Next Article in Journal
The Essential Oil Composition in Commercial Samples of Verbena officinalis L. Herb from Different Origins
Previous Article in Journal
The Impact of Biostimulants on the Yield and Quality Attributes of Essential Oil from Different Basil Varieties
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Crops
Volume 5
Issue 2
10.3390/crops5020015
crops-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Physio-Biochemical Responses and Cadmium Partitioning Associated with Stress Tolerance in Hulless Barley Genotypes

by
Said Bouhraoua
1,
Mohamed Ferioun
1,2,*,
Abdelali Boussakouran
1,
Douae Belahcen
1,
Taoufiq Benali
3,
Naoufal El Hachlafi
4,
Mohamed Akhazzane
5,
Abdelmajid Khabbach
6,
Khalil Hammani
1 and
Said Louahlia
1,6
1
Natural Resources and Environment Laboratory, Polydiciplinary Faculty of Taza, Sidi Mohamed Ben Abdellah University, Fez 30000, Morocco
2
Microbial Biotechnology and Bioactive Molecules Laboratory, Sciences and Technology Faculty, Sidi Mohamed Ben Abdellah University, Fez 30000, Morocco
3
Laboratory of Ecotoxicology, Bioresources, and Coastal Geomorphology, Polydisciplinary Faculty of Safi, Cadi Ayyad University, P.O. Box 4162, Safi 46000, Morocco
4
Faculty of Medicine and Pharmacy, Ibn Zohr University, Guelmim 81000, Morocco
5
Engineering Laboratory of Organometallic and Molecular Materials and Environment, Faculty of Sciences Dhar El Mahraz, Sidi Mohamed Ben Abdellah University, Fez 30000, Morocco
6
Biotechnology, Environment, Agri-Food and Health Laboratory, Faculty of Sciences Dhar el Mahraz, Sidi Mohamed Ben Abdellah University, Fez 30000, Morocco
*
Author to whom correspondence should be addressed.
Crops 2025, 5(2), 15; https://doi.org/10.3390/crops5020015
Submission received: 2 February 2025 / Revised: 13 March 2025 / Accepted: 27 March 2025 / Published: 1 April 2025
Browse Figures
Versions Notes

Abstract

:
Among heavy metals, cadmium (Cd) is shown to have adverse consequences for plants. Due to its harmful nature and ability to move through the soil–plant system, it is a very worrying element for soil experts and plant physiologists. In this work, we designed a pot experiment to study the influence of three soil concentrations of cadmium (0, 15, and 30 mg/kg) to explore its physiological impacts, and its portioning in the whole plant of three hulless barley varieties. Our findings demonstrated marked Cd accumulation in roots, leaves, and stems under severe Cd stress (30 mg/kg). Cd stress was also shown to reduce photosynthetic activity, chlorophyll fluorescence (Fv/Fm), and transpiration rates (E). The application of Cd in the soil increased the activities of catalase (CAT), ascorbate peroxidase (APX), and guaiacol peroxidase (POD) enzymes, as well as the levels of oxidative stress markers such as malondialdehyde (MDA), hydrogen peroxide (H2O2), and proline. These results reflect the negative effects of cadmium on morpho-physiological traits in barley genotypes. However, the principal component analysis indicated a significant correlation between oxidative stress indicators and enzymatic activities, along with different levels of Cd tolerance between Tombari, Assiya, and Giza 130 genotypes. When exposed to Cd, these varieties shifted a significant amount of energy from growth to produce antioxidant compounds and osmolytes. Despite this, these defenses did not effectively shield the plant from the detrimental effects of oxidative stress induced by Cd accumulation at vegetative stages. Consequently, we highly recommend testing these varieties under Cd-contaminated soil to investigate the rate of cadmium accumulation in the seeds, the harvested part used in human nutrition.

1. Introduction

Since the initiation of the industrial revolution in the latter part of the 19th century, there has been a systematic amplification of the ecological consequences stemming from industrial and agricultural activities [1]. During this time, there was a significant change in how human activities impacted the environment, particularly those associated with industry and agriculture. The pedosphere and hydrosphere have long been considered regeneratively infinite reservoirs capable of absorbing human waste without severely damaging ecosystems, as asserted by Borjac et al. [2]. The increase in the concentration and bioavailability of Cd in the environment is mainly attributed to anthropogenic activities, such as industrialization, urbanization, excessive use of contaminated fertilizers in agriculture, as well as mining and refining practices [3,4]. Studies have demonstrated that Cd can accumulate in the human body through various pathways, with the consumption of contaminated food being the most significant [5]. This contaminant is consistently being discharged into the environment and may be associated with the incidence of major human illnesses [6]. Among these challenges, toxic metals contamination in soil has been identified as one of the world’s most serious environmental issues [7]. Soil heavy metal contamination has been identified as one of the world’s most serious issues in agricultural soils globally, leading to increased scientific interest in how plants absorb these metals and their effects on food quality and security [8,9].
Agricultural soils may naturally contain heavy metals, although these are in small amounts and do not pose a threat regarding the transmission of these contaminants to edible plants. However, increased levels of toxic metals in nature and the pollution of agricultural land are mostly caused by human activities [10]. One of the most highly polluting metals, cadmium, is mostly introduced to agricultural soil through uncontrolled (nonconventional) amendments, the irrigation of reclaimed wastewater, and the vicinity of farms to mines that are either exploited or not [11].
Cadmium is not an essential mineral for plants. When its threshold levels are exceeded, the high concentration of Cd causes development abnormalities and cell metabolism disruptions in some crops [12,13]. Indeed, Cd exposure inhibits the extension of plant shoots and root systems, which enhances leaf peeling and bleaching [14]. The distribution and movement of nutritional components in plants can be impacted by Cd ions in the soil, which can also have an impact on root absorption [15]. It is well known that cadmium significantly inhibits photosynthesis [16]. It has been found that Cd accumulation in leaves of oilseed, legume, and cereal crops decreases stomatal opening, and a clear association between transpiration and photosynthetic suppression was noted [13,17]. High cadmium levels in plants affect the photosynthetic apparatus, especially the intricate light-harvesting photosystems I and II, and decrease photoactivation of photosystem II (PSII) by electron transmission inhibition [18,19]. Trace metals can stress plants directly or indirectly by causing reactive oxygen species (ROS) to be produced [20,21,22]. In fact, via disrupting the electron transport chain, Cd may indirectly contribute to the production of reactive oxygen species (ROS) in mitochondria and chloroplasts [23,24].
In the Mediterranean basin countries, barley species stands out as the primary cultivated crop, covering approximately 20 million hectares [25,26,27]. In North African countries (Morocco, Algeria, Tunisia, Libya, and Egypt), barley is the second most important cultivated crop after wheat, with 3.8 million hectares [28]. Barley (Hordeum vulgare L.) is the fourth most cultivated cereal crop globally, following wheat (Triticum aestivum L.), rice (Oryza sativa L.), and maize (Zea mays L.) [29]. In 2013, 30 million tons of barley were produced throughout European and African nations within the area of the Mediterranean region [30]. Indeed, this species shows substantial promise for a large capacity for biomass (straw), which could be used as useful feed [31]. Crop cultivation requires the use of mineral fertilizers such as nitrogen (N), potassium (K), and phosphate (P). Morocco is known as the world’s biggest producer of phosphate, with 32.8 million tons produced in 2017 [32]. Water, air, plants, and soils can become contaminated due to the phosphate industry’s emissions, which are high in trace metals including cadmium, zinc, and chromium [33]. Furthermore, previous studies have pointed out that mineral phosphate fertilizer is a significant source of Cd in agricultural soils [34]. In Morocco, barley is usually cultivated for human food and livestock purposes in regions which are characterized by a notably high concentration of Cd in the soils, primarily attributed to this excessive use of fertilizers [35]. Barley is an adaptable crop that can thrive in adverse conditions, promoting typically constant yields with little labor [36]. This cereal is considered as tolerant to abiotic stress, a crucial genetic diversity that facilitates its potential cultivation under various environmental and soil conditions [37,38,39]. Barley’s high content of fibers, vitamins, and minerals resulted in greater interest in the consumption of this cereal [40,41,42].
Studies have explored cadmium (Cd) uptake, distribution, and detoxification in plants, yet the specific mechanisms involved in these processes differ depending on species, varieties, and levels of environmental stress. Notably, few studies have thoroughly examined the biochemical mechanisms involved in cadmium (Cd) partitioning across different plant organs, particularly in phytoremediation. This study addresses this gap by investigating the effects of Cd exposure on various cultivated barley genotypes to identify Cd-safe genotypes with potential for phytoremediation applications. These genotypes are expected to effectively limit Cd translocation from roots to shoots and grains, thereby reducing Cd contamination in edible parts. Specifically, the research focuses on three hulless barley genotypes: Assiya (from Morocco), Giza130 (from Egypt), and Tombari (from Tunisia). These genotypes were subjected to three cadmium concentrations (0, 15, and 30 mg/kg) to evaluate their morphological, physiological, and biochemical responses, with particular emphasis on Cd accumulation, translocation, and their phytoremediation potential.

2. Materials and Methods

2.1. Plant Material, Growing Conditions, Treatment, and Sampling

The research study used three Hulless barley different types: Assiya from Morocco, Giza-130 from Egypt, and Tombari from Tunisia. The grain seeds were graciously donated by the National Institute of Agricultural Research in Morocco, The National Gene Bank in Tunisia and the National Research Centre in Egypt. Table 1 shows the hulless barley uses and their origins. An experiment in a greenhouse was performed to examine reactions to Cd toxicity and accumulation. Seeds were sown in plastic pots (5 kg soil) filled with non-contaminated (control) and soil artificially mixed with 15 and 30 mg/kg Cd, respectively. To achieve Cd concentrations of 15 to 30 mg/kg during the swelling stage, sufficient amounts of CdCl2 were measured, combined with water, and sprayed onto the soil. After that, the mixture was saturated with distilled water three times, and the paw was well mixed three times daily. After being allowed to dry outside, the soil was carefully remixed and divided among the 5 kg pots. Before planting, we ensured no discernible difference in the soil’s Cd content of 15–30 mg/kg. The planting density was nine seeds per pot, and five plants were preserved for further analysis. The pots were placed in a randomized organization, with three replicates of each genotype. Each pot (the control and two levels of Cd-supplemented soils) was irrigated with tap water to keep soil moisture at 80% of the maximum field capacity. At the stage of reproduction, formed and mature flag leaves were collected for a study of morphological traits, chlorophyll parameters, oxidative damage caused by reactive oxygen species, and antioxidant enzyme activity. Samples of flag leaves were promptly refrigerated at −20 °C till examination. Additionally, samples of leaves, stems, and roots were collected and dehydrated in order to evaluate the accumulation of Cd.

2.2. Morphological Measurements

Using a portable leaf area meter (AM-350, ADC Bioscientific Ltd., Hoddesdon, England), the shoot height (cm) and flag leaf area (per plant) were calculated. The samples were dried for 24 h at 70 °C and were used to calculate the root and shoot dry weight (RDW and SDW) [43].

2.3. Determination of Cd Accumulation Using ICP-AES

The total Cd content of all barley plant samples was measured using the Inductive Coupled Plasma Atomic Emission Spectrometer (ICP-AES). All samples were dried at 70 degrees Celsius for 24 h. Dried samples were immersed in concentrated HNO3 overnight. The sample mass of 100 mg was digested by heating at 250 °C for 6 h. After cooling, the digested solution was diluted with deionized water and filtered using 0.22 μm cellulose acetate membrane filters. All digestions were performed in triplicate. The blank diluted HNO3 served as the negative control. All tests were performed in triplicate.

2.4. Estimation of Fag Leaf Relative Water Content

The technique described by Ogbaga et al. [44] was used to calculate the relative water content (RWC) of flag leaf. To determine the relative water content of the flag leaf (RWC), the leaves of three different plants were used in each duplicate. From every plant, three leaf disks of ten millimeters in diameter were selected at random. The fresh weight (FW) of the standard disks was instantly determined. The weighted leaf disks were submerged in distilled water for 24 h at 20 °C. To measure water uptake, the turgid mass (TW) of transferring leaf disks was measured. The dry mass (DW) of the leaf disks was determined by drying at 70 °C for 48 h. The RWC was calculated as follows:
RWC = (FW − DW) × 100/(TW − DW).

2.5. Flag Leaf Photosynthetic Parameters and Transpiration Measurement

The physiological parameters of transpiration rate (E), chlorophyll fluorescence (Fv/Fm), and chlorophyll content (SPAD index) were measured on three flag leaves that were chosen from the pot. Every measurement was taken on a flag leaf that was fully exposed to the sun at midday. The transpiration rate (E) was calculated using an ADC Bioscientific portable infrared gas analyzer (LCi-SD, ADC Bioscientific Ltd., Hoddesdon, UK). A chlorophyll fluorometer (OS-30p, OptiScience, Hudson, NH, USA) was used to measure the amount of fluorescence in the green leaf. Using leaf clips, each flag leaf was first dark acclimated for at least twenty-five minutes. Following the application of a saturating actinic light pulse of 3.000 μmol m−2 s−1 for 0.8 s, the maximum fluorescence in the light (Fm) was then measured. The maximum quantum efficiency of photosystem II (Fv/Fm) and variable fluorescence (Fv = Fm − F0) were then calculated using F0 and Fm. The SPAD index was computed using the Konica Minolta SPAD 502 Plus portable SPAD meter (Konica Minolta, Tokyo, Japan).

2.6. Determination of Leaf Proline Content

Bates et al. [45] swift colorimetric approach was used to measure proline accumulation in fresh leaves. Grinding 0.25 g of fresh flag leaf tissue in 5 mL of 3% (v/v) sulphosalicylic acid was used to extract each sample. After that, the mixture was centrifuged for 15 min at 10,000× g. After adding two milliliters of the supernatant and two milliliters of freshly made ninhydrin (1.25 g of ninhydrin, forty milliliters of phosphoric acid, and sixty milliliters of glacial acetic acid) solution to a test tube, each tube was incubated in a water bath at 90 °C for 35 min. The reaction was terminated in an ice bath. The chromophore proline–ninhydrin was extracted with 3 mL of toluene and the tubes were placed in the dark for 10 min at room temperature to allow the toluene and aqueous phases to separate. The absorbance of the chromophore fraction was measured at 520 nm using toluene as reference.

2.7. Determination of Lipid Peroxidation, Hydrogen Peroxide (H2O2) Contents, and Enzymatic Activities in Leaves

The degree of lipid peroxidation in leaves was determined by measuring MDA content following the method of Stewart and Bewley [46]. Hydrogen peroxide (H2O2) in flag leaves was assessed spectrophotometrically according to method of Lipkin [47]. CAT activity was calculated using the method provided by Cakmak and Marschner. [48]. The activity of peroxidase (POD, EC1.11.1.7) in leaves was determined using the approach reported by Wu et al. [49], with modifications in some reactive products. The activity of ascorbate peroxidase (APX, EC 1.11.1.11) was determined using the Nakano and Asada method [50].

2.8. Statistical Analysis

The responses of the different genotypes, treatments, and their interactions were examined using an analysis of variance (ANOVA). The least significant difference (LSD) values were determined at a probability level of 0.05. The correlation coefficients for physio-biochemical characteristics were calculated using mean values. Stepwise regression analysis was used, with the mean flag leaf of each genotype acting as the dependent variable and morpho-physiological changes, and biochemical features as the independent variables. All statistical analyses were carried out independently for each treatment using the STATGRAPHICS Centurion XVII package (Stat Point Technologies, Warrenton, VA, USA).

3. Results

3.1. Data Variability

The analysis of variance (Table 2) indicates that all morphological, physiological, and biochemical characteristics of the three hulless North African barley genotypes tested are consistent with one another. The three distinct cadmium concentration levels significantly impacted these characteristics (with a significance level of p < 0.001). It has been demonstrated that the biochemical and physiological parameters under study were greatly altered by genotypes, treatment, and their combination. Treatment, however, was the primary cause of variability for every parameter examined, except FLA, RWC, and MDA contents (47, 43, and 38%, respectively). More than 80% of the RDW, stem length, transpiration, and SPAD index are affected by the treatment factor. Meanwhile, proline, SDW, Fv/Fm, H2O2, and APX activities are affected also by this factor more than 65%; whereas CAT is affected by it slightly more than 50%. The cultivar factor was the main source of variability for FLA, RWC, and MDA content, accounting for 51, 53, and 50% of total variability, respectively. Treatment by cultivar interaction, on the other hand, is a significant source of variability for H2O2, CAT, and APX parameters, accounting for roughly 18% of the total variability (Table 2).

3.2. Cadmium Effect on Plant Growth

The major growth parameters, such as shoot and root dry weights per plant, flag leaf area, and stem length were significantly reduced by both cadmium concentrations compared with those at control without cadmium in the soil. At 15 mg/kg of Cd, Tombari showed a significantly reduced stem length, flag leaf area, shoot and root dry weights by 33%, 18%, 10%, and 57%, and by 53%, 63%, 20%, and 66% at 30 mg/kg, respectively. However, Assiya and Giza130 were less affected under 15 mg/kg, compared to control plants, but elevated Cd concentrations induced a significant reduction in shoot and root dry weights (Figure 1a,b), stem length (Figure 1c), and flag leaf area (Figure 1d). Furthermore, each of the three genotypes’ assessed characteristics showed a significant difference when exposed to varying doses of Cd. Increases in Cd concentrations coincided with this decrease in plant growth, and this was more noticeable in Tombari than in Assiya and Giza 130 (Figure 1).
Crops 05 00015 g001
Figure 1. Means values of different morphological traits including root dry weight (a), shoot dry weight (b), stem length (c), and flag leaf area (d) of hulless barley varieties under different levels of cadmium concentrations. Values indicate the mean ± SD (n = 3).
Figure 1. Means values of different morphological traits including root dry weight (a), shoot dry weight (b), stem length (c), and flag leaf area (d) of hulless barley varieties under different levels of cadmium concentrations. Values indicate the mean ± SD (n = 3).
Crops 05 00015 g001
Table 2. Mean squares of the combined analyses of variance for various morphological, physiological, and biochemical parameters of three North African hulless barley varieties grown under exposure to three cadmium levels concentrations (0, 15, and 30 mg/kg) at the reproductive stage.
Table 2. Mean squares of the combined analyses of variance for various morphological, physiological, and biochemical parameters of three North African hulless barley varieties grown under exposure to three cadmium levels concentrations (0, 15, and 30 mg/kg) at the reproductive stage.
SourceDFRDWSDWStem LengthFLARWCESPADFv/FmProlineMDAH2O2CATAPXPOD
Variety (VAR)22.732 ***69.801 ***92.68 ***375.59 ***559.855 ***2.6842 ***15.134 ***0.0016 ***8.5164 ***176.80 ***5.9331 ***0.0136 ***1.536 ***180.236 ***
Treatment (TRT)211.48 ***162.21 ***582.49 ***350.85 ***449.832 ***27.920 ***199.57 ***0.00401 ***22.807 ***134.02 ***23.397 ***0.0329 ***9.233 ***399.568 ***
Replicates20.03251.6010.8230.3260.050.00930.420.000040.06490.030.06070.00020.01250.043
VAR*TRT40.037 ***7.312 ***21.997 ***13.24 ***41.898 ***1.2295 ***8.833 ***0.00044 ***4.0231 ***42.29 ***5.8488 ***0.0111 ***2.434 ***122.363 ***
Error160.0920.3941.9990.514.3060.13770.8190.0000540.13340.4840.04590.00020.03361.455
Total26
*** Significant at p < 0.001. RDW: Root dry weight. SDW: Shoot dry weight FLA: Flag leaf area. RWC: Relative water content. E: Transpiration. SPAD: Spad index. Fv/Fm: chlorophyll fluorescence. MDA: Malondialdehyde. H2O2: Hydrogen peroxide. CAT: Catalase activity. APX: Ascorbate peroxidase activity. POD: Guaiacol peroxidase.

3.3. Accumulation Levels of Cadmium in Roots, Stems, and Leaves

In the roots, at 15 mg/kg of Cd in the soil referred to as moderate stress the Cd concentrations in roots recorded lower levels, no more than 68, 64, and 58 μg/g DW was measured in the roots of Assiya, Giza130, and Tombari, respectively. In contrast, at 30 mg/kg of cadmium in the soil, thus under severe stress, the Assiya variety accumulated the highest Cd concentration, followed by Giza 130 and Tombari. Cd levels in the roots of Assiya, Giza 130, and Tombari were 154, 105, and 86 μg/g DW, respectively (Figure 2a).
Cd accumulated at lower quantities in stems than in roots, and there were major differences across genotypes. As in the roots, the maximum Cd amounts were seen under extreme stress conditions. The concentration of cadmium in the straw of Tunisian (Tombari), Moroccan (Assiya), and Egyptian (Giza 130) genotypes was 32, 23, and 19 μg/g DW at 15 mg/kg, respectively. Conversely, at a high concentration of Cd in the soil (30 mg/kg), the Giza130 and Assiya genotypes exhibited the lowest Cd concentrations in the straw, with roughly 33 μg/g DW. The Tombari genotype had the second-highest level of Cd accumulation, measuring 45 μg/g DW) (Figure 2b).
Under extreme stress, the amounts of Cd in leaves (Figure 2a) did not surpass 32 μg/g DW. These organs had the lowest concentration of Cd, while Tombari had the highest Cd content in its leaves in both treatments. At 15 mg/kg, the lowest concentration of Cd in leaves of 4 μg/g DW was found in Assiya, and 12 μg/g DW in Giza130, while the highest value of 24 μg/g DW was recorded in Tombari (Figure 2a). At 30 mg/kg of Cd in the medium, the leaves of Giza130 and Assiya contain 25 and 13 μg/g DW of Cd, respectively.

3.4. Cadmium Effects on SPAD Index, Chlorophyll Fluorescence and Transpiration

SPAD index and chlorophyll fluorescence (Fv/Fm) significantly and remarkably declined with the increase of cadmium levels in the rhizosphere (15 and 30 mg/kg) when compared to the control conditions (Figure 3c,d). The declines of the SPAD index, and chlorophyll fluorescence (Fv/Fm) were much more pronounced in Tombari in both cadmium treatments. In this variety, the SPAD index decreased by about 14% and 24% and chlorophyll fluorescence (Fv/Fm) by 3% and 8%, at 15 and 30 mg/kg, respectively. However, Assiya and Giza130 showed a static ratio at 15 mg/kg but a significant decline at 30 mg/kg of Cd, when compared to the control. At 15 and 30 mg/kg the values recorded in Assiya and Giza130 declined by 15% and 13% for the SPAD index and by 6% and 2% for chlorophyll fluorescence (Fv/Fm), respectively.
Under cadmium stress, the transpiration rate (E) exhibited differential decrease taking into consideration plant variety, and soil cadmium concentrations (Figure 3b). At 15 mg/kg of Cd in soil, the transpiration rates (E) were significantly decreased in Assiya and Giza130 by about 22 and 31%, respectively. When cadmium soil contamination increased to 30 mg/kg the transpiration rates in Assiya and Giza130 were more affected with drops of 59% and 45%, respectively. Meanwhile, Tombari showed a marked decrease in transpiration rate of 58% at 15 mg/kg and this was made worse at 30 mg/kg by a significant decrease of 81% when compared to control (Figure 3b).

3.5. Effects of Cadmium on Relative Water Content, Proline Content, and Oxidative Damage

Compared to control settings, leaf RWC (relative water content) exhibited a notable decline of approximately 10% in Assiya, 4% in Giza 130, and 15% in Tombari when treated with 15 mg/kg cadmium. At the higher concentration of 30 mg/kg cadmium, the reduction in leaf RWC increased to 19% in Assiya, 6% in Giza 130, and 21% in Tombari (Figure 3a). Regarding the impact of cadmium on proline content in leaves, the results in Figure 4a showed significant increases in all barley varieties. This was observed both at 15 and 30 mg/kg of cadmium. The cadmium effect on proline contents was larger in Assiya and Giza 130 than in Tombari. At 15 mg/kg, Tombari has registered an increase of 5% compared to Assiya and Giza 130 which recorded increases in proline contents of 31% and 50%, respectively. At severe stress conditions of 30 mg/kg, the Tombari genotype exhibited the lowest proline content (2.7 μmol g−1 FW) compared to Giza 130 and Assiya, which had 7 μmol g−1 FW and 6.3 μmol g−1 FW, respectively.
MDA and H2O2 contents sharply increased with the severity of cadmium stress (Figure 4b,c). At 15 mg/kg of Cd, in Tombari the hydrogen peroxide and MDA concentrations exhibited the highest values of 4.5 mg/g and 17 nM/g WF compared to Assiya with 3.3 mg/g and 12 nM/g WF and Giza130 with 2.8 mg/g and 8 nM/g WF, respectively. When the concentration of Cd in the medium increased to 30 mg/kg, Tombari had the highest increment of hydrogen peroxide and MDA. The contents of these metabolites increased by 81% and 63%, respectively, when compared to the control. In contrast, in Assiya and Giza130, the increases of H2O2 and MDA contents were less pronounced by 33 and 22% in Assiya and by 42% and 36% in Giza130, respectively.

3.6. Effect of Cadmium on the Activity of Antioxidant Enzymes

Without cadmium in the medium, differences were observed between the three varieties regarding the antioxidant enzymes activities (Figure 4d–f). Significant differences in the activity of antioxidant enzymes in the flag leaf of the three barley genotypes were observed when cadmium was applied at concentrations of 15 and 30 mg/kg. Significant high CAT and POD activities were recorded under both Cd treatments, while APX showed significant differences under the 30 mg/kg cadmium treatment compared to the control. In the three barley genotypes, the maximum POD and CAT activity levels were seen with a Cd treatment of 15 mg/kg. In contrast, a Cd dose of 30 mg/kg produced the maximal APX activity. The APX activity increased by 25% and 49% in Assiya and 9% and 20% in Giza 130 compared to the control. However, in Tombari, a lower increase was recorded, with 1% and 6% being under 15 and 30 mg/kg Cd stress compared to the control, respectively. Moreover, The Assiya and Giza130 genotypes exhibited increases in POD by approximately 25% and 36%, and in CAT by 16% and 26%, respectively. In contrast, the Tombari genotype showed no changes in POD activity or CAT levels under 15 and 30 mg/kg Cd exposure conditions, respectively.

3.7. Relationship Between the Studied Parameters

A correlation analysis was conducted to evaluate the relationship between the physico-biochemical traits of the flag leaf in three different hulless barley genotypes. Among the physical and biochemical traits analyzed, the strongest positive correlation was found between E and the SPAD index (r = 0.982 ***, p < 0.001), followed by the correlation between SDW and FLA (r = 0.934 ***, p < 0.001). Traits such as RDW exhibited the strongest positive correlation with all the photosynthetic parameters, including E (r = 0.958 ***), SPAD index (r = 0.945 ***, p < 0.001), and Fv/Fm (r = 0.879 **) (Table 3). However, certain traits exhibited a notably strong negative correlation, with the most significant being between H2O2 and the SPAD index (r = −0.911 ***, p < 0.001) and Fv/Fm (r = −0.909 ***, p < 0.001), followed by RWC and MDA (r = −0.869 **, p < 0.001). The flag leaf area exhibited a negative correlation with all the traits analyzed, except for photosynthetic traits and relative water content (RWC).

3.8. Principal Component Analysis (PCA)

To illustrate the combined impact of treatment and variety on physiological and biochemical traits, PCA was performed using the mean data values, as presented in Figure 5. The results indicated that the first two principal component axes explained approximately 87% of the overall variability, with 67% attributed to PC1 and 20% to PC2. The variation along PC1 was primarily attributed to ProC, Proteins, POD, APX, CAT, MDA, and H2O2, which were positioned on the left side, whereas yield per plant, RDW, SDW, LP, FLA, RWC, SPAD index, E, and Fv/Fm were found on the right side. PC2 separated H2O2 and MDA, which appeared in the negative direction, from all other parameters, which were positioned in the positive direction. Figure 5a illustrates the spatial distribution of various characteristics in relation to cadmium treatments. PC1 seems to have distinctly separated stressed Cd1 and Cd2 on its left side, showing significant scores for all biochemical traits. Meanwhile, the cluster for controlled genotypes appeared on the right side, where they had higher values for physiological traits. In Figure 5b, which illustrates the variability of different varieties, PC2 separates the Tombari variety, which is positioned in the negative direction with high MDA and H2O2 values, from the Assiya and Giza130 genotypes. The latter are primarily associated with RWC, the SPAD index, and various morphological and biochemical traits, positioning them towards the upper direction.
Table 3. Pearson’s correlation coefficient (r) for measured morphological, physiological, and biochemical characteristics of three North African hulless barley under control and cadmium treatment.
Table 3. Pearson’s correlation coefficient (r) for measured morphological, physiological, and biochemical characteristics of three North African hulless barley under control and cadmium treatment.
VariablesSDWStem LengthFLA RWCESPADProCMDAH2O2Fv/FmCATAPXPOD
RDW0.938 ***0.887 **0.926 ***0.843 **0.958 ***0.945 ***−0.466−0.751 *−0.803 **0.879 **−0.589−0.489−0.323
SDW 0.753 *0.934 ***0.696 *0.913 ***0.875 **−0.426−0.654−0.765 *0.797 **−0.315−0.374−0.188
LP 0.712 *0.752 *0.866 **0.890 **−0.530−0.792 **−0.835 **0.867 **−0.659−0.530−0.294
FLA 0.821 **0.842 **0.796 *−0.239−0.698−0.690 *0.796 **−0.381−0.254−0.072
RWC 0.819 **0.822 **−0.047−0.869 **−0.780 *0.907 ***−0.610−0.287−0.044
E 0.982 ***−0.465−0.755 *−0.8660.924 ***−0.555−0.539−0.308
SPAD −0.452−0.810−0.9110.911 ***−0.566−0.508−0.309
ProC −0.0470.183−0.2160.5800.848 **0.789 *
MDA 0.937−0.886 **0.3380.051−0.204
H2O2 −0.909 ***0.3210.231−0.061
Fv/Fm −0.522−0.402−0.044
CAT 0.789 *0.666 *
APX 0.771 *
* Significant at p < 0.05 probability level; ** Significant at p < 0.01 probability level; *** Significant at p < 0.001. RDW: Root dry weight. SDW: Shoot dry weight. FLA: Flag leaf area. RWC: Relative water content. E: Transpiration. SPAD: Spad index. ProC: Proline content. Fv/Fm: chlorophyll fluorescence. MDA: Malondialdehyde. H2O2: Hydrogen peroxide. CAT: Catalase activity. APX: Ascorbate peroxidase activity. POD: Guaiacol peroxidase.
Crops 05 00015 g005
Figure 5. Principal component analyses PCA plots showing the contribution of the morphological, physiological, and biochemical traits of the variation under control and cadmium stress conditions (15 and 30 mg·kg−1) and grouping of the three North African hulless barley genotypes according to F1 and F2 axes of traits and treatment (a) and genotypes (b).
Figure 5. Principal component analyses PCA plots showing the contribution of the morphological, physiological, and biochemical traits of the variation under control and cadmium stress conditions (15 and 30 mg·kg−1) and grouping of the three North African hulless barley genotypes according to F1 and F2 axes of traits and treatment (a) and genotypes (b).
Crops 05 00015 g005

4. Discussion

Cadmium is an element that appears to have no positive effect on plant metabolism. Cd stress usually causes reduced development in plants. This reaction might be attributed to Cd ion toxicity that affects plant metabolism, or to irregularities in the absorption of critical bio-elements required for growth and development [51]. Because cadmium and phosphorus create insoluble complexes, it has been found that phosphorus deficit was the primary cause of reduced development in plants under Cd stress [52]. Under heavy metal stress, a deficiency or absence of photosynthetic equipment inhibits organic metabolites, resulting in reduced development [53].
Our findings indicated that cadmium inhibited the development of three hulless barley genotypes: Assiya, Giza130, and Tombari. Significant reductions in shoot and root dry weight per plant, flag leaf area, and stem length were noted, along with particularly damaging consequences at elevated stress levels. Our findings are consistent with previously reported investigations which found that cotton and sorghum cultivars under heavy metal stress showed a linear decline in plant height, root and shoot dry weight, and leaf width [53,54,55]. Globally, plants that are grown under high-soil concentration of Cd are affected by altered metabolic processes that result in decreased growth and biomass production [56]. Cd accumulation in barley plant roots, leaves, and stems increased as the soil Cd content increased. Indeed, Cadmium accumulation in plant organs has been shown to affect important physiological activities and inhibit plant development [57,58,59,60,61]. Cd stress influences plant mineral absorption by decreasing the acquisition of a variety of important minerals [62]. It inhibits or reduces photosynthesis and lowers the generation of photo-assimilates, thus limiting growth. These negative impacts are more visible in the aboveground sections of barley plants than in the subsurface ones [63]. Consequentially, one important indicator of a plant’s ability to tolerate stress is its leaf’s relative water content (RWC). As shown in our work, most studies discovered that Cd stress decreased the water in barley plants [64]. The RWC in barley under Cd stress also significantly decreased compared with the control. The likely cause of the negative impact of Cd is an alteration of membrane transporters’ functional structure, according to the results of Liu et al. [65].
Photosynthesis is a major physiological mechanism in plant development and growth [66,67,68]. Cd stress has been reported in several studies to limit plant photosynthesis [69,70,71]. In a number of plant systems, it has been observed that Cd inhibits chlorophyll content [16,53,72]. In addition, Cadmium toxicity also reduced the photosynthetic process, as assessed by chlorophyll SPAD, transpiration rate, and fluorescence (Fv/Fm) according to Millán et al. [73] in Solanum lycopersicum L. (tomato) and Khan et al. [74] in Brassica rapa subsp. chinensis (L.) Hanelt (bok choy) and Ayachi et al. [40] in Hordeum vulgare L. (common barley). Our research revealed that cadmium (Cd) stress caused a notable decrease in the SPAD index, transpiration rate, and chlorophyll fluorescence (Fv/Fm) in hulless barley leaves, suggesting that the drop in the SPAD index was primarily attributed to non-stomatal factors [75]. Simultaneously, the transpiration rate was also decreased in all barley varieties according to the results of Liu et al. [76] and Zhao et al. [7]. Other research has shown comparable results in cotton and rice under heavy metal stress [77,78]. The decrease in photosynthetic pigments might be owing to increased hydrogen peroxide generation or the enzyme-mediated destruction of chlorophyll by chlorophyllase [79]. On the other hand, Fv/Fm was reduced under Cd stress in all varieties with a high reduction in Tombari compared to Assiya and Giza130, which indicates impeded photosynthesis according to [70,80]. Fluorescence was determined in order to investigate the fundamental mechanisms causing variations in flag leaf photosynthetic efficiency and the photosynthetic defense mechanism when the two concentrations of cadmium were applied. Fv/Fm decreases suggest photoinhibition as well as a decrease in the maximal quantum efficiency of open PSII units [81]. The decrease in chlorophyll fluorescence metrics most likely indicates that the plants are under stress, such as manganese toxicity [82], lead toxicity [83], or cadmium toxicity [80]. In unfavorable conditions, the increase in reactive oxygen species (ROS) and increased membrane lipid peroxidation led to a decline in oxidative system function, carbon uptake, and PSII activity, ultimately lowering the plant’s photosynthetic capacity [55]. Proline is an essential osmotic protective chemical substance for maintaining adequate cell function, protecting the structural integrity of cell membranes, and maintaining biological macromolecule structures’ stability [84]. The negative impact of the heavy metal exposure is frequently associated with the production and accumulation of different metabolites, such as certain amino acids (e.g., proline) [85]. The formation of amino acids in response to metal stress can be related to the occurrence of protein degradation or amino acid biosynthesis [86]. It was shown that among the amino acids, proline is one of the most common metabolites generated in response to stress [87,88]. According to numerous studies, different abiotic stresses induce plants to generate a considerable quantity and accumulate proline in their organs [51,89]. The effects of proline are not constant since plants use various processes for proline synthesis and degradation under different situations [90]. In our study, proline accumulated with increasing cadmium concentration levels compared to the control, suggesting that cadmium stress induces barley plants to produce more proline to resist osmotic stress. Proline has been suggested to be a component of the higher adaption response to unfavorable circumstances in the environment. Its functions include fluid compatible osmoregulation, metal removal and detoxification, enzymatic defense, proteins synthesis machinery stabilization, and ROS scavenging [91,92].
Toxic metals have been discovered to induce the generation of reactive oxygen species (ROS), which subsequently respond with lipids, nucleic acids, proteins, and other substances, causing lipid peroxidation, membrane degradation, and enzyme deactivation, thus negatively impacting cell function and survival [93]. Cadmium toxicity stimulates the defense antioxidant systems of plants to reduce oxidative damage [94]. Damage caused by ROS increases the amount of H2O2 and MDA in stressed plant tissues [95,96]. Under abiotic stresses such as cadmium, H2O2, the most prevalent and constant species of ROS, plays an important regulatory role in organs of plants, protecting them from abiotic stress [43,97]. MDA levels, a biochemical indication of lipid peroxidation in cellular organelles, can increase in response to a range of external stressful situations [55]. In the current study, all varieties accumulated H2O2 and MDA in their flag leaf tissues as cadmium concentration levels increased, with a high value recorded in Tombari compared to Assiya and Giza130. It might be assumed that cadmium stress induces the generation of lipid peroxidation and membrane degradation as a consequence of H2O2 generation in barley flag leaf. The Assiya Cd-tolerant genotype accumulated more proline and antioxidant enzymes than Cd-sensitive genotypes (Tombari). This buildup may reduce the impact of cadmium on seedling growth in Cd-tolerant genotypes. Conversely, lower MDA content in the Assiya genotype suggests that it prevents the degradation of cells, further supporting the conclusion that this genotype is superior to the other two genotypes tested (Giza130 and Tombari). The results of the PCA revealed that the physiochemical traits associated with the different degrees of tolerance are affected by Cd concentration. The correlation findings confirmed this result.
Numerous studies have shown that enhancing the activity of the protective enzyme system helps to decrease lipid membrane peroxidation and preserve the structural integrity of the membrane system [98]. Antioxidant enzyme activity progressively increases as cadmium levels grow in plants under cadmium stress. However, the protective enzyme system is compromised at extremely high cadmium concentrations, which decreases enzyme activity [99]. In the present study, the activities of the main antioxidant enzymes such as CAT, APX, and POD, were elevated in the presence of cadmium compared to the control in Assiya and Giza130. In contrast, they decreased continuously with increasing cadmium concentration in Tombari. These findings revealed that CAT, APX, and POD were most likely the primary protective enzymes involved in the reactive oxygen elimination mechanism in barley flag leaf. These findings also show that the barley varieties Assiya and Giza130 enhance their resistance to cadmium stress and adjust to the formation of reactive oxygen species (ROS) by modifying the activities of CAT, APX, and POD, eliminating hazardous materials like O2− and H2O2 to keep plants’ free radical metabolism functioning correctly [100]. Simultaneously, the elevated toxicity of Cd can inhibit the antioxidant system’s capacity to respond to damage [60]. However, the activities of CAT, APX, and POD in stressed plants decreased when the concentration of cadmium exceeded a threshold. This caused a limited capacity to eliminate ROS and the occurrence of significant damage to the functioning membranes and enzyme systems of plant tissues and cells in barley plants.

5. Conclusions

In our research, higher levels of Cd stress led to a significant decrease in plant growth, evident in the effect on shoot and root growth. Despite this, the increased accumulation of Cd in leaves under higher stress levels suggests that barley could be a promising candidate for phytoremediation in Cd-polluted soils. Furthermore, key indicators such as photosynthesis rate, SPAD index, and transpiration rate declined with escalating Cd stress. The impact of Cd stress included heightened lipid peroxidation, with varying responses in antioxidant mechanisms. Notably, the activities of CAT, APX, and POD decreased with increasing Cd stress, while proline levels rose. Consequently, Cd application disrupted the physiological and biochemical processes in hulless barley varieties, leading to compromised osmotic adjustment, increased oxidative damage, and reduced photosynthesis and growth. The genotype Tombari was the most sensitive and accumulated high amounts of cadmium, but Assiya and Giza130 were the more tolerant genotypes, with a lower accumulation in their shoots. Future investigations involving molecular and proteomics studies are essential for a more comprehensive understanding of Cd-stress tolerance in hulless barley.

Author Contributions

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

Funding

This research received no external funding.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Acknowledgments

We would like to thank the INRA in Morocco, the NRC in Egypt, and the NGB in Tunisia for providing us with the seeds of barley which we investigated in this work. We also thank all members of the plant research station at the NRE Lab for their help with the plant harvest and managing plants culture in the greenhouse.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
Fv/FmChlorophyll fluorescence
ETranspiration rates
CdCadmium
CATCatalase
APXAscorbate peroxidase
PODGuaiacol peroxidase
MDAMalondialdehyde
H2O2Hydrogen peroxide
RWCRelative water content

References

  1. Yan, H.; Xu, W.; Xie, J.; Gao, Y.; Wu, L.; Sun, L.; Feng, L.; Chen, X.; Zhang, T.; Dai, C.; et al. Variation of a Major Facilitator Superfamily Gene Contributes to Differential Cadmium Accumulation between Rice Subspecies. Nat. Commun. 2019, 10, 2562. [Google Scholar] [CrossRef]
  2. Borjac, J.; El Joumaa, M.; Kawach, R.; Youssef, L.; Blake, D.A. Heavy Metals and Organic Compounds Contamination in Leachates Collected from Deir Kanoun Ras El Ain Dump and Its Adjacent Canal in South Lebanon. Heliyon 2019, 5, e02212. [Google Scholar] [CrossRef]
  3. Abdikulov, Z.; Ergashev, M. Effect of Cadmium Metal on Barley (Hordeum Vulgare) Growth and Development. In E3S Web of Conferences; EDP Sciences: Les Ulis, France, 2021; Volume 304, p. 03017. [Google Scholar]
  4. Ai-Qasi, B.A.; Sharqi, M.M.; Faiath, S.E. Effect of Nitrogen Fertilizer Sources, Lead and Cadmium Pollution on Some Properties of Barley (Hordeum Vulgare). In Proceedings of the IOP Conference Series: Earth and Environmental Science, Ramadi, Iraq, 17–18 November 2021; Volume 904, p. 012057. [Google Scholar]
  5. González, A.; Gil-Díaz, M.; Lobo, M.C. Response of two barley cultivars to increasing concentrations of cadmium or chromium in soil during the growing period. Biol. Trace Elem. Res. 2015, 163, 235–243. [Google Scholar] [PubMed]
  6. Saxena, G.; Chandra, R.; Bharagava, R.N. Environmental Pollution, Toxicity Profile and Treatment Approaches for Tannery Wastewater and Its Chemical Pollutants; Impact Factor: 7.00 @ JCR Reports 2018 Environmental Pollution; Springer: Berlin/Heidelberg, Germany, 2016. [Google Scholar]
  7. Zhao, S.; Zhang, Q.; Liu, M.; Zhou, H.; Ma, C.; Wang, P. Regulation of Plant Responses to Salt Stress. Int. J. Mol. Sci. 2021, 22, 4609. [Google Scholar] [CrossRef] [PubMed]
  8. Nouri, M.; Haddioui, A. Human and Animal Health Risk Assessment of Metal Contamination in Soil and Plants from Ait Ammar Abandoned Iron Mine, Morocco. Environ. Monit. Assess. 2016, 188, 6. [Google Scholar] [CrossRef]
  9. Liang, C.; Xiao, H.; Hu, Z.; Zhang, X.; Hu, J. Uptake, Transportation, and Accumulation of C60 Fullerene and Heavy Metal Ions (Cd, Cu, and Pb) in Rice Plants Grown in an Agricultural Soil. Environ. Pollut. 2018, 235, 330–338. [Google Scholar] [CrossRef]
  10. Haider, F.U.; Liqun, C.; Coulter, J.A.; Cheema, S.A.; Wu, J.; Zhang, R.; Wenjun, M.; Farooq, M. Cadmium Toxicity in Plants: Impacts and Remediation Strategies. Ecotoxicol. Environ. Saf. 2021, 211, 111887. [Google Scholar] [CrossRef]
  11. Bouhraoua, S.; Ferioun, M.; Boussakouran, A.U.; Boussakouran, A.; Belahcen, D.; Srhiouar, N.; Louahlia, S. BIO Web of Conferences. BIO Web Conf. 2024, 98, 1–5. [Google Scholar]
  12. Tran, T.A.; Popova, L.P. Functions and Toxicity of Cadmium in Plants: Recent Advances and Future Prospects. Turk. J. Bot. 2013, 37, 1–13. [Google Scholar] [CrossRef]
  13. Zhang, M.; Fu, M.M.; Qiu, C.W.; Cao, F.; Chen, Z.H.; Zhang, G.; Wu, F. Response of Tibetan Wild Barley Genotypes to Drought Stress and Identification of Quantitative Trait Loci by Genome-Wide Association Analysis. Int. J. Mol. Sci. 2019, 20, 791. [Google Scholar] [CrossRef]
  14. Abbas, T.; Rizwan, M.; Ali, S.; Adrees, M.; Zia-ur-Rehman, M.; Qayyum, M.F.; Ok, Y.S.; Murtaza, G. Effect of Biochar on Alleviation of Cadmium Toxicity in Wheat (Triticum Aestivum L.) Grown on Cd-Contaminated Saline Soil. Environ. Sci. Pollut. Res. 2018, 25, 25668–25680. [Google Scholar] [CrossRef]
  15. Rochayati, S.; Du Laing, G.; Rinklebe, J.; Meissner, R.; Verloo, M. Use of Reactive Phosphate Rocks as Fertilizer on Acid Upland Soils in Indonesia: Accumulation of Cadmium and Zinc in Soils and Shoots of Maize Plants. J. Plant Nutr. Soil Sci. 2011, 174, 186–194. [Google Scholar] [CrossRef]
  16. Vassilev, A.; Perez-Sanz, A.; Semane, B.; Carleer, R.; Vangronsveld, J. Cadmium Accumulation and Tolerance of Two Salix Genotypes Hydroponically Grown in Presence of Cadmium. J. Plant Nutr. 2005, 28, 2159–2177. [Google Scholar] [CrossRef]
  17. Younis, U.; Malik, S.A.; Rizwan, M.; Qayyum, M.F.; Ok, Y.S.; Shah, M.H.R.; Rehman, R.A.; Ahmad, N. Biochar Enhances the Cadmium Tolerance in Spinach (Spinacia oleracea) through Modification of Cd Uptake and Physiological and Biochemical Attributes. Environ. Sci. Pollut. Res. 2016, 23, 21385–21394. [Google Scholar] [CrossRef]
  18. Hasan, S.A.; Ali, B.; Hayat, S.; Ahmad, A. Cadmium-Induced Changes in the Growth and Carbonic Anhydrase Activity of Chickpea. Turk. J. Biol. 2007, 31, 1–5. [Google Scholar]
  19. Farooq, M.A.; Ali, S.; Hameed, A.; Bharwana, S.A.; Rizwan, M.; Ishaque, W.; Farid, M.; Mahmood, K.; Iqbal, Z. Cadmium Stress in Cotton Seedlings: Physiological, Photosynthesis and Oxidative Damages Alleviated by Glycinebetaine. S. Afr. J. Bot. 2016, 104, 61–68. [Google Scholar] [CrossRef]
  20. Anjum, S.A.; Tanveer, M.; Hussain, S.; Bao, M.; Wang, L.; Khan, I.; Ullah, E.; Tung, S.A.; Samad, R.A.; Shahzad, B. Cadmium Toxicity in Maize (Zea mays L.): Consequences on Antioxidative Systems, Reactive Oxygen Species and Cadmium Accumulation. Environ. Sci. Pollut. Res. 2015, 22, 17022–17030. [Google Scholar] [CrossRef]
  21. Nagajyoti, P.C.; Lee, K.D.; Sreekanth, T.V.M. Heavy Metals, Occurrence and Toxicity for Plants: A Review. Environ. Chem. Lett. 2010, 8, 199–216. [Google Scholar] [CrossRef]
  22. Syed, R.; Kapoor, D.; Bhat, A.A. Heavy Metal Toxicity in Plants: A Review. Plant Arch. 2018, 18, 1229–1238. [Google Scholar]
  23. Heyno, E.; Klose, C.; Krieger-Liszkay, A. Origin of Cadmium-Induced Reactive Oxygen Species Production: Mitochondrial Electron Transfer versus Plasma Membrane NADPH Oxidase. New Phytol. 2008, 179, 687–699. [Google Scholar] [CrossRef]
  24. Gallego, S.M.; Pena, L.B.; Barcia, R.A.; Azpilicueta, C.E.; Iannone, M.F.; Rosales, E.P.; Zawoznik, M.S.; Groppa, M.D.; Benavides, M.P. Unravelling Cadmium Toxicity and Tolerance in Plants: Insight into Regulatory Mechanisms. Environ. Exp. Bot. 2012, 83, 33–46. [Google Scholar] [CrossRef]
  25. Newton, A.C.; Flavell, A.J.; George, T.S.; Leat, P.; Mullholland, B.; Ramsay, L.; Revoredo-Giha, C.; Russell, J.; Steffenson, B.J.; Swanston, J.S.; et al. Crops That Feed the World 4. Barley: A Resilient Crop? Strengths and Weaknesses in the Context of Food Security. Food Secur. 2011, 3, 141–178. [Google Scholar] [CrossRef]
  26. Bouhraoua, S.; Ferioun, M.; Nassira, S.; Boussakouran, A.; Akhazzane, M.; Belahcen, D.; Hammani, K.; Louahlia, S. Biomass Partitioning and Physiological Responses of Four Moroccan Barley Varieties Subjected to Salt Stress in a Hydroponic System. J. Plant Biotechnol. 2023, 50, 115–126. [Google Scholar]
  27. Ferioun, M.; Zouitane, I.; Bouhraoua, S.; Elouattassi, Y.; Belahcen, D.; Errabbani, A.; Louahlia, S.; Sayyed, R.; El Ghachtouli, N. Applying Microbial Biostimulants and Drought-Tolerant Genotypes to Enhance Barley Growth and Yield under Drought Stress. Front. Plant Sci. 2025, 15, 1494987. [Google Scholar]
  28. Salih, G.; Jilal, A.; Garcia, M.S.; Visioni, A. L’orge Alimentaire En Afrique Du Nord: Etat Des Connaissances et Opportunités de Développement. Afr. Mediterr. Agric. J. Al Awamia 2022, 137, 41–64. [Google Scholar]
  29. Ferioun, M.; Bouhraoua, S.; Srhiouar, N.; Boussakouran, A.; Belahcen, D.; El Ghachtouli, N.; Sayyed, R.Z.; Louahlia, S. Advanced Multivariate Approaches for Selecting Moroccan Drought-Tolerant Barley (Hordeum vulgare L.) Cultivars. Ecol. Front. 2024, 44, 820–828. [Google Scholar]
  30. FAO (2016) FAOSTAT. Online Statistical Database—Recherche Google. Available online: https://www.google.com/search?q=FAO+%282016%29+FAOSTAT.+Online+statistical+datab (accessed on 5 February 2025).
  31. Ferioun, M.; Zouitane, I.; Bouhraoua, S.; Belahcen, D.; Srhiouar, N.; Louahlia, S.; El Ghachtouli, N. PGPR Consortia Promote Soil Quality and Functioning in Barley Rhizosphere under Different Levels of Drought Stress. Ecol. Front. 2024, 45, 444–454. [Google Scholar] [CrossRef]
  32. Cop 2017 Recherche Google. Available online: https://www.google.com/search?q=cop+2017+Morocco+is+know (accessed on 11 March 2025).
  33. Hakkou, R.; Benzaazoua, M.; Bussière, B. Valorization of Phosphate Waste Rocks and Sludge from the Moroccan Phosphate Mines: Challenges and Perspectives. Procedia Eng. 2016, 138, 110–118. [Google Scholar] [CrossRef]
  34. Forster, B.P.; Ellis, R.P.; Moir, J.; Talamè, V.; Sanguineti, M.C.; Tuberosa, R.; This, D.; Teulat-Merah, B.; Ahmed, I.; Mariy, S.A.E.E.; et al. Genotype and Phenotype Associations with Drought Tolerance in Barley Tested in North Africa. Ann. Appl. Biol. 2004, 144, 157–168. [Google Scholar] [CrossRef]
  35. Nouri, M.; El Rasafi, T.; Haddioui, A. Responses of Two Barley Subspecies to in Vitro-Induced Heavy Metal Stress: Seeds Germination, Seedlings Growth and Cytotoxicity Assay. Agriculture 2019, 65, 107–118. [Google Scholar] [CrossRef]
  36. ICARDA 2017. Barley Is an Adaptable Crop That Can Thrive in Adverse Conditions, Promoting Typically Constant Yields with Little Labor—Recherche Google. Available online: https://www.google.com/search?q=ICARDA+2017+Barley+is+an+adapta (accessed on 11 March 2025).
  37. Dawson, I.K.; Russell, J.; Powell, W.; Steffenson, B.; Thomas, W.T.B.; Waugh, R. Barley: A Translational Model for Adaptation to Climate Change. New Phytol. 2015, 206, 913–931. [Google Scholar] [CrossRef] [PubMed]
  38. Muñoz-Amatriaín, M.; Cuesta-Marcos, A.; Hayes, P.M.; Muehlbauer, G.J. Barley Genetic Variation: Implications for Crop Improvement. Brief. Funct. Genom. Proteom. 2014, 13, 341–350. [Google Scholar] [CrossRef]
  39. Ryan, J.; Sommer, R. Soil Fertility and Crop Nutrition Research at an International Center in the Mediterranean Region: Achievements and Future Perspective. Arch. Agron. Soil Sci. 2012, 58, 37–41. [Google Scholar] [CrossRef]
  40. Ayachi, I.; Ghabriche, R.; Zineb, A.B.; Hanana, M.; Abdelly, C.; Ghnaya, T. NaCl Effect on Cd Accumulation and Cell Compartmentalization in Barley. Environ. Sci. Pollut. Res. 2023, 30, 49215–49225. [Google Scholar] [CrossRef]
  41. Stephania, G.; Macpherson, H.G. Food Barley: Importance, Uses and Local Knowledge. In Barley-Based Food in Southern Morocco; ICARDA: Beriut, Lebanon, 2005; pp. 53–82. [Google Scholar]
  42. Bouhraoua, S.; Ferioun, M.; Boussakouran, A.; Belahcen, D.; Srhiouar, N.; Hammani, K.; Louahlia, S. Physio-Biochemical Responses and Yield Performance of North African Barley Genotypes Submitted to Moderate and Severe Salinity. Cereal Res. Commun. 2024, 53, 337–353. [Google Scholar] [CrossRef]
  43. Wang, M.; Yang, Y.; Chen, W. Manganese, Zinc, and pH Affect Cadmium Accumulation in Rice Grain under Field Conditions in Southern China. J. Environ. Qual. 2018, 47, 306–311. [Google Scholar] [CrossRef]
  44. Ogbaga, C.C.; Stepien, P.; Johnson, G.N. Sorghum (Sorghum bicolor) Varieties Adopt Strongly Contrasting Strategies in Response to Drought. Physiol. Plant. 2014, 152, 389–401. [Google Scholar] [CrossRef]
  45. Bates, L.S. Short Communication Rapid Determination of Free Proline for water-stress studies. Plant Soil 1973, 207, 205–207. [Google Scholar]
  46. Stewart, R.R.C.; Bewley, J.D. Lipid Peroxidation Associated with Accelerated Aging of Soybean Axes. Plant Physiol. 1980, 65, 245–248. [Google Scholar] [CrossRef]
  47. Lipkin, H.J. Interference, Mixing, and Angular Correlations in Decays of Boson Resonances. Phys. Rev. 1968, 176, 1709–1714. [Google Scholar] [CrossRef]
  48. Cakmak, I.; Marschner, H. Magnesium Deficiency and High Light Intensity Enhance Activities of Superoxide Dismutase, Ascorbate Peroxidase, and Glutathione Reductase in Bean Leaves. Plant Physiol. 1992, 98, 1222–1227. [Google Scholar] [CrossRef] [PubMed]
  49. Wu, J.; Feng, Y.; Dai, Y.; Cui, N.; Anderson, B.; Cheng, S. Biological Mechanisms Associated with Triazophos (TAP) Removal by Horizontal Subsurface Flow Constructed Wetlands (HSFCW). Sci. Total Environ. 2016, 553, 13–19. [Google Scholar] [CrossRef] [PubMed]
  50. Nakano, Y.; Asada, K. APX Nakano & Asada 1981.Pdf. Plant Cell Physiol. 2018, 22, 867–880. [Google Scholar]
  51. Waheed, A.; Haxim, Y.; Islam, W.; Ahmad, M.; Ali, S.; Wen, X.; Khan, K.A.; Ghramh, H.A.; Zhang, Z.; Zhang, D. Impact of Cadmium Stress on Growth and Physio-Biochemical Attributes of Eruca Sativa Mill. Plants 2022, 11, 2981. [Google Scholar] [CrossRef]
  52. Gonçalves, J.F.; Antes, F.G.; Maldaner, J.; Pereira, L.B.; Tabaldi, L.A.; Rauber, R.; Rossato, L.V.; Bisognin, D.A.; Dressler, V.L.; de Moraes Flores, É.M.; et al. Cadmium and Mineral Nutrient Accumulation in Potato Plantlets Grown under Cadmium Stress in Two Different Experimental Culture Conditions. Plant Physiol. Biochem. 2009, 47, 814–821. [Google Scholar] [CrossRef]
  53. Hasan, S.; Sehar, Z.; Khan, N.A. Gibberellic Acid and Sulfur-Mediated Reversal of Cadmium-Inhibited Photosynthetic Performance in Mungbean (Vigna radiata L.) Involves Nitric Oxide. J. Plant Growth Regul. 2020, 39, 1605–1615. [Google Scholar] [CrossRef]
  54. Daud, M.K.; Sun, Y.; Dawood, M.; Hayat, Y.; Variath, M.T.; Wu, Y.X.; Raziuddin; Mishkat, U.; Salahuddin; Najeeb, U.; et al. Cadmium-Induced Functional and Ultrastructural Alterations in Roots of Two Transgenic Cotton Cultivars. J. Hazard. Mater. 2009, 161, 463–473. [Google Scholar] [CrossRef]
  55. An, M.J.; Wang, H.J.; Fan, H.; Ippolito, J.A.; Meng, C.; Yulian, E.; Li, Y.; Wang, K.; Wei, C. Effects of Modifiers on the Growth, Photosynthesis, and Antioxidant Enzymes of Cotton Under Cadmium Toxicity. J. Plant Growth Regul. 2019, 38, 1196–1205. [Google Scholar] [CrossRef]
  56. Saidi, I.; Ayouni, M.; Dhieb, A.; Chtourou, Y.; Chaïbi, W.; Djebali, W. Oxidative Damages Induced by Short-Term Exposure to Cadmium in Bean Plants: Protective Role of Salicylic Acid. S. Afr. J. Bot. 2013, 85, 32–38. [Google Scholar] [CrossRef]
  57. Ali, B.; Deng, X.; Hu, X.; Gill, R.A.; Ali, S.; Wang, S.; Zhou, W. Deteriorative Effects of Cadmium Stress on Antioxidant System and Cellular Structure in Germinating Seeds of Brassica napus L. J. Agric. Sci. Technol. 2015, 17, 63–74. [Google Scholar]
  58. Anwaar, S.A.; Ali, S.; Ali, S.; Ishaque, W.; Farid, M.; Farooq, M.A.; Najeeb, U.; Abbas, F.; Sharif, M. Silicon (Si) Alleviates Cotton (Gossypium hirsutum L.) from Zinc (Zn) Toxicity Stress by Limiting Zn Uptake and Oxidative Damage. Environ. Sci. Pollut. Res. 2015, 22, 3441–3450. [Google Scholar] [CrossRef] [PubMed]
  59. Gill, S.S.; Khan, N.A.; Tuteja, N. Cadmium at High Dose Perturbs Growth, Photosynthesis and Nitrogen Metabolism While at Low Dose It up Regulates Sulfur Assimilation and Antioxidant Machinery in Garden Cress (Lepidium sativum L.). Plant Sci. 2012, 182, 112–120. [Google Scholar] [CrossRef] [PubMed]
  60. Yang, L.P.; Zhu, J.; Wang, P.; Zeng, J.; Tan, R.; Yang, Y.Z.; Liu, Z.M. Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotoxicol. Environ. Saf. 2018, 160, 10–18. [Google Scholar] [CrossRef]
  61. Shah, A.A.; Khan, W.U.; Yasin, N.A.; Akram, W.; Ahmad, A.; Abbas, M.; Ali, A.; Safdar, M.N. Butanolide Alleviated Cadmium Stress by Improving Plant Growth, Photosynthetic Parameters and Antioxidant Defense System of Brassica Oleracea. Chemosphere 2020, 261, 127728. [Google Scholar] [CrossRef]
  62. Kaya, C.; Akram, N.A.; Ashraf, M.; Alyemeni, M.N.; Ahmad, P. Exogenously Supplied Silicon (Si) Improves Cadmium Tolerance in Pepper (Capsicum annuum L.) by up-Regulating the Synthesis of Nitric Oxide and Hydrogen Sulfide. J. Biotechnol. 2020, 316, 35–45. [Google Scholar] [CrossRef]
  63. Ekmekçi, Y.; Tanyolaç, D.; Ayhan, B. Effects of Cadmium on Antioxidant Enzyme and Photosynthetic Activities in Leaves of Two Maize Cultivars. J. Plant Physiol. 2008, 165, 600–611. [Google Scholar] [CrossRef]
  64. Al Mahmud, J.; Hasanuzzaman, M.; Nahar, K.; Rahman, A.; Hossain, M.S.; Fujita, M. Maleic Acid Assisted Improvement of Metal Chelation and Antioxidant Metabolism Confers Chromium Tolerance in Brassica Juncea L. Ecotoxicol. Environ. Saf. 2017, 144, 216–226. [Google Scholar] [CrossRef]
  65. Liu, X.; Meng, Y.; Wei, S.; Gu, W. Exogenous Hemin Confers Cadmium Tolerance by Decreasing Cadmium Accumulation and Modulating Water Status and Matter Accumulation in Maize Seedlings. Agronomy 2021, 11, 739. [Google Scholar] [CrossRef]
  66. Liu, H.; Zhang, C.; Wang, J.; Zhou, C.; Feng, H.; Mahajan, M.D.; Han, X. Influence and Interaction of Iron and Cadmium on Photosynthesis and Antioxidative Enzymes in Two Rice Cultivars. Chemosphere 2017, 171, 240–247. [Google Scholar] [CrossRef]
  67. Zhang, Z.; Rengel, Z.; Meney, K.; Pantelic, L.; Tomanovic, R. Polynuclear Aromatic Hydrocarbons (PAHs) Mediate Cadmium Toxicity to an Emergent Wetland Species. J. Hazard. Mater. 2011, 189, 119–126. [Google Scholar] [CrossRef] [PubMed]
  68. Ferioun, M.; Bouhraoua, S.; Belahcen, D.; Zouitane, I.; Srhiouar, N.; Louahlia, S.; El Ghachtouli, N. PGPR Consortia Enhance Growth and Yield in Barley Cultivars Subjected to Severe Drought Stress and Subsequent Recovery. Rhizosphere 2024, 31, 100926. [Google Scholar]
  69. Chu, J.; Zhu, F.; Chen, X.; Liang, H.; Wang, R.; Wang, X.; Huang, X. Effects of Cadmium on Photosynthesis of Schima Superba Young Plant Detected by Chlorophyll Fluorescence. Environ. Sci. Pollut. Res. 2018, 25, 10679–10687. [Google Scholar] [CrossRef]
  70. Parmar, P.; Kumari, N.; Sharma, V. Structural and Functional Alterations in Photosynthetic Apparatus of Plants under Cadmium Stress. Bot. Stud. 2013, 54, 45. [Google Scholar] [CrossRef]
  71. Qin, X.; Nie, Z.; Liu, H.; Zhao, P.; Qin, S.; Shi, Z. Influence of Selenium on Root Morphology and Photosynthetic Characteristics of Winter Wheat under Cadmium Stress. Environ. Exp. Bot. 2018, 150, 232–239. [Google Scholar] [CrossRef]
  72. Jain, M.; Pal, M.; Gupta, P.; Gadre, R. Effect of Cadmium on Chlorophyll Biosynthesis and Enzymes of Nitrogen Assimilation in Greening Maize Leaf Segments: Role of 2-Oxoglutarate. Indian J. Exp. Biol. 2007, 45, 385–389. [Google Scholar] [PubMed]
  73. López-Millán, A.F.; Sagardoy, R.; Solanas, M.; Abadía, A.; Abadía, J. Cadmium Toxicity in Tomato (Lycopersicon esculentum) Plants Grown in Hydroponics. Environ. Exp. Bot. 2009, 65, 376–385. [Google Scholar] [CrossRef]
  74. Khan, K.Y.; Ali, B.; Stoffella, P.J.; Cui, X.; Yang, X.; Guo, Y. Study Amino Acid Contents, Plant Growth Variables and Cell Ultrastructural Changes Induced by Cadmium Stress between Two Contrasting Cadmium Accumulating Cultivars of Brassica rapa ssp. Chinensis L. (Pak choi). Ecotoxicol. Environ. Saf. 2020, 200, 110748. [Google Scholar] [CrossRef]
  75. Bloomfield, K.J.; Farquhar, G.D.; Lloyd, J. Photosynthesis-Nitrogen Relationships in Tropical Forest Tree Species as Affected by Soil Phosphorus Availability: A Controlled Environment Study. Funct. Plant Biol. 2014, 41, 820–832. [Google Scholar] [CrossRef]
  76. Liu, L.; Shang, Y.K.; Li, L.; Chen, Y.H.; Qin, Z.Z.; Zhou, L.J.; Yuan, M.; Ding, C.B.; Liu, J.; Huang, Y.; et al. Cadmium Stress in Dongying Wild Soybean Seedlings: Growth, Cd Accumulation, and Photosynthesis. Photosynthetica 2018, 56, 1346–1352. [Google Scholar] [CrossRef]
  77. Daud, M.K.; Quiling, H.; Lei, M.; Ali, B.; Zhu, S.J. Ultrastructural, Metabolic and Proteomic Changes in Leaves of Upland Cotton in Response to Cadmium Stress. Chemosphere 2015, 120, 309–320. [Google Scholar] [CrossRef] [PubMed]
  78. Li, H.; Luo, N.; Li, Y.W.; Cai, Q.Y.; Li, H.Y.; Mo, C.H.; Wong, M.H. Cadmium in Rice: Transport Mechanisms, Influencing Factors, and Minimizing Measures. Environ. Pollut. 2017, 224, 622–630. [Google Scholar] [CrossRef] [PubMed]
  79. Hassan, B.K. The effect of copper and cadmium on oxygen consumption of the juvenile common carp, Cyprinus carpio (L.). Mesopotamian J. Mar. Sci. 2011, 26, 25–34. [Google Scholar]
  80. Zouari, M.; Ben Ahmed, C.; Zorrig, W.; Elloumi, N.; Rabhi, M.; Delmail, D.; Ben Rouina, B.; Labrousse, P.; Ben Abdallah, F. Exogenous Proline Mediates Alleviation of Cadmium Stress by Promoting Photosynthetic Activity, Water Status and Antioxidative Enzymes Activities of Young Date Palm (Phoenix dactylifera L.). Ecotoxicol. Environ. Saf. 2016, 128, 100–108. [Google Scholar] [CrossRef]
  81. Murchie, E.H.; Lawson, T. Chlorophyll Fluorescence Analysis: A Guide to Good Practice and Understanding Some New Applications. J. Exp. Bot. 2013, 64, 3983–3998. [Google Scholar] [CrossRef]
  82. Li, P.; Song, A.; Li, Z.; Fan, F.; Liang, Y. Silicon Ameliorates Manganese Toxicity by Regulating Both Physiological Processes and Expression of Genes Associated with Photosynthesis in Rice (Oryza sativa L.). Plant Soil 2015, 397, 289–301. [Google Scholar] [CrossRef]
  83. Li, X.; Bu, N.; Li, Y.; Ma, L.; Xin, S.; Zhang, L. Growth, Photosynthesis and Antioxidant Responses of Endophyte Infected and Non-Infected Rice under Lead Stress Conditions. J. Hazard. Mater. 2012, 213, 55–61. [Google Scholar] [CrossRef] [PubMed]
  84. Zhao, H.; Guan, J.; Liang, Q.; Zhang, X.; Hu, H.; Zhang, J. Effects of Cadmium Stress on Growth and Physiological Characteristics of Sassafras Seedlings. Sci. Rep. 2021, 11, 9913. [Google Scholar] [CrossRef]
  85. Jha, A.B.; Dubey, R.S. Carbohydrate Metabolism in Growing Rice Seedlings under Arsenic Toxicity. J. Plant Physiol. 2004, 161, 867–872. [Google Scholar] [CrossRef]
  86. Sharma, S.S.; Dietz, K.J. The Significance of Amino Acids and Amino Acid-Derived Molecules in Plant Responses and Adaptation to Heavy Metal Stress. J. Exp. Bot. 2006, 57, 711–726. [Google Scholar] [CrossRef]
  87. Khan, M.I.R.; Nazir, F.; Asgher, M.; Per, T.S.; Khan, N.A. Selenium and Sulfur Influence Ethylene Formation and Alleviate Cadmium-Induced Oxidative Stress by Improving Proline and Glutathione Production in Wheat. J. Plant Physiol. 2015, 173, 9–18. [Google Scholar] [CrossRef] [PubMed]
  88. Rady, M.M.; Hemida, K.A. Modulation of Cadmium Toxicity and Enhancing Cadmium-Tolerance in Wheat Seedlings by Exogenous Application of Polyamines. Ecotoxicol. Environ. Saf. 2015, 119, 178–185. [Google Scholar] [CrossRef] [PubMed]
  89. Asgher, M.; Khan, M.I.R.; Iqbal, N.; Masood, A.; Khan, N.A. Cadmium Tolerance in Mustard Cultivars: Dependence on Proline Accumulation and Nitrogen Assimilation. J. Funct. Environ. Bot. 2012, 3, 30. [Google Scholar] [CrossRef]
  90. Deng, X.; Walker, R.G.; Morris, J.; Davidson, W.S.; Thompson, T.B. Role of Conserved Proline Residues in Human Apolipoprotein A-IV Structure and Function. J. Biol. Chem. 2015, 290, 10689–10702. [Google Scholar] [CrossRef]
  91. Sharmila, P.; Pardha Saradhi, P. Proline Accumulation in Heavy Metal Stressed Plants: An Adaptive Strategy. In Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants; Springer: Berlin/Heidelberg, Germany, 2002; pp. 179–199. [Google Scholar] [CrossRef]
  92. Siddique, A.; Kandpal, G.; Kumar, P. Proline Accumulation and Its Defensive Role under Diverse Stress Condition in Plants: An Overview. J. Pure Appl. Microbiol. 2018, 12, 1655–1659. [Google Scholar] [CrossRef]
  93. Ahmad, P.; Jaleel, C.A.; Salem, M.A.; Nabi, G.; Sharma, S. Roles of Enzymatic and Nonenzymatic Antioxidants in Plants during Abiotic Stress. Crit. Rev. Biotechnol. 2010, 30, 161–175. [Google Scholar] [CrossRef]
  94. Shahid, M. Reviews of Environmental Contamination and Toxicology; Springer: Berlin/Heidelberg, Germany, 2014; Volume 232, ISBN 9783319067452. [Google Scholar]
  95. Nie, S.; Huang, S.; Wang, S.; Mao, Y.; Liu, J.; Ma, R.; Wang, X. Enhanced Brassinosteroid Signaling Intensity via SlBRI1 Overexpression Negatively Regulates Drought Resistance in a Manner Opposite of That via Exogenous BR Application in Tomato. Plant Physiol. Biochem. 2019, 138, 36–47. [Google Scholar] [CrossRef]
  96. Sairam, R.K.; Chandrasekhar, V.; Srivastava, G.C. Sairam et al 2000.PDF. Biol. Plant. 2001, 44, 89–94. [Google Scholar] [CrossRef]
  97. Kohli, S.K.; Khanna, K.; Bhardwaj, R.; Abd Allah, E.F.; Ahmad, P.; Corpas, F.J. Assessment of Subcellular ROS and NO Metabolism in Higher Plants: Multifunctional Signaling Molecules. Antioxidants 2019, 8, 641. [Google Scholar] [CrossRef]
  98. Ozfidan-Konakci, C.; Yildiztugay, E.; Bahtiyar, M.; Kucukoduk, M. The Humic Acid-Induced Changes in the Water Status, Chlorophyll Fluorescence and Antioxidant Defense Systems of Wheat Leaves with Cadmium Stress. Ecotoxicol. Environ. Saf. 2018, 155, 66–75. [Google Scholar] [CrossRef]
  99. Chaâbene, Z.; Hakim, I.R.; Rorat, A.; Elleuch, A.; Mejdoub, H.; Vandenbulcke, F. Copper Toxicity and Date Palm (Phoenix dactylifera) Seedling Tolerance: Monitoring of Related Biomarkers. Environ. Toxicol. Chem. 2018, 37, 797–806. [Google Scholar] [CrossRef] [PubMed]
  100. Liu, Q.; Vetukuri, R.R.; Xu, W.; Xu, X. Transcriptomic Responses of Dove Tree (Davidia involucrata Baill.) to Heat Stress at the Seedling Stage. Forests 2019, 10, 656. [Google Scholar] [CrossRef]
Crops 05 00015 g002
Figure 2. Cadmium concentrations (a) and proportions (b) in leaves, stems, and roots in North African hulless barley genotypes under control and cadmium stress conditions (15 and 30 mg/kg).
Figure 2. Cadmium concentrations (a) and proportions (b) in leaves, stems, and roots in North African hulless barley genotypes under control and cadmium stress conditions (15 and 30 mg/kg).
Crops 05 00015 g002
Crops 05 00015 g003
Figure 3. Means values of different physiological traits including relative water content (a), transpiration (b), SPAD (c), and Fv/Fm (d) of hulless barley varieties under different levels of cadmium concentrations. Values indicate the mean ± SD (n = 3).
Figure 3. Means values of different physiological traits including relative water content (a), transpiration (b), SPAD (c), and Fv/Fm (d) of hulless barley varieties under different levels of cadmium concentrations. Values indicate the mean ± SD (n = 3).
Crops 05 00015 g003
Crops 05 00015 g004
Figure 4. Means values of different biochemical traits including: proline content (a), Malondialdehyde (MDA) (b), H2O2 (c), catalase (CAT) activity (d), ascorbate peroxidase (APX) activity (e), and peroxidase (POD) activity (f) of hulless barley varieties under different levels of cadmium concentrations. Values indicate the mean ± SD (n = 3).
Figure 4. Means values of different biochemical traits including: proline content (a), Malondialdehyde (MDA) (b), H2O2 (c), catalase (CAT) activity (d), ascorbate peroxidase (APX) activity (e), and peroxidase (POD) activity (f) of hulless barley varieties under different levels of cadmium concentrations. Values indicate the mean ± SD (n = 3).
Crops 05 00015 g004
Table 1. Names and characteristics of the barley collection genotypes used in this study.
Table 1. Names and characteristics of the barley collection genotypes used in this study.
Official NameCountry of OriginRow TypeHulled/Hulless
AssiyaMorocco6 rowsHulless
TombariTunisia6 rowsHulless
Giza 130Egypt6 rowsHulless
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Bouhraoua, S.; Ferioun, M.; Boussakouran, A.; Belahcen, D.; Benali, T.; El Hachlafi, N.; Akhazzane, M.; Khabbach, A.; Hammani, K.; Louahlia, S. Physio-Biochemical Responses and Cadmium Partitioning Associated with Stress Tolerance in Hulless Barley Genotypes. Crops 2025, 5, 15. https://doi.org/10.3390/crops5020015

AMA Style

Bouhraoua S, Ferioun M, Boussakouran A, Belahcen D, Benali T, El Hachlafi N, Akhazzane M, Khabbach A, Hammani K, Louahlia S. Physio-Biochemical Responses and Cadmium Partitioning Associated with Stress Tolerance in Hulless Barley Genotypes. Crops. 2025; 5(2):15. https://doi.org/10.3390/crops5020015

Chicago/Turabian Style

Bouhraoua, Said, Mohamed Ferioun, Abdelali Boussakouran, Douae Belahcen, Taoufiq Benali, Naoufal El Hachlafi, Mohamed Akhazzane, Abdelmajid Khabbach, Khalil Hammani, and Said Louahlia. 2025. "Physio-Biochemical Responses and Cadmium Partitioning Associated with Stress Tolerance in Hulless Barley Genotypes" Crops 5, no. 2: 15. https://doi.org/10.3390/crops5020015

APA Style

Bouhraoua, S., Ferioun, M., Boussakouran, A., Belahcen, D., Benali, T., El Hachlafi, N., Akhazzane, M., Khabbach, A., Hammani, K., & Louahlia, S. (2025). Physio-Biochemical Responses and Cadmium Partitioning Associated with Stress Tolerance in Hulless Barley Genotypes. Crops, 5(2), 15. https://doi.org/10.3390/crops5020015

Article Metrics

Back to TopTop