]; global wheat production and grain yield ha−1 increased from 585 Mt and 2.7 t ha−1 in 2000 to 734 Mt and 3.4 t ha−1 in 2018 [43]. Around 30% of the global population relies on wheat to fulfill calories and protein requirements [44]; with population growth, wheat demand is expected to increase by 70% by 2050 [45]. Satisfying this demand will partly be realized by overcoming environmental stresses, including those due to HMs [8].
The aim of this study was therefore to investigate the effects of hydrogen peroxide (H2O2) on growth, physiology, yield traits, and metal ion uptake of Cu-stressed wheat plants.

2. Results

2.1. Effects of Hydrogen Peroxide on Plant Height of Wheat under Cu Stress

The results presented in Figure 1 show that Cu stress (i.e., 300 mg Cu kg−1 soil) significantly reduced plant height at different growth stages in comparison to plants grown with 150 mg Cu kg−1 soil or control treatment (untreated soil with Cu). However, foliar application of hydrogen peroxide (30 µM H2O2) resulted in the highest plants of wheat grown without or with Cu stress at different growth stages. At 100 DAS, plants treated with only H2O2 were 17 and 21% higher than those grown with 150 mg Cu kg−1 soil + H2O2 and 300 mg Cu kg−1 soil, respectively.

2.2. Effects of Hydrogen Peroxide on Leaf Area of Wheat under Cu Stress

The total leaf area of wheat plants grown with 300 mg Cu kg−1 soil + H2O2 and with only 300 mg Cu kg−1 soil was reduced by 27 and 48% compared with those grown in control at 100 DAS, respectively (Figure 2), while the total leaves area of wheat plants grown with only H2O2, 150 mg Cu kg−1 soil + H2O2, and 150 mg Cu kg−1 soil was increased by 28, 9.5, and 0.2% compared with those obtained from plants grown under control treatment at 100 DAS, respectively (Figure 2). In general, the total leaves area of wheat plants grown with 150 mg Cu kg−1 soil, 300 mg Cu kg−1 soil + H2O2, and 300 mg Cu kg−1 soil was reduced by 6, 31, and 49% compared with those grown in the control, respectively (Figure 2). However, the total leaves area of wheat plants grown with H2O2 and 150 mg Cu kg−1 soil + H2O2 was increased by 23 and 7% compared with those obtained from plants grown under control treatment, respectively.

2.3. Effects of Hydrogen Peroxide on Whole Dry Weight of Wheat under Cu Stress

Whole plant dry weight (i.e., root, shoot, and leaves) steadily increased from 0.29 to 39 g DM plant−1 at 45 and 60 DAS, and from 0.90 to 3.84 g DM plant−1 at 75 and 100 DAS as average under different treatments, respectively (Figure 3). On the other hand, whole plant dry weight of wheat grown with 150 mg Cu kg−1 soil, 300 mg Cu kg−1 soil + H2O2, and with only 300 mg Cu kg−1 soil was reduced by 15, 32, and 45% compared with those grown in control at 100 DAS, respectively (Figure 3). Total plant dry weight of wheat grown with only H2O2 and 150 mg Cu kg−1 soil + H2O2 soil was increased by 21 and 12% compared with those obtained from plants grown under control treatment at 100 DAS, respectively (Figure 3).

2.4. Effects of Hydrogen Peroxide on Total Chlorophyll of Wheat under Cu Stress

Compared with plants grown under control treatment at four growth stages, the total chlorophyll of wheat plants grown with only H2O2 and 150 mg Cu kg−1 soil + H2O2 soil was not significant (Figure 4). However, total chlorophyll of wheat grown with 150 mg Cu kg−1 soil, 300 mg Cu kg−1 soil + H2O2, and with only 300 mg Cu kg−1 soil was significantly reduced by 3, 33, and 24% compared with those grown in control at 72 DAS, respectively (Figure 4).

2.5. Effects of Hydrogen Peroxide on Net Photosynthesis and Stomatal Conductance of Wheat under Cu Stress

Data presented in Figure 5 and Figure 6 show the positive effect of H2O2 and the negative effect of Cu stress on net photosynthesis and stomatal conductance of wheat plants, while net photosynthesis and stomatal conductance rates of wheat plants were lower by 5 and 6% with 150 mg Cu kg−1 soil + H2O2; 23 and 13% with 150 mg Cu kg−1 soil; 36 and 27% with 300 mg Cu kg−1 soil + H2O2; and 51 and 44% with 300 mg Cu kg−1 soil than those obtained from the control treatment at 100 DAS, respectively (Figure 5 and Figure 6).

2.6. Effects of Hydrogen Peroxide on Growth Traits of Wheat under Cu Stress

Plant growth traits in terms of the number of leaves per plant, number of tillers per plant, spike length, and number of spikelets per spike were significantly and negatively affected under Cu stress, while the foliar application of H2O2 alleviated the negative effects of Cu (Figure 7). For instance, a single application of 300 mg Cu kg−1 soil resulted in a significant reduction in leaves per plant, the number of tillers per plant, spike length, and the number of spikelets per spike by 27, 31, 31, and 26% compared to those obtained from control treatment, respectively (Figure 7). However, foliar application of H2O2 reduced the negative effects of 300 mg Cu kg−1 soil to 13, 3, 15, and 15% for the number of leaves per plant, number of tillers per plant, spike length, and number of spikelets per spike in comparison to those grown with control treatment, respectively (Figure 7).

2.7. Effects of Hydrogen Peroxide on Yield Traits of Wheat under Cu Stress

Single applications of 150 and 300 mg Cu kg−1 soil significantly reduced the number of grains per spike by 4 and 23%, grain weight per spike by 2 and 25%, and 1000-grain weight by 0.3 and 19% in comparison to control treatment, respectively (Figure 8). However, foliar application of H2O2 into plants grown under the stress of 300 and 150 mg Cu kg−1 soil reduced the negative effect of Cu by −12 and +1% for the number of grains per spike, −18 and +0.3% for grain weight per spike, and −7 and +0.3% for 1000-grain weight in comparison to the control treatment, respectively (Figure 8).

2.8. Effects of Hydrogen Peroxide on Cu, Zn, and Cd Concentration of Whole Wheat Plants Grown under Cu Stress

Stressed wheat plants with 300 mg Cu kg−1 soil significantly contained the highest Cu (18 mg kg−1 DM) and Cd (0.70 mg kg−1 DM) followed by stressed plants with 150 mg Cu kg−1 soil in comparison to unstressed plants (control; 15 mg Cu kg−1 DM and 0.50 mg Cd kg−1 DM) or plants treated with H2O2 (12 mg kg−1 DM and 0.39 mg Cd kg−1 DM) (Figure 9). However, plants treated only with H2O2 contained the highest Zn (16.6 mg kg−1 DM), followed by plants treated with mg Cu kg−1 soil + H2O2 (16.2 mg kg−1 DM) and untreated plants (15.5 mg kg−1 DM) compared to plants treated with 300 mg Cu kg−1 soil (14.6 mg Zn kg−1 DM).

3. Discussion

Recent work suggests that exogenous application of H2O2 can enhance abiotic stress resistance and improve plant growth via protecting sub-cellular structures [46] under salinity [47], drought [48], high temperatures [49], or superfluous water stress [19,50,51]. Therefore, our study was performed to investigate the beneficial effects of H2O2 and its link to Cu stress tolerance in wheat plants grown in sandy soil. In the current investigation, single applications of 150 and 300 mg Cu kg−1 soil negatively affected growth, physiological traits, yield, and yield-related attributes in comparison to unstressed plants.
Plant growth relies on the uptake of water, ability to alleviate water stress [52], and mineral induction over the root hairs’ plasma membranes. This is controlled by a network of hormones to rearrange the growth and oxidation-reduction reactions in meristematic plant tissues. Although Cu is required for plant growth and is involved in some vital plant metabolic processes with low concentration, its excessive application can cause toxicity for plants and the environment [53]. Plant root systems play an active role in Cu uptake from the soil which is then transported via the xylem to aerial plant parts. In addition to the apoplast pathway, considering Cu an essential micronutrient, root cells have copper transporter proteins to actively absorb Cu. Furthermore, Cu in its cationic form (Cu1+, Cu2+) is attracted by negative cell wall charges produced by cellulose, glycoproteins, and pectin [54]. The excessive accumulation of Cu on the root surface leads to disruption of the cell membrane, inhibition of root hair development, deformation of roots, and impaired root growth [33]. Plant growth indicators such as plant height, leaf area, and dry mass weight were significantly affected by Cu stress in this study and stood consistently lower throughout the plant’s life as compared with control treatments (Figure 1, Figure 2 and Figure 3). Plant growth relies on the uptake of water and mineral induction over the root hairs’ plasma membranes [53]. Hossain et al. [55] reported inhibited root and shoot growth and lower biomass production in Lens culinaris under high Cu stress (3.0 mM). In Arabidopsis thaliana, Cu stress showed altered cell division and elongation and disrupted auxin homeostasis which in return significantly inhibited growth [56]. Copper at the rate of 800 mg Kg−1 soil caused distortion of leaf the blade and reduced leaf area in Arachis hypogeae [57]. Similarly, decreased stem size and leaf expansion were also reported in Cu-stressed Brassica napus and Brassica juncea [58]. The reduction in leaf area and plant height under Cu stress could be associated with lignin accumulation in the xylem and hardening of the cell wall which negatively affects cell division and enlargement [22].
Impaired photosynthetic activity, reduced gaseous exchange, and disruption of the biosynthesis of photosynthetic pigments are among the most common effects of Cu toxicity in plants [54]. Results showed that Cu treatments as 150 mg Cu kg−1 soil and 300 mg Cu kg−1 soil significantly reduced the total chlorophyll contents (SPAD), net photosynthesis, and stomatal conductance in wheat plants as compared to control (Figure 4, Figure 5 and Figure 6). Copper plays an important role in the biosynthesis of photosynthetic pigments in plants; however, its high accumulation in leaves can seriously affect chlorophyll production. Several studies have reported the Cu stress-induced reduction in photosynthetic pigments in a number of crop plants, such as spinach, Spinacia oleracea L. [33]; maize, Zea mays L. [59]; cauliflower, Brassica oleracea var. botrytis L. [60]; Chinese cabbage, Brassica rapa subsp. Pekinensis L. [61,62]; sunflower, Helianthus annuus L. [63]; and mustard, Brassica juncea L. [64]. These results can be associated with the disruption of enzymatic activity in the metabolic pathway of chlorophyll synthesis as well as reduced development of chloroplasts [32]. Furthermore, Cu toxicity is linked with damage of the ultrastructure of mesophyll chloroplast, alters the chemical composition of the thylakoid membrane, and reduces lipid concentration in chloroplast membranes [65,66]. Moreover, Cu toxicity induces physiological impairment of photosynthesis by limiting the Rubisco activity, inhibiting the electron transport chain, and declining the photosystem II (PS II) efficiency [27,67]. Panou-Filotheou et al. [68] reported a reduced volume and number of mesophyll chloroplasts in Cu-stressed Origanum vulgare plants. Feigl et al. [69] found a significant reduction in photosynthetic pigments in young Indian mustard and rapeseed plants when exposed to high Cu concentrations. Furthermore, Aly and Mohamed [70] noted a 55.8% decline in maize’s total chlorophyll contents under Cu stress. These deleterious effects of Cu toxicity may be associated with lower uptake of iron (Fe) and phosphorous (P) in stressed plants as compared to non-stressed [71]. Moreover, high accumulation of Cu in leaves also affected photosynthesis due to stomatal factors. Damage to PSII, electron transport chain, and Rubisco consequently lowers the CO2 assimilation which in return increases intercellular CO2 concentration and hence promotes stomatal closure [54].
Copper is essential for plant growth and development. However, it becomes lethal when it exceeds a tolerable limit which may lead to retarded growth and loss of economic production. Thus, the lower agricultural yield of crop plants is a final consequence of changes made by Cu toxicity initially at mineral, biochemical, and physiological levels. Our study showed a significant decline in growth, yield, and yield-related attributes when Cu stress was imposed both as 150 mg Cu kg−1 soil and 300 mg Cu kg−1 soil in wheat plants (Figure 7, Figure 8 and Figure 9). The high accumulation of Cu disrupts the ionic balance of various essential nutrients in plants by altering nutrient uptake mechanisms, and osmotic balance and by damaging transport channel proteins. Interestingly, the reduction in Fe, Zn, P, N, and Mg concentrations in leaves of plants under Cu stress are directly linked with lower leaf area, plant height, number of branches, total chlorophyll contents, and lower grain yield [54,72]. The Cu stress-mediated reduction in photosynthesis affects the net CO2 assimilation negatively. Consequently, declined phosphate triose, a major constituent of structural and nonstructural components of plants, culminates in lower vegetative growth, slower development, and hence lower yield [73].
However, foliar application of H2O2 alleviated the negative effects of 300 and 150 mg Cu kg−1 soil on the above-mentioned traits (Figure 1, Figure 2, Figure 3, Figure 4, Figure 5, Figure 6, Figure 7, Figure 8 and Figure 9). Hydrogen peroxide can inhibit Cu-inflicted alterations in H2O2 and O2− radicals, and it can reduce ascorbate bonds [74]. It regulates the antioxidant system as a major mechanism of Cu-toxicity [53,54]. Hydrogen peroxide also can modulate proline accumulation in leaves of rice exposed to Cu stress [75].
In the current study, the single applications of 150 and 300 mg Cu kg−1 soil significantly reduced plant height, whole dry weight per plant, photosynthesis, leaf area, and chlorophyll traits in comparison to the control treatment (Figure 1, Figure 2, Figure 3, Figure 4, Figure 5 and Figure 6). However, foliar application of H2O2 into plants grown under the stress of Cu resulted in an improvement in growth and physiological traits (Figure 1, Figure 2, Figure 3, Figure 4, Figure 5 and Figure 6). This could be due to the metabolism of H2O2 in seedlings of wheat since it can be involved as a signal in the processes of laser-induced water acclimation. Hydrogen peroxide plays a vital role in plant growth and physiological traits such as the seed’s germination [56,76,77], root development system [78], and stomatal aperture regulation [79]. It can be produced in plant cells through numerous routes; for instance, photorespiration, redox reaction, and electron transport chain [46]. This indicates that H2O2 can positively affect plant growth of different parts via enhancing endogenous H2O2, or by regulating relative gene expression. Such changes can positively affect plant growth and development in terms of antioxidant enzyme activity [77]. Hydrogen peroxide can maintain chloroplast ultrastructure to sustain the photosynthesis process under Cu stress [46,54]. Furthermore, it might be involved in signaling crosstalk between nitric oxide and hydrogen sulfide to persuade thermotolerance in the seedlings of maize [6,79]. The vital role of H2O2 might be due to it promoting photosynthetic genes by brassinosteroids (BRs) and reducing the generation of ROS, from which can be inferred that the Calvin cycle and sugar metabolism are regulated by H2O2 and 24-epibrassinolide (EBR) via redox signaling, thus enhancing photosynthetic efficiency and conclusively crop productivity in under HM stress such as Cu [80,81].
Hydrogen peroxide can act as a stress transducer for enhancing plant stress resistance [40]; consequently, it can mediate stress defense and enhance metabolic functions in plants grown under environmental stress [82]. Different researchers reported that exogenous application of H2O2 can influence plant growth; however, the effect may differ depending on concentrations. For example, the application of H2O2 into rice plants with 100–500 µM H2O2 impeded root expansion; conversely, a lower application (0–100 µM) improved root diameter and cell elongation [83]. Furthermore, H2O2 application with 90 µM can stimulate root systems in wheat plants [84]. Application of H2O2 with an optimal application can improve chlorophyll, while its elevated application can cause chlorophyll degradation in different wheat genotypes [85]. In Brassica juncea, foliar applications of H2O2 (i.e., 25, 50, or 100 µM) improved net photosynthesis and growth parameters, but 50 µM was reported to be the optimal dose [86].
In the current investigation, the application of H2O2 improved the stomatal conductance of wheat plants stressed with Cu at different growth stages, particularly 150 and 300 mg H2O2 kg−1 soil in comparison to untreated plants with H2O2 (Figure 6). It was reported that foliar application of H2O2 enhanced stomatal conductance in Solanum lycopersicum, and such enhancement can occur through the interaction of BR and H2O2 which can cause an osmotic modification for reducing stomata opening [53]. In addition, Kumari and Verma [87] revealed that the stomatal opening in wheat plants treated with foliar application of H2O2 was rehabilitated due to the correlation with the reduction of stomatal development and its size. Enhancing stomata closure as a result of the exogenous application of H2O2 might be attributable to the reduction in K+ concentration and the amplification of K+ discharge at the plasma membrane of the guard cell via K+ channels [88].
Although stressed plants with Cu produced the lowest yield and its components, the application of H2O2 into stressed wheat plants improved the yield and its components (Figure 8). In this respect, the application of H2O2 into plant roots significantly enhanced growth and yield-related traits as well as improved physiological traits such as photosynthesis and antioxidant enzymes of plants grown with 100 mg Cu kg−1 soil [53]. Moreover, Fariduddin et al. [89] reported the positive role of H2O2 as a foliar application (2.5 mM) on the antioxidant metabolism in stressed Vigna radiata with Cu. Additionally, Guzel and Terzi [90] reported that the growth of Cu-stressed Zea mays plants was improved with H2O2 via defensive endogenous cellular structures as well as improvements of minerals and osmotic solute concentrations in leaves. Hasan et al. [91] investigated the effect of hydrogen peroxide (0.1, 0.5, 1.0, and 1.5 mM) on the optimization growth and photosynthetic traits of cowpea. They reported that hydrogen peroxide (0.5–1.0 mM) enhanced the photosynthetic traits such as water use efficiency, net photosynthesis, and chlorophyll content as well as enhanced growth traits such as root and shoot length and fresh and dry weight of cowpea. Hydrogen peroxide improved the activity of peroxidase and catalase enzymes and leaf proline content [91].

4. Materials and Methods

4.1. Plant Materials and Treatments

The current study was conducted to investigate the effects of hydrogen peroxide (H2O2) on the growth, and physiological and yield traits of wheat (Triticum aestivum L., cv. Gemmeiza 12) grown under Cu stress (0, 150, 300 mg Cu kg−1 soil) at the glasshouse of the College of Food and Agriculture Sciences, King Saud University, Saudi Arabia during 2019–2020. The experiment included six combination treatments of Cu (CuSO4·5H2O, AppliChem Panreac, Darmstadt, Germany) and H2O2 (30 µM, Merck KGaA, Darmstadt, Germany) as follows: Control (zero Cu + zero H2O2), H2O2 (zero Cu + 30 µM H2O2), 150 Cu (150 mg Cu kg−1 soil + zero H2O2), 150 Cu + H2O2 (150 mg Cu kg−1 soil + 30 µM H2O2), 300 Cu (300 mg Cu kg−1 soil + zero H2O2), and 300 Cu + H2O2 (300 mg Cu kg−1 soil + 30 µM H2O2). The Cu treatments were applied prior to the sowing process, and were well mixed with soil in each pot, while hydrogen peroxide treatments were exogenously applied at 35 and 50 days after sowing (DAS). Different treatments were placed in a completely randomized design, and each treatment was repeated four times.
A contaminated sandy loam soil (sand 57.0%, silt 28.2%, and clay 14.8) due to the irrigation with treated wastewater for about fifteen years was used as an experimental soil. The soil was collected from the Agricultural Research Station of King Saud University (24°42′ N, 44°46′ E, 400 m asl), Saudi Arabia. The soil was air-dried, grinded, and screened by passing through a 2 mm sieve. Soil pH, EC, and OM were 7.85, 3.69 dS m−1, and 0.48%, respectively. The soil macro elements were N 3.5 g kg−1, P 1.65 g kg−1, and K 0.09 mg kg−1, while soil trace elements were Mn 46.7 mg kg−1, Cu 12.0 mg kg−1, Cd 6.5 mg kg−1, Co 0.9 mg kg−1, and Zn 9.1 mg kg−1.
In each pot, a weight of 5 kg of soil was added. Approximately, 13 wheat grains were dibbled at 3–5 cm depth in each pot on 15 November 2019. NPK fertilizers were added in three doses (i.e., 20, 40, and 40% of the total doses) during the growing period as recommended by the Agricultural Ministry. At 14 DAS, ten healthy seedlings were kept in each pot. The plants were treated with hydrogen peroxide through foliar application at 35 and 50 DAS. Furthermore, untreated plants were also sprayed with distilled water. A 20 mL hydrogen peroxide with distilled water was sprayed on plants in each pot to ensure full foliage coverage.

4.2. Measurements

4.2.1. Plant Height and Leaf Area

Plant samples were collected at 45, 60, 75, and 100 DAS, washed with distilled water and blotted with tissue papers. Plant height was manually measured using a ruler. Moreover, the leaf area of all green leaves from collected plants at each sampling date was measured using a leaf area meter (LI-3000C, Portable Leaf Area Meter, LI-COR Inc., Lincoln, NE, USA).

4.2.2. Number of Leaves, Number of Tillers, and Whole Dry Weight per Plant

The number of leaves and tillers per plant was recorded at the end of the experiment. In addition, the whole plant was weighed (leaves, shoots, and roots) to obtain the fresh weight quantum of each part. The plant samples were placed in an oven at +65 °C until the constant dry weight was obtained. Dried plant parts were ground into a fine powder (0.5 mm size) and stored for elemental analysis.

4.2.3. Total Chlorophyll

Total chlorophyll was recorded through a SPAD meter (Model: SPAD-502, Minolta Sensing Ltd., Osaka, Japan). Five flag leaves of wheat were used for measuring total chlorophyll in each pot at 42, 57, 72, and 97 DAS.

4.2.4. Gas Exchange Characteristics

The measurements, such as net photosynthetic rate and stomatal conductance, were taken at 42, 57, 72, and 97 DAS using the portable gas meter (Li-6400, Li-COR, Lincoln, NE, USA). The flag leaf was used for these measurements between 10 a.m. and 12 p.m.

4.2.5. Yield Traits

At physiological maturity, wheat plants were manually harvested and grain yield and related parameters (spike length (cm), number of spikelets spike−1, number of grains spike−1, grains weight spike−1, and 1000-grain weight (g)) were recorded.

4.2.6. Elemental Analysis

Trace elements (i.e., Cu, Cd, and Zn) were analyzed in whole plant dry weight of wheat at the end of the experiment as described by Seleiman et al. [1]. Ground plant samples (200 mg) were weighed and inserted into PTFE Teflon tubes (CEM, Matthews, North Carolina, USA). For microwave digestion, 6 mL of nitric acid (67%) and 1 mL of hydrogen peroxide (30%) were inserted into Teflon tube with the plant sample. The digested wheat plant samples were filtered via a Whatman paper (grade No. 4). The filtered samples were diluted using distilled water to a constant volume. The analysis of Cu, Cd, and Zn was done using Inductively Coupled Plasma-Optical Emission Spectrometry (iCAP 6200, Thermo Fisher Scientific, Cambridge, UK).

4.3. Statistical Analysis

Raw data obtained from the effects of hydrogen peroxide on growth, physiological, and yield traits of wheat grown under different levels of Cu were statistically analyzed (analysis of variance; ANOVA) using PASW statistics 21.0 (IBM Inc., Chicago, IL, USA). Least Significant Difference (LSD at p ≤ 0.05) was used to compare the differences between the mean of different treatments.

5. Conclusions

Single applications of 150 and 300 mg Cu kg−1 soil significantly reduced photosynthesis traits, leaf area, chlorophyll, grain yield, and yield-related traits in comparison to the control treatment. However, foliar application of H2O2 into plants grown under the stress of 300 and 150 mg Cu kg−1 soil resulted in an improvement in growth, physiological, and yield traits. For instance, foliar application of H2O2 into plants grown under the stress of 300 mg Cu kg−1 soil reduced the negative effect of Cu by −11.7% for the number of grains per spike and −6.91% for 1000-grain weight in comparison to the control treatment, respectively. In addition, foliar application of H2O2 on wheat grown in soil stressed with Cu reduced the accumulation of trace elements (i.e., Cd and Cu) and increased Zn in the whole plant compared to those obtained from untreated plants. Consequently, foliar application of H2O2 can enhance the growth and grain yield of wheat under Cu stress in sandy soil.

Author Contributions

Conceptualization, B.A.A. and M.F.S.; methodology, B.A.A. and M.F.S.; software, M.F.S.; validation, B.A.A.; formal analysis, B.A.A. and M.F.S.; investigation, B.A.A. and M.F.S.; resources, M.F.S. and M.T.H.; data curation, B.A.A.; writing—original draft preparation, M.F.S.; writing—review and editing, B.A.A. and M.T.H. All authors have read and agreed to the published version of the manuscript.

Funding

The authors extend their appreciation to the Deputyship for Research and Innovation, Ministry of Education in Saudi Arabia for funding this research work through the project number (IF2/PSAU/2022/01/19487).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data are presented within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Seleiman, M.F.; Santanen, A.; Stoddard, F.L.; Mäkelä, P.S.A. Feedstock quality and growth of bioenergy crops fertilized with sewage sludge. Chemosphere 2012, 89, 1211–1217. [Google Scholar] [CrossRef] [PubMed]
  2. Bi, C.; Zhou, Y.; Chen, Z.; Jia, J.; Bao, X. Heavy metals and lead isotopes in soils, road dust and leafy vegetables and health risks via vegetable consumption in the industrial areas of Shanghai, China. Sci. Total Environ. 2018, 619, 1349–1357. [Google Scholar] [CrossRef] [PubMed]
  3. Seleiman, M.F.; Selim, S.; Jaakkola, S.; Mäkelä, P. Chemical composition and in vitro digestibility of whole-crop maize fertilized with synthetic fertilizer or digestate and harvested at two maturity stages in boreal growing conditions. Agric. Food Sci. 2017, 26, 47–55. [Google Scholar] [CrossRef] [Green Version]
  4. Alengebawy, A.; Abdelkhalek, S.T.; Qureshi, S.R.; Wang, M.-Q. Heavy Metals and Pesticides Toxicity in Agricultural Soil and Plants: Ecological Risks and Human Health Implications. Toxics 2021, 9, 42. [Google Scholar] [CrossRef] [PubMed]
  5. Seleiman, M.F.; Kheir, A.M.S.; Al-Dhumri, S.; Alghamdi, A.G.; Omar, E.S.H.; Aboelsoud, H.M.; Abdella, K.A.; Abou El Hassan, W.H. Exploring optimal tillage improved soil characteristics and productivity of wheat irrigated with different water qualities. Agronomy 2019, 9, 233. [Google Scholar] [CrossRef] [Green Version]
  6. Seleiman, M.F.; Santanen, A.; Kleemola, J.; Stoddard, F.L.; Mäkelä, P.S.A. Improved sustainability of feedstock production with sludge and interacting mychorriza. Chemosphere 2013, 91, 1236–1242. [Google Scholar] [CrossRef]
  7. Sofy, M.; Seleiman, M.F.; Alhammad, B.A.; Alharbi, B.A.; Mohamed, H.I. Minimizing adverse effects of Pb stress on maize yield, macro elements, and physiological and biochemical traits by combined treatment with jasmonic acid, salicylic acid, and proline. Agronomy 2020, 10, 699. [Google Scholar] [CrossRef]
  8. Rai, P.K.; Lee, S.S.; Zhang, M.; Tsang, Y.F.; Kim, K. Heavy metals in food crops: Health risks, fate, mechanisms, and management. Environ. Int. 2019, 125, 365–385. [Google Scholar] [CrossRef]
  9. Mununga Katebe, F.; Raulier, P.; Colinet, G.; Ngoy Shutcha, M.; Mpundu Mubemba, M.; Jijakli, M.H. Assessment of Heavy Metal Pollution of Agricultural Soil, Irrigation Water, and Vegetables in and Nearby the Cupriferous City of Lubumbashi, (Democratic Republic of the Congo). Agronomy 2023, 13, 357. [Google Scholar] [CrossRef]
  10. Rawnsley, R.P.; Smith, A.P.; Christie, K.M.; Harrison, M.T.; Eckard, R.J. Current and future direction of nitrogen fertiliser use in Australian grazing systems. Crop Pasture Sci. 2019, 70, 1034–1043. [Google Scholar] [CrossRef]
  11. Langworthy, A.D.; Rawnsley, R.P.; Freeman, M.J.; Pembleton, K.G.; Corkrey, R.; Harrison, M.T.; Lane, P.A.; Henry, D.A. Potential of summer-active temperate (C3) perennial forages to mitigate the detrimental effects of supraoptimal temperatures on summer home-grown feed production in south-eastern Australian dairying regions. Crop Pasture Sci. 2018, 69, 808–820. [Google Scholar] [CrossRef]
  12. Phelan, D.C.; Harrison, M.T.; McLean, G.; Cox, H.; Pembleton, K.G.; Dean, G.J.; Parsons, D.; do Amaral Richter, M.E.; Pengilley, G.; Hinton, S.J.; et al. Advancing a farmer decision support tool for agronomic decisions on rainfed and irrigated wheat cropping in Tasmania. Agric. Syst. 2018, 167, 113–124. [Google Scholar] [CrossRef]
  13. Ara, I.; Turner, L.; Harrison, M.T.; Monjardino, M.; deVoil, P.; Rodriguez, D. Application, adoption and opportunities for improving decision support systems in irrigated agriculture: A review. Agric. Water Manag. 2021, 257, 107161. [Google Scholar] [CrossRef]
  14. Seleiman, M.F.; Kheir, A.S. Maize productivity, heavy metals uptake and their availability in contaminated clay and sandy alkaline soils as affected by inorganic and organic amendments. Chemosphere 2018, 204, 514–522. [Google Scholar] [CrossRef]
  15. Abdullahi, N.; Igwe, E.C.; Dandago, M.A. Heavy metal uptake and stress in food crops: A Review. Agric. Sci. Technol. 2021, 13, 323–332. [Google Scholar] [CrossRef]
  16. Seleiman, M.F.; Santanen, A.; Mäkelä, P.S.A. Recycling Sludge on Cropland as Fertilizer–Advantages and Risks. Resour. Conserv. Recycl. 2020, 155, 104647. [Google Scholar] [CrossRef]
  17. Ibrahim, A.; Harrison, M.; Meinke, H.; Fan, Y.; Johnson, P.; Zhou, M. A regulator of early flowering in barley (Hordeum vulgare L.). PLoS ONE 2018, 13, e0200722. [Google Scholar] [CrossRef]
  18. Harrison, M.T.; Roggero, P.P.; Zavattaro, L. Simple, efficient and robust techniques for automatic multi-objective function parameterisation: Case studies of local and global optimisation using APSIM. Environ. Model. Softw. 2019, 117, 109–133. [Google Scholar] [CrossRef]
  19. Liu, K.; Harrison, M.T.; Shabala, S.; Meinke, H.; Ahmed, I.; Zhang, Y.; Tian, X.; Zhou, M. The State of the Art in Modeling Waterlogging Impacts on Plants: What Do We Know and What Do We Need to Know. Earth’s Future 2020, 8, e2020EF001801. [Google Scholar] [CrossRef]
  20. Muchuweti, M.; Birkett, J.; Chinyanga, E.; Zvauya, R.; Scrimshaw, M.D.; Lester, J. Heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: Implications for human health. Agric. Ecosyst. Environ. 2006, 112, 41–48. [Google Scholar] [CrossRef] [Green Version]
  21. Shahid, M.J.; Ali, S.; Shabir, G.; Siddique, M.; Rizwan, M.; Seleiman, M.F.; Afzal, M. Comparing the performance of four macrophytes in bacterial assisted floating treatment wetlands for the removal of trace metals (Fe, Mn, Ni, Pb, and Cr) from polluted river water. Chemosphere 2020, 243, 125353. [Google Scholar] [CrossRef] [PubMed]
  22. McLaughlin, M.J.; Parker, D.R.; Clarke, J.M. Metals and micronutrients-food safety issues. Field Crops Res. 1999, 60, 143–163. [Google Scholar] [CrossRef]
  23. Khan, I.; Seleiman, M.F.; Chattha, M.U.; Jalal, R.S.; Mahmood, F.; Hassan, F.A.S.; Izzet, W.; Alhammad, B.A.; Ali, E.F.; Roy, R.; et al. Enhancing antioxidant defense system of mung bean with a salicylic acid exogenous application to mitigate cadmium toxicity. Not. Bot. Horti Agrobot. Cluj-Napoca 2021, 49, 12303. [Google Scholar] [CrossRef]
  24. Wang, B.; Chu, C.; Wei, H.; Zhang, L.; Ahmad, Z.; Wu, S.; Xie, B. Ameliorative effects of silicon fertilizer on soil bacterial community and pakchoi (Brassica chinensis L.) grown on soil contaminated with multiple heavy metals. Environ. Pollut. 2020, 267, 115411. [Google Scholar] [CrossRef]
  25. Shar, G.Q.; Kazi, T.G.; Shah, F.A.; Shar, A.H.; Soomro, F.M. Variable uptake and accumulation of essential and heavy metals in maize (Zea mays L.) grains of six maize varieties. Aust. J. Basic Appl. Sci. 2011, 5, 117–121. [Google Scholar]
  26. Stobrawa, K.; Lorenc-Plucinska, G. Changes soilin carbohydrate metabolism in fine roots of the native European black poplar (Populus nigra L.) in a heavy metal-polluted environment. Sci. Total Environ. 2007, 373, 157–165. [Google Scholar] [CrossRef]
  27. Mir, A.R.; Pichtel, J.; Hayat, S. Copper: Uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals 2021, 34, 737–759. [Google Scholar] [CrossRef]
  28. Adnan, M.; Fahad, S.; Saleem, M.H.; Ali, B.; Mussart, M.; Ullah, R.; Amanullah, Jr.; Arif, M.; Ahmad, M.; Shah, W.A.; et al. Comparative efficacy of phosphorous supplements with phosphate solubilizing bacteria for optimizing wheat yield in calcareous soils. Sci. Rep. 2022, 12, 11997. [Google Scholar] [CrossRef]
  29. Shabbir, Z.; Sardar, A.; Shabbir, A.; Abbas, G.; Shamshad, S.; Khalid, S.; Murtaza, G.; Dumat, C.; Shahid, M. Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere 2020, 259, 127436. [Google Scholar] [CrossRef]
  30. Adrees, M.; Ali, S.; Rizwan, M.; Ibrahim, M.; Abbas, F.; Farid, M.; Zia-urRehman, M.; Irshad, M.K.; Bharwana, S.A. The effect of excess copper on growth and physiology of important food crops: A review. Environ. Sci. Pollut. Res. 2015, 22, 8148–8162. [Google Scholar] [CrossRef]
  31. Ouzounidou, G. Effect of copper on germination and seedling growth of Minuartia, Silene, Alyssum and Thlaspi. Plant Biol. 1995, 37, 411–416. [Google Scholar] [CrossRef]
  32. Ke, W.; Xiong, Z.; Xie, M.; Luo, Q. Accumulation, subcellular localization and ecophysiological responses to copper stress in two Daucus carota L. populations. Plant Soil 2007, 292, 291–304. [Google Scholar] [CrossRef]
  33. Mittler, R.; Vanderauwera, S.; Gollery, M.; Van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004, 9, 490–498. [Google Scholar] [CrossRef]
  34. Almeida, J.M.; Fidalgo, F.; Confraria, A.; Santos, A.; Pires, H.; Santos, I. Effect of hydrogen peroxide on catalase gene expression, isoform activities and levels in leaves of potato sprayed with homobrassinolide and ultrastructural changes in mesophyll cells. Funct. Plant Biol. 2005, 32, 707–720. [Google Scholar] [CrossRef]
  35. Nurnaeimah, N.; Mat, N.; Mohd, K.S.; Badaluddin, N.A.; Yusoff, N.; Sajili, M.H.; Mahmud, K.; Adnan, A.F.M.; Khandaker, M.M. The Effects of Hydrogen Peroxide on Plant Growth, Mineral Accumulation, as Well as Biological and Chemical Properties of Ficus deltoidei. Agronomy 2020, 10, 599. [Google Scholar] [CrossRef] [Green Version]
  36. Seleiman, M.F.; Abdel-Aal, S.M.; Ibrahim, M.E.; Monneveux, P. Variation of yield and milling, technological and rheological characteristics in some Egyptian bread wheat (Triticum aestivum L.) cultivars. Emir. J. Food Agric. 2010, 22, 84–90. [Google Scholar] [CrossRef]
  37. Seleiman, M.; Abdel-Aal, M. Response of growth, productivity and quality of some Egyptian wheat cultivars to different irrigation regimes. Egypt. J. Agron. 2018, 40, 313–330. [Google Scholar] [CrossRef]
  38. Al-Ashkar, I.; Alderfasi, A.; El-Hendawy, S.; Al-Suhaibani, N.; El-Kafafi, S.; Seleiman, M.F. Detecting salt tolerance in doubled haploid wheat lines. Agronomy 2019, 9, 211. [Google Scholar] [CrossRef] [Green Version]
  39. Ding, Z.; Ali, E.F.; Elmahdy, A.M.; Ragab, K.; Seleiman, M.F.; Kheir, A.M.S. Modeling the combined impacts of deficit irrigation, rising temperature and compost application on wheat yield and water productivity. Agric. Water Manag. 2021, 244, 106626. [Google Scholar] [CrossRef]
  40. Ding, Z.; Kheir, A.S.; Ali, O.A.; Hafez, E.; Elshamey, E.A.; Zhou, Z.; Wang, B.; Lin, X.; Ge, Y.; Fahmy, A.E.; et al. A vermicompost and deep tillage system to improve saline-sodic soil quality and wheat productivity. J. Environ. Manag. 2021, 277, 111388. [Google Scholar] [CrossRef]
  41. Yan, H.; Harrison, M.T.; Liu, K.; Wang, B.; Feng, P.; Fahad, S.; Meinke, H.; Yang, R.; Liu, D.L.; Archontoulis, S.; et al. Crop traits enabling yield gains under more frequent extreme climatic events. Sci. Total Environ. 2022, 808, 152170. [Google Scholar] [CrossRef] [PubMed]
  42. Shahpari, S.; Allison, J.; Harrison, M.T.; Stanley, R. An integrated economic, environmental and social approach to agricultural land-use planning. Land 2021, 10, 364. [Google Scholar] [CrossRef]
  43. FAOSTAT. 2020. Available online: http://www.fao.org/faostat/en/#data/QC (accessed on 20 February 2023).
  44. Chaves, M.S.; Martinelli, J.A.; Wesp-Guterres, C.; Graichen, F.A.S.; Brammer, S.P.; Scagliusi, S.M.; da Silva, P.R.; Wiethölter, P.; Torres, G.A.M.; Lau, E.Y.; et al. The importance for food security of maintaining rust resistance in wheat. Food Secur. 2013, 5, 157–176. [Google Scholar] [CrossRef] [Green Version]
  45. Chenu, K.; Porter, J.R.; Martre, P.; Basso, B.; Chapman, S.C.; Ewert, F.; Bindi, M.; Asseng, S. Contribution of crop models to adaptation in wheat. Trends Plant Sci. 2017, 22, 472–490. [Google Scholar] [CrossRef]
  46. Niu, L.; Liao, W. Hydrogen peroxide signaling in plant development and abiotic responses: Crosstalk with nitric oxide and calcium. Front. Plant Sci. 2016, 7, 230. [Google Scholar] [CrossRef] [Green Version]
  47. Bagheri, M.; Gholami, M.; Baninasab, B. Hydrogen peroxide-induced salt tolerance in relation to antioxidant systems in pistachio seedlings. Sci. Hortic. 2019, 243, 207–213. [Google Scholar] [CrossRef]
  48. Andrade, C.A.; de Souza, K.R.; de Oliveira Santos, M.; da Silva, D.M.; Alves, J.D. Hydrogen peroxide promotes the tolerance of soybeans to waterlogging. Sci. Hortic. 2018, 232, 40–45. [Google Scholar] [CrossRef]
  49. Wu, D.; Chu, H.Y.; Jia, L.X.; Chen, K.M.; Zhao, L.Q. A feedback inhibition between nitric oxide and hydrogen peroxide in the heat shock pathway in arabidopsis seedlings. Plant Growth Regul. 2015, 75, 503–509. [Google Scholar] [CrossRef]
  50. Chen, Y.; Guerschman, J.; Shendryk, Y.; Henry, D.; Harrison, M.T. Estimating pasture biomass using sentinel-2 imagery and machine learning. Remote Sens. 2021, 13, 603. [Google Scholar] [CrossRef]
  51. Sándor, R.; Ehrhardt, F.; Grace, P.; Recous, S.; Smith, P.; Snow, V.; Soussana, J.F.; Basso, B.; Bhatia, A.; Brilli, L.; et al. Ensemble modelling of carbon fluxes in grasslands and croplands. Field Crops Res. 2020, 252, 107791. [Google Scholar] [CrossRef]
  52. Taylor, C.A.; Harrison, M.T.; Telfer, M.; Eckard, R. Modelled greenhouse gas emissions from beef cattle grazing irrigated leucaena in northern Australia. Anim. Prod. Sci. 2016, 56, 594–604. [Google Scholar] [CrossRef]
  53. Nazir, F.; Hussain, A.; Fariduddin, Q. Hydrogen peroxide modulate hotosynthesis and antioxidant systems in tomato (Solanum lycopersicum L.) plants under copper stress. Chemosphere 2019, 230, 544–558. [Google Scholar] [CrossRef]
  54. Cruz, F.J.R.; da Cruz Ferreira, R.L.; Conceição, S.S.; Lima, E.U.; de Oliveira Neto, C.F.; Galvão, J.R.; da Cunha Lopes, S.; Viegas, I.D.J.M. Copper toxicity in plants: Nutritional, physiological, and biochemical aspects. In Advances in Plant Defense Mechanisms; IntechOpen: London, UK, 2022. [Google Scholar]
  55. Hossain, M.S.; Abdelrahman, M.; Tran, C.D.; Nguyen, K.H.; Chu, H.D.; Watanabe, Y.; Hasanuzzaman, M.; Mohsin, S.M.; Fujita, M.; Tran, L.S.P. Insights into acetate-mediated copper homeostasis and antioxidant defense in lentil under excessive copper stress. Environ. Pollut. 2020, 258, 113544. [Google Scholar] [CrossRef]
  56. Yuan, M.; Li, X.; Xiao, J.; Wang, S. Molecular and functional analyses of COPT/Ctr-type copper transporter-like gene family in rice. BMC Plant Biol. 2011, 11, 69. [Google Scholar] [CrossRef] [Green Version]
  57. Marques, D.M.; Veroneze Júnior, V.; da Silva, A.B.; Mantovani, J.R.; Magalhães, P.C.; de Souza, T.C. Copper toxicity on photosynthetic responses and root morphology of Hymenaea courbaril L. (Caesalpinioideae). Water Air Soil Pollut. 2018, 229, 138. [Google Scholar] [CrossRef] [Green Version]
  58. Feigl, G.; Kumar, D.; Lehotai, N.; Tugyi, N.; Molnár, Á.; Ördög, A.; Szepesi, Á.; Gémes, K.; Laskay, G.; Erdei, L.; et al. Physiological and morphological responses of the root system of Indian mustard (Brassica juncea L. Czern.) and rapeseed (Brassica napus L.) to copper stress. Ecotoxicol. Environ. Saf. 2013, 94, 179–189. [Google Scholar] [CrossRef] [Green Version]
  59. Mocquot, B.; Vangronsveld, J.; Clijsters, H.; Mench, M. Copper toxicity in young maize (Zea mays L.) plants: Effects on growth, mineral and chlorophyll contents, and enzyme activities. Plant Soil 1998, 182, 287–300. [Google Scholar] [CrossRef]
  60. Chatterjee, J.; Chatterjee, C. Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ. Pollut. 2000, 109, 69–74. [Google Scholar] [CrossRef]
  61. Shahbaz, M.; Tseng, M.H.; Stuiver, C.E.E.; Koralewska, A.; Posthumus, F.S.; Venema, J.H.; Parmar, S.; Schat, H.; Hawkesford, M.J.; De Kok, L.J. Copper exposure interferes with the regulation of the uptake, distribution and metabolism of sulfate in Chinese cabbage. J. Plant Physiol. 2010, 167, 438–446. [Google Scholar] [CrossRef]
  62. Ali, S.; Shahbaz, M.; Shahzad, A.N.; Khan, H.A.A.; Anees, M.; Haider, M.S.; Fatima, A. Impact of copper toxicity on stone-head cabbage (Brassica oleracea var. capitata) in hydroponics. PeerJ 2015, 3, 1119. [Google Scholar] [CrossRef] [Green Version]
  63. Zengin, F.K.; Kirbag, S. Effects of copper on chlorophyll, proline, protein and abscisic acid level of sunflower (Helianthus annuus L.) seedlings. J. Environ. Biol. 2007, 28, 561. [Google Scholar] [PubMed]
  64. Zlobin, I.E.; Kholodova, V.P.; Rakhmankulova, Z.F.; Kuznetsov, V.V. Brassica napus responses to short-term excessive copper treatment with decrease of photosynthetic pigments, differential expression of heavy metal homeostasis genes including activation of gene NRAMP4 involved in photosystem II stabilization. Photosynth. Res. 2015, 125, 141–150. [Google Scholar] [CrossRef] [PubMed]
  65. Rozentsvet, O.A.; Nesterov, V.N.; Sinyutina, N.F. The effect of copper ions on the lipid composition of subcellular membranes in Hydrilla verticillata. Chemosphere 2012, 89, 108–113. [Google Scholar] [CrossRef] [PubMed]
  66. Rehman, M.; Liu, L.; Wang, Q.; Saleem, M.H.; Bashir, S.; Ullah, S.; Peng, D. Copper environmental toxicology, recent advances, and future outlook: A review. Environ. Sci. Pollut. Res. 2019, 26, 18003–18016. [Google Scholar] [CrossRef] [PubMed]
  67. Xu, Q.; Qiu, H.; Chu, W.; Fu, Y.; Cai, S.; Min, H.; Sha, S. Copper ultrastructural localization, subcellular distribution, and phytotoxicity in Hydrilla verticillata (Lf) Royle. Environ. Sci. Pollut. Res. 2013, 20, 8672–8679. [Google Scholar] [CrossRef] [PubMed]
  68. Panou-Filotheou, H.; Bosabalidis, A.M.; Karataglis, S. Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum). Ann. Bot. 2001, 88, 207–214. [Google Scholar] [CrossRef] [Green Version]
  69. Feigl, G.; Kumar, D.; Lehotai, N.; Pető, A.; Molnár, Á.; Rácz, É.; Ördög, A.; Erdei, L.; Kolbert, Z.; Laskay, G. Comparing the effects of excess copper in the leaves of Brassica juncea (L. Czern) and Brassica napus (L.) seedlings: Growth inhibition, oxidative stress and photosynthetic damage. Acta Biol. Hung. 2015, 66, 205–221. [Google Scholar] [CrossRef] [Green Version]
  70. Aly, A.A.; Mohamed, A.A. The impact of copper ion on growth, thiol compounds and lipid peroxidation in two maize cultivars (‘Zea mays’ L.) grown‘in vitro’. Aust. J. Crop Sci. 2012, 6, 541–549. [Google Scholar]
  71. Ambrosini, V.G.; Rosa, D.J.; Basso, A.; Borghezan, M.; Pescador, R.; Miotto, A.; Melo, G.W.B.D.; Soares, C.R.F.D.S.; Comin, J.J.; Brunetto, G. Liming as an ameliorator of copper toxicity in black oat (Avena strigosa Schreb.). J. Plant Nutr. 2017, 40, 404–416. [Google Scholar] [CrossRef]
  72. Ke, W.; Xiong, Z.T.; Chen, S.; Chen, J. Effects of copper and mineral nutrition on growth, copper accumulation and mineral element uptake in two Rumex japonicus populations from a copper mine and an uncontaminated field sites. Environ. Exp. Bot. 2007, 59, 59–67. [Google Scholar] [CrossRef]
  73. Cambrollé, J.; García, J.L.; Figueroa, M.E.; Cantos, M. Evaluating wild grapevine tolerance to copper toxicity. Chemosphere 2015, 120, 171–178. [Google Scholar] [CrossRef] [Green Version]
  74. Wang, L.; Yang, L.; Yang, F.; Li, X.; Song, Y.; Wang, X.; Hu, X. Involvements of H2O2 and metallothionein in NO-mediated tomato tolerance to copper toxicity. J. Plant Physiol. 2010, 167, 1298–1306. [Google Scholar] [CrossRef]
  75. Zhang, H.; Lv, S.; Xu, H.; Hou, D.; Li, Y.; Wang, F. H₂O₂ is involved in the metallothionein-mediated rice tolerance to copper and cadmium toxicity. Int. J. Mol. Sci. 2017, 18, 2083. [Google Scholar] [CrossRef] [Green Version]
  76. Chen, B.T.; Avshalumov, M.V.; Rice, M.E. H2O2 is a novel, endogenous modulator of synaptic dopamine release. J. Neurophysiol. 2001, 85, 2468–2476. [Google Scholar] [CrossRef] [Green Version]
  77. Barba-Espín, G.; Diaz-Vivancos, P.; Job, D.; Belghazi, M.; Job, C.; Hernández, J.A. Understanding the role of H2O2 during pea seed germination: A combined proteomic and hormone profiling approach. Plant Cell Environ. 2011, 34, 1907–1919. [Google Scholar] [CrossRef]
  78. Ma, F.; Wang, L.; Li, J.; Samma, M.K.; Xie, Y.; Wang, R.; Wang, J.; Zhang, J.; Shen, W. Interaction between HY1 and H2O2 in auxin-induced lateral root formation in Arabidopsis. Plant Mol. Biol. 2014, 85, 49–61. [Google Scholar] [CrossRef]
  79. Ge, X.M.; Cai, H.L.; Lei, X.; Zou, X.; Yue, M.; He, J.M. Heterotrimeric G protein mediates ethylene-induced stomatal closure via hydrogen peroxide synthesis in Arabidopsis. Plant J. 2015, 82, 138–150. [Google Scholar] [CrossRef]
  80. Ashfaque, F.; Khan, M.I.; Khan, N.A. Exogenously applied H2O2 promotes proline accumulation., water relations., photosynthetic efficiency and growth of wheat (Triticum aestivum L.) under salt stress. Annu. Res. Rev. Biol. 2014, 4, 105–120. [Google Scholar] [CrossRef]
  81. Nazir, F.; Fariduddin, Q.; Khan, T. Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere 2020, 252, 126486. [Google Scholar] [CrossRef]
  82. Ellouzi, H.; Sghayar, S.; Abdelly, C. H2O2 seed priming improves tolerance to salinity; drought and their combined effect more than mannitol in Cakile maritima when compared to Eutrema salsugineum. J. Plant Physiol. 2017, 210, 38–50. [Google Scholar] [CrossRef]
  83. Xiong, J.; Yang, Y.; Fu, G.; Tao, L. Novel roles of hydrogen peroxide (H2O2) in regulating pectin synthesis and demethylesterification in the cell wall of rice (Oryza sativa) root tips. New Phytol. 2015, 206, 118–126. [Google Scholar] [CrossRef] [PubMed]
  84. Hameed, A.M.; Farooq, S.H.; Iqbal, N.A.; Arshad, R.U. Influence of exogenous application of hydrogen peroxide on root and seedling growth on wheat (Triticum aestivum L.). Int. J. Agric. Biol. 2004, 6, 366–369. [Google Scholar]
  85. Sairam, R.K.; Srivastava, G.C. Induction of oxidative stress and antioxidant activity by hydrogen peroxide treatment in tolerant and susceptible wheat genotypes. Biol. Plant. 2000, 43, 381–386. [Google Scholar] [CrossRef]
  86. Khan, M.I.; Khan, N.A.; Masood, A.; Per, T.S.; Asgher, M. Hydrogen peroxide alleviates nickel- inhibited photosynthetic responses through increase in useefficiency of nitrogen and sulfur, and glutathione production in mustard. Front. Plant Sci. 2016, 7, 44. [Google Scholar] [CrossRef] [Green Version]
  87. Kumari, S.; Verma, V.K. Hydrogen peroxide mediates suberization, root thickness and stomatal movement in wheats. Int. J. Curr. Microbiol. Appl. Sci. 2019, 8, 2448–2454. [Google Scholar] [CrossRef]
  88. An, Y.; Feng, X.; Liu, L.; Xiong, L.; Wang, L. ALA-induced flavonols accumulation in guard cells is involved in scavenging H2O2 and inhibiting stomatal closure in Arabidopsis cotyledons. Front. Plant Sci. 2016, 7, 1713. [Google Scholar] [CrossRef] [Green Version]
  89. Fariduddin, Q.; Khan, T.A.; Yusuf, M. Hydrogen peroxide mediated tolerance to copper stress in the presence of 28-homobrassinolide in Vigna radiata. Acta Physiol. Plant. 2014, 36, 2767–2778. [Google Scholar] [CrossRef]
  90. Guzel, S.; Terzi, R. Exogenous hydrogen peroxide increases dry matter production., mineral content and level of osmotic solutes in young maize leaves and alleviates deleterious effects of copper stress. Bot. Stud. 2013, 54, 26. [Google Scholar] [CrossRef] [Green Version]
  91. Hasan, S.A.; Irfan, M.; Masrahi, Y.S.; Khalaf, M.A.; Hayat, S. Growth, photosynthesis, and antioxidant responses of Vigna unguiculata L. treated with hydrogen peroxide. Cogent Food Agric. 2016, 2, 1155331. [Google Scholar] [CrossRef]
Agriculture 13 00862 g001 550
Figure 1. Effect of hydrogen peroxide on plant height at 45, 60, 75, and 100 days after sowing (DAS) of wheat grown in copper contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 1. Effect of hydrogen peroxide on plant height at 45, 60, 75, and 100 days after sowing (DAS) of wheat grown in copper contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Agriculture 13 00862 g002 550
Figure 2. Effects of hydrogen peroxide on leaf area per plant at 45, 60, 75, and 100 DAS of wheat grown in copper contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 2. Effects of hydrogen peroxide on leaf area per plant at 45, 60, 75, and 100 DAS of wheat grown in copper contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Figure 3. Effect of hydrogen peroxide on whole dry weight per plant at 45, 60, 75, and 100 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 3. Effect of hydrogen peroxide on whole dry weight per plant at 45, 60, 75, and 100 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Figure 4. Effect of hydrogen peroxide on total chlorophyll content (SPAD) at 42, 57, 72, and 97 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 4. Effect of hydrogen peroxide on total chlorophyll content (SPAD) at 42, 57, 72, and 97 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Figure 5. Effect of hydrogen peroxide on net photosynthesis at 42, 57, 72, and 97 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 5. Effect of hydrogen peroxide on net photosynthesis at 42, 57, 72, and 97 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Figure 6. Effect of hydrogen peroxide on stomatal conductance at 42, 57, 72, and 97 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 6. Effect of hydrogen peroxide on stomatal conductance at 42, 57, 72, and 97 DAS of wheat grown in contaminated sandy soil. Means followed by the same letter at each sampling date are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Figure 7. Effect of hydrogen peroxide on growth traits of wheat grown in contaminated sandy soil. Means followed by the same letter in each parameter are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 7. Effect of hydrogen peroxide on growth traits of wheat grown in contaminated sandy soil. Means followed by the same letter in each parameter are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Figure 8. Effect of hydrogen peroxide on yield traits of wheat grown in contaminated sandy soil. Means followed by the same letter in each parameter are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 8. Effect of hydrogen peroxide on yield traits of wheat grown in contaminated sandy soil. Means followed by the same letter in each parameter are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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Figure 9. Effect of hydrogen peroxide on elemental analysis of whole wheat plants grown in contaminated sandy soil. Means followed by the same letter in each parameter are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
Figure 9. Effect of hydrogen peroxide on elemental analysis of whole wheat plants grown in contaminated sandy soil. Means followed by the same letter in each parameter are not significantly different according to the least significant differences (LSD) test (p ≤ 0.05). Error bars are ± Standard Error (SE).
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MDPI and ACS Style

Alhammad, B.A.; Seleiman, M.F.; Harrison, M.T. Hydrogen Peroxide Mitigates Cu Stress in Wheat. Agriculture 2023, 13, 862. https://doi.org/10.3390/agriculture13040862

AMA Style

Alhammad BA, Seleiman MF, Harrison MT. Hydrogen Peroxide Mitigates Cu Stress in Wheat. Agriculture. 2023; 13(4):862. https://doi.org/10.3390/agriculture13040862

Chicago/Turabian Style

Alhammad, Bushra Ahmed, Mahmoud F. Seleiman, and Matthew Tom Harrison. 2023. "Hydrogen Peroxide Mitigates Cu Stress in Wheat" Agriculture 13, no. 4: 862. https://doi.org/10.3390/agriculture13040862

APA Style

Alhammad, B. A., Seleiman, M. F., & Harrison, M. T. (2023). Hydrogen Peroxide Mitigates Cu Stress in Wheat. Agriculture, 13(4), 862. https://doi.org/10.3390/agriculture13040862

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