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Article

Mitigation of Cadmium Induced Oxidative Stress by Using Organic Amendments to Improve the Growth and Yield of Mash Beans [Vigna mungo (L.)]

by
Muhammad Umer Chattha
1,
Warda Arif
2,
Imran Khan
1,
Walid Soufan
3,
Muhammad Bilal Chattha
4,
Muhammad Umair Hassan
5,
Najeeb Ullah
6,
Ayman El Sabagh
7,* and
Sameer H. Qari
8
1
Department of Agronomy, University of Agriculture, Faisalabad 38040, Pakistan
2
Department of Botany, University of Agriculture, Faisalabad 38040, Pakistan
3
Plant Production Department, College of Food and Agriculture Sciences, King Saud University, P.O. Box 2460, Riyadh 11451, Saudi Arabia
4
Department of Agronomy, Faculty of Agricultural Sciences, University of the Punjab Lahore, Lahore 54590, Pakistan
5
Research Center on Ecological Sciences, Jiangxi Agricultural University, Nanchang 330045, China
6
Queensland Alliance Agriculture and Food Innovation Center for Plant Science, University of Queens Land Wilsonton Heights, Toowoomba, QLD 4350, Australia
7
Department of Agronomy, Faculty of Agriculture, Kafrelsheikh University, Kafrelsheikh 33516, Egypt
8
Biology Department, Aliumum University College, Umm Al-Qura University, Mecca 21955, Saudi Arabia
*
Author to whom correspondence should be addressed.
Agronomy 2021, 11(11), 2152; https://doi.org/10.3390/agronomy11112152
Submission received: 1 October 2021 / Revised: 19 October 2021 / Accepted: 19 October 2021 / Published: 27 October 2021
(This article belongs to the Special Issue Physio–Devo of Source–Sink Relationship Underlying Abiotic Stress Resilience in Crop Plants)
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Abstract

:
Cadmium (Cd) stress is a serious environmental hazard that has devastating impacts on plant growth and productivity. Moreover, the entrance of Cd into the human food chain by eating Cd-contaminated food also poses serious health issues. Organic amendments (OA) possess an excellent potential to reduce the adverse impacts of Cd stress. Therefore, the aim of this study was to determine the potential of different OA in improving the mash beans growth and yield grown under Cd-contaminated soil. The soil was spiked with different concentrations of Cd (0, 10 and 20 mg/kg) and subjected to different OA, i.e., control, cow manure (5%), sugarcane press mud (5%) and a combination of cow manure (2.5%) and sugarcane press mud (2.5%). Results indicated that Cd stress induced a significant reduction in growth and yield traits, leaf water status, photosynthetic pigments, protein accumulation and anti-oxidant activities. However, the application of OA appreciably reduced the Cd-induced toxic effects and caused a significant increase in growth and yield. The application of 5% sugarcane press mud remained the top performer and it increased the mash bean growth and yield through improved photosynthetic pigments, leaf water status (56%) and reduced Cd uptake (18%), hydrogen peroxide (H2O2) production (38.52%), electrolyte leakage (EL) (42.13%) malondialdehyde (MDA) accumulation (55.88%) and increased accumulation of soluble protein (60.15%) and free amino acids (54%) through improved activities of anti-oxidant enzymes. Therefore, these findings suggested that the application of sugarcane press mud enhanced the growth and yield through reduced Cd accumulation, enhanced photosynthetic pigments, leaf water status, protein and amino accumulation and reduced H2O2, EL and MDA accumulation through a stronger anti-oxidant defense system.

1. Introduction

Soil toxic metals pollution has become a serious issue across the globe and its intensity is continuously increasing which is posing serious threats to crop production and subsequently human health [1]. Human activities are the major source of soil contamination with toxic metals and this problem needs special attention to safe humans, animals and plants. The application of sewage water, industrial activities, mining, waste production and heavy application of pesticides are major reasons of soil contamination [2,3,4]. Toxic metals retain in soil and affect the soil microbes and plant growth and subsequently transferred into plants and impact the human health by entering the food chain [5]. Moreover, they also induced serious alteration in plants ranging from reduction in growth to subsequent mortality [1,6,7].
Cadmium (Cd) is a serious toxic metal that has devastating impacts on plants and human health [8] and it is ranked seventh on the priority list of pollutants [9]. Cadmium is a non-essential metal for plants that has no toxic effects at lower concentrations; however, at higher concentrations, it is highly toxic for plants [10]. Cadmium stress induces serious impacts on the physiological, biochemical and morphological processes of plants [11]. It also disturbs the cell redox status and causes damage to major molecules through over-production of ROS by inhibiting the activities of anti-oxidant enzymes [6,12]. Cadmium stress also disrupts membrane permeability, stomatal movements, photosynthesis, water relations and plant mineral nutrition [13,14,15]. Moreover, Cd also destroys the enzymes of carbohydrate metabolism and the Calvin cycle, and causes significant reduction in photosynthesis and subsequently in crop yield [15,16].
Soil remediation is considered as an imperious strategy to reduce the bio-availability of toxic metals in contaminated soils [17,18]. Soil remediation can be carried out by diverse physical, chemical and biological practices. Biological remediation is standard practice for restoring metal-contaminated soils owing to the fact that it is cost-effective and environmentally friendly as compared to chemical methods [19]. Soil biological remediation techniques can be divided into further strategies including toxic metal stabilization and extraction. Stabilization involves the use of different amendments including compost, biochar, humic acid and farmyard manures to reduce the bio-availability and leaching of HM [20,21]. This practice has been found effective, eco-friendly and economical in reducing the toxic metal bio-availability [22,23]. The application of organic amendments such as press mud, compost, and farmyard manures (FYM) improve the soil properties and reduce the toxic metals’ bio-availability in contaminated soils [24,25]. The application of organic amendments decreases the metals’ availability by forming strong organic complexes with metals [26]. The application of organic amendments improves the soil properties and reduces the metal availability which in turn improves the overall productivity and reduces the effects of toxic metals on soil and subsequently on plants and humans [26,27].
Press-mud is produced in larger quantities as a by-product from the sugar industry [4,28] and it is considered a good soil conditioner [29,30]. The mixing of rock phosphate with press-mud substantially reduces the bio-availability of toxic metals [29]. Press mud possesses an excellent potential to buffer the soil pH which in turn reduces the metals uptake [31,32]. Similarly, press mud also contains functional groups such as hydroxyl ions that play an important role in the adsorption of metals [32]. Moreover, the addition of press mud also improves the soil health and soil structure which, therefore, reduces the accumulation of metals in plant tissues [33]. The application of SPM increases the Cd immobilization in soil owing to the presence of organic matter which, therefore, improves crop growth, productivity and reduces subsequent Cd accumulation in plant parts [31]. Likewise, SPM effectively reduces the uptake of toxic metals which in turn improves overall growth and productivity, and triggers anti-oxidant activities [34]. The application of SPM induces change in soil pH and increases the soil organic matter which increases the nutrient uptake and decreases the Cd uptakes, resulting in an improvement in photosynthetic efficiency, growth and yield, and anti-oxidant activities under Cd stress [35]. Moreover, SPM mobilizes the extractable Cd in the soil solution by charge-specific chelation and cation exchange processes and increases the Cd immobilization by influencing soil properties, resulting in significant improvement in growth [36].
Farmyard manures are also an important natural amendment and their soil application appreciably improves the soil properties, soil fertility and reduces the availability of metals [37]. Cow manure is rich in organic matter and essential nutrients [38] thus its field application is considered as an imperative approach to improve soil fertility [39]. The addition of cow manure and other farmyard manures substantially reduce the mobility and uptake of toxic metals in crops and soil [39]. For, instance the application of chicken and cow manures significantly reduce the Cd phyto-availability in contaminated soil and increased the growth and yield of sweet basil [40,41]. The organic matter present in cow manure substantially increases the Cd immobilization by stable complexes with Cd and increases the nutrients availability and overall growth and yield [40,41,42]. Similarly, other authors also noted that the presence of a higher amount of humified organic matter in cow manure decreases the bio-availability of toxic metals. Cow manure forms strong complexes with Cd, resulting in Cd immobilization and subsequently reducing Cd accumulation in maize, wheat and sweet basil [43,44]. Moreover, cow manure reduces the translocation of Cd from the roots to straw and grains due to reduced Cd availability in the soil solution [45]. Additionally, cow manure also significantly reduces Cd uptake and reduces the Cd induced increase in MDA and ROS through improved anti-oxidant activities [46,47,48].
Mash bean (Vigna mungo) is an important legume crop grown widely in Asia for food, fodder and green manure purposes. It is an important and cheap source of protein and being a legume crop it substantially improves the soil fertility by fixing nitrogen [49]. The seed of mash beans contains 20–31% protein and 56–64% carbohydrate, which makes it an imperative and cheap food for humans [50]. Mash beans not only fix the N; its addition to soil as green manure crop considerably improves the soil fertility on a long-term basis [50]. To our best knowledge, no information is available about the effectiveness of different OA to mitigate the Cd toxicity in mash beans crop. Thus we hypothesized that the application of OA (cow manure and press mud) could improve mash bean growth and yield by reducing the Cd uptake, physiological activities and triggering an anti-oxidant defense system. Therefore, keeping in mind all the aforementioned facts, this study was conducted to determine the potential of cow manure and sugarcane press mud to enhance the growth and yield of mash beans grown in Cd-contaminated soil.

2. Materials and Methods

2.1. Experimental Site

The present study was conducted at the University of Agriculture Faisalabad during April–July 2019. Plastic pots with a 46 cm length and 25 cm diameter were filled with a 3:1 composition of soil and silt. In total, 36 pots were used to perform this study and each pot was filled with 8 kg soil. The soil was collected from the agronomy field to fill the plastic pots. The seeds of mash beans were collected from Ayub Agriculture Research Institute and treated with 70% ethanol to avoid contamination, and then washed with distilled water for the removal of any residues. The experiment was carried out in a completely randomized design (CRD) using three replications in a factorial arrangement.

2.2. Treatments and Crop Husbandry

The experiment was comprised of different levels of cadmium stress control, 10 mg/kg and 20 mg/kg of soil and organic amendments; control, cow manure 5%, sugarcane press mud 5% and cow manure 2.5% + sugarcane press mud 2.5%. Cadmium chloride was used as the source of cadmium to achieve different levels of Cd stress. Cadmium chloride was added into the soil and, after homogenizing, the soil was left for three days for the complete absorption of cadmium chloride. After that, OA (cow manure 5%, sugarcane press mud 5% and cow manure 2.5%+ sugarcane press mud 2.5%) was added into pots according to treatments and properly mixed with soil. To achieve the desired levels of 5% cow manure and 5% press mud, 500 g of cow manure and sugarcane press mud was added in each pot and left for 7 days. Cow manure was collected from Agronomy Farm while press mud was taken from Madina Sugar Mills Limited, Faisalabad. Press mud contained of carbon 304.2 g kg−1 dry weight (DW), nitrogen 108 g kg−1 DW, phosphorus 72 g kg−1 DW, potassium 52 g kg−1 DW, and had pH 6.8. Likewise, cow manure also contained carbon 105 g kg−1 dry weight (DW), 72.5 g kg−1 DW, phosphorus 61.3 g kg−1 DW, potassium 48.4 g kg−1 DW, and had pH 6.42. Moreover, a very low quantity of 0.0042 and 0.0053 g kg−1 DW of Cd was detected in SPM and CM. The seeds of mash beans were sown during the first week of April, 2019 and in each pot, 10 seeds were sown at depth of 1 cm. The pots were regularly visited and irrigation was applied according to crop needs.

2.3. Growth Traits

Three plants from each pot were taken and plant height was measured and leaves per plant were counted and the average was taken. Likewise, same three plants were up-rooted carefully and roots were separated from shoots. After that, roots were washed to remove soil particles and their lengths were measured and averaged. Likewise, the length of separated shoots was measured and averaged. Later on, harvested roots and shoots were weighed to determine the fresh weight and lately oven dried to determine the dry weights.

2.4. Physiological Traits

Fresh leaves were taken and weighed on electrical balance to determine the fresh weight (FW) afterward they were soaked in the water for 24 h and weighed again to determine the turgid weight (TW). The same leaves were oven dried at 70 °C for 24 h to determine the dry weight (DW) and leaf relative water content (RWC) was calculated according to methods of Karrou and Maranville [51] by using the formula given below.
R W C   % = F W − D R T W − D R × 100
Cell membrane permeability was recorded by measuring the electrolyte leakage of cells according to method of Blum and Ebercon [52]. Fresh leaf samples of 0.5 g were dipped in distilled water for 30 min and EC1 was calculated with the help of EC meter, then the samples were heated at 90 °C for 30 min in a water bath for calculation of EC2 and electrolyte leakage percentage determined by the following formula.
EC (%) = (EC1 ÷ EC2) × 100

2.5. Chlorophyll and Carotenoid Contents

Plant photosynthetic pigments (chlorophylls and carotenoids) were measured by methods of Lichtenthale [53]. An amount of 0.5 g of plant leaves was taken, chopped and dipped in 5 mL of 80% methanol solution. After 24 h, samples were centrifuged and the extract was filtered at 10,000 rpm for 10 min. The absorbance of the supernatant was read on a spectrophotometer at a wavelength of 663, 645 and 480 nm and the values of photosynthetic pigments were calculated by the formulas given below:
c h l o r o p h y l l   a = ( 12.7   O D 663 − 2.69   O D 645 × V / 1000 × W
c h l o r o p h y l l   b = ( ( 22.9   O D 645 − 4.68   O D 663 × V / 1000 × W
𝐶𝑎𝑟𝑜𝑡𝑒𝑛𝑜𝑖𝑑 = ((𝑂𝐷480 + 0.114 × 𝑂𝐷663 − 0.636 × 𝑂𝐷645)

2.6. Hydrogen Peroxide (H2O2) and Malondialdehyde (MDA) Contents

H2O2 content was measured according to the protocol as given by Velikova et al. [54]. Leaf samples of 0.5 g were ground in 5 mL of 5% TCA and placed in centrifugation machine at 10,000 rpm for 15 min at 4 °C. The supernatant was collected in Eppendorf. Then, 1 mL of supernatant was added in 1 mL of KI-buffer and 100 µL of phosphate buffer and placed at room temperature for 30 min. The absorbance was recorded at 390 nm wavelength in a spectrophotometer andH2O2 contents were calculated by using standardization curve of different concentrations of H2O2. MDA content was measured by the protocol of Buege and Aust [55]. An amount of 0.5 g of leaf sample was ground in 5 mL of 5% TCA and centrifuged at 15,000 rpm for 15 min at 4 °C. Then, the supernatant was collected and 1 mL of supernatant was added in 1 mL of 0.5% TCA and 1 mL of 20% TBA and placed at 9 °C for 50 min. The specific absorbance was recorded at 532 nm and nonspecific-background observation at 600 nm was subtracted from readings. The concentration of MDA was calculated using a molar extinction coefficient 155 mM−h cm−c and expressed as nmol g−a of fresh weight.

2.7. Total Soluble Proteins and Free Amino Acids

Total soluble proteins were determined by the protocol of Bradford [56]. An amount of 5 g of plant leaves was grinded in 5 mL of 50 mM potassium phosphate buffer using chilled pestle and mortar and centrifuged for 15 min at 12,000 rpm. An amount of 100 µL of supernatant was mixed with 3 mL of Bradford reagent and left for 15 min at room temperature. The absorbance was recorded at 590 nm on a spectrometer. Total free amino acids were measured using the protocol of Hamilton and Vanslyke [57]. An amount of 1 mL of plant material was mixed with 1 mL of 2% ninhydrin and 1 mL of 10% pyridine, and then test tubes were placed in the water bath at 90 °C for 30 min. After that, test tubes were cooled at room temperature for 15 min and absorbance was measured at 570 nm.

2.8. Anti-Oxidant Activities

For CAT, POD and APX activity, 1.0 g of leaf sample was grinded in 10 mL of 50 mM K-buffer. Then, it was placed in a centrifugation machine (14,000 rpm) for 30 min at 4 °C and supernatant was collected. For measuring CAT activity, the methodology of Chance and Maehly et al. [58] was followed. An amount of 0.1 mL of supernatant was added in 0.1 mL of H2O2 and 2.5 mL of buffer and absorbance was measured at 240 nm on a spectrometer. POD activity was determined according to the methods of Chance and Maehly [58]. An amount of 100 µL of supernatant was mixed with 700 µL of 50 mM phosphate buffer, 100 µL of 180 mM H2O2 and 180 mM of 100 µL guaiacol and absorbance was measured at 470 nm. APX activity was measured using the protocol of Asada and Takahashi, [59]. An amount of 100 µL of enzyme extract was mixed with 100 µL of 0.5 M ascorbic acid, 6.1 mM of H2O2 and 700 µL of 50 mM buffer. Absorbance was measured at 290 nm using a single beam spectrophotometer. The ascorbic acid activity was determined by the methods of Mukherjee and Choudhri [60]. An amount of 0.5 g of stored leaves was grinded in 5 mL of 10% trichloroacetic acid and centrifuged at 15,000 rpm 15 min at 4 °C. After that 2 mL enzyme extract was reacted with 0.5 mL of DTC (2, 4-dinitrophenyl hydrazine, thiourea and copper sulphate reagent) and incubated for 3 h at 37 °C. Afterward, quickly cooled for 10 min by keeping in ice; 2.5 mL of ice cold H2SO4 was added in it dropwise and the mixture was kept at 37 °C for 30 min and later on absorbance was read at 520 nm.

2.9. Determination of Yield Traits

The pods on each plant were manually counted and the average was taken. Similarly, ten pods from plants of each pot were taken and pod length was measured and grains per pod were counted and averaged. Moreover, harvested plants were weighed to determine the biological yield and, later on, pods from each plant were threshed to determine the grains yield. Additionally, a sub-sample of 100 grains was taken and weighed to determine 100 seed weight.

2.10. Determination of Cadmium Concentrations in Root, Shoot and Seed

The plant samples were oven dried and stored in the laboratory. After that, plant samples were grinded and 0.5 g of each plant part was digested on a hot plate by adding a mixture of acids (HNO3: HClO4 at ratio 2:1) as advised by Jones and Case [61]. After digestion, Cd concentration in different plants parts (roots, stem, leaves and grains) was determined by atomic absorption spectrometry (AAS, PerkinElmer Analyst™ 800) and calculated by the following formula: Cd concentration (µg g−1 of D.M) = (reading of AAS× dilution factor)/dry weight of plant sample.

2.11. Statistical Analysis

The recorded data were analyzed by analysis of variance technique using computer-based software STATISTIX 8.1 (https://statistix.updatestar.com/: accessed on 10 October 2021 and the least significant difference (LSD) test was used to check the significance of treatment means at 5% probability level [62].

3. Results

3.1. Growth Traits

The results indicated that Cd stress induced a significant reduction in growth traits of mash beans; however, application of various organic amendments (OA) appreciably improved growth and biomass production (Figure 1 and Figure 2). The maximum root length (RL) (6.85 cm) was noted in control conditions with application of 5% sugarcane press mud (SPM) and the lowest RL (3.89 cm) was recorded in 20 mg/kg Cd stress level without OA (Figure 1). Shoot length was decreased by 33.55% and 45.20% under 10 mg/kg and 20 mg/kg cadmium stress (Figure 1). However, OA showed a marked increase in SL and SPM significantly increased the SL as compared to other OA and control (Figure 1). Cadmium also induced a marked reduction in root and shoot biomass production (Figure 2). The shoot fresh weight (39.95% and 55.64%) and dry weight (4.00% and 13.33%) were decreased at modest (10 mg/kg) and highest (20 mg/kg) Cd stress levels (Figure 2). Similarly, root fresh weight (13.53% and 27.06%), root dry weight (12.19% and 31.70%) was also decreased under 10 and 20 mg/kg Cd stress levels (Figure 2). However, 5% SPM marked increased the root fresh weight (75% and 89%) and dry weight (161% and 173%), respectively, under 10 and 20 mg/kg Cd stress (Figure 2). Cadmium also reduced the leaves production and 5% SMP significantly increased LPP under normal and Cd stress conditions (Figure 1).

3.2. Photosynthetic Pigments

The results indicated that chlorophyll and carotenoids contents significantly decreased under Cd stress (Table 1). The chlorophyll a and chlorophyll b contents decreased by 13.57% and 50.00% and 12.50% and 38.00% at 10 and 20 mg/kg Cd stress as compared to control (Table 1). Similarly, carotenoids contents also showed a reduction of 17.67% and 32.82% at 10 and 20 mg/kg Cd stress levels as compared to control (Table 1). Under the 10 mg/kg of Cd stress, 5% SPM increased chlorophyll a, chlorophyll b and carotenoid contents by 10.84%, 51.47% and 46.19% whereas under 20 mg/kg of Cd stress 5% SPM enhanced the chlorophyll a, chlorophyll b and carotenoid contents by 32.83%, 55.23% and 61.17% as compared control (Table 1).

3.3. Relative Water Contents and Electrolyte Leakage

Cadmium stress showed a marked reduction in relative water contents (RWC); however, electrolyte leakage (EL) significantly increased under f Cd stress (Figure 3). RWC showed a reduction of 16.83% and 60.50% at 10 and 20 mg/kg Cd stress, conversely, EL showed an increase of 17.86% and 45.81% under both Cd stress levels as compared to control (Figure 3). The application of organic amendments improved the RWC and decreased EL. The application of 5% SPM increased the RWC by 44.26% and 67.54% and decreased the EL by 41.61% and 42.66% under modest (10 mg/kg) and strongest (20 mg/kg) Cd stress (Figure 3).

3.4. Hydrogen Peroxide (H2O2) and Malondialdehyde (MDA) Contents

The results indicated that H2O2 contents were increased by 25.35% and 41.56% and MDA contents were increased by 59.93% and 70.10% at 10 mg/kg and 20 mg/kg Cd stress as compared to no Cd stress (Figure 3). The application of AO decreased MDA and H2O2 accumulation. The application of 5% SPM reduced the H2O2 accumulation by 41.65% and 35.39% and MDA accumulation by 63.95% and 47.82% in both levels of Cd stress (10 and 20 mg/kg) as compared to control (Figure 3).

3.5. Anti-Oxidant Activities

Cadmium stress reduced the anti-oxidant activities; however, the application of different OA substantially increased the anti-oxidant activity (Figure 4). The CAT activity was decreased by 5.49% and 25.70% where APX activities were decreased by 15.72% and 30.31% at both levels of Cd stress (10 and 20 mg/kg) (Figure 4). The activities of CAT and APX were significantly enhanced by the application of OA (Figure 4). The application of 5% SPM increased the CAT activities by 40.09% and 41.10% and APX activities by 60.19% and 69.98% under both Cd stress levels (Figure 4). The application of AO markedly also improved the activities of these two anti-oxidants (POD and ascorbic acid); however, 5% SPM remained the top performer in increasing the activities of POD and ascorbic acid activities as compared to other OA (Figure 4).

3.6. Total Soluble Proteins and Free Amino Acids

The mash beans seedling subjected to Cd stress showed a reduction in both total soluble protein (TSP) and free amino acids (FAA) (Figure 5). TSP showed a reduction of 12.87% and 22.77% at 10 mg/kg and 20 mg/kg (Figure 5). All the organic amendments performed well but 5% SPM showed the best results and increased TSP by 67.93% and 52.38% under both Cd stress levels (Figure 5). Likewise, FAA also decreased by 28.16% and 34.69% in both Cd stress levels and the application of 5% SPM produced the best results, followed by a combination of SPM and cow manure (CM) and CM alone, in increasing the FAA contents (Figure 5).

3.7. Yield Traits

The imposition of Cd stress caused a marked reduction in yield components of the mash beans crop (Table 2). The maximum pod length (12.63) and grains per pod (13.33) were recorded in no Cd stress with 5% SPM application followed by the combination of SPM and CM and small pods (7.92 cm) with more seeds (eight) was recorded in maximum Cd stress level (20 mg/kg) without application of OA (Table 2). The Cd stress also imposed a significant reduction in 100-seed weight, seed yield/pot and biological yield/pot (Table 2). A reduction of 16.63% 12.80% was recorded in 100-seed weight under both Cd stress levels (Table 2). Similarly, grain yield/pot also decreased by 18.29% and 33.31% at lower and higher Cd stress levels, while biological yield showed a reduction of 14.59% and 18.23% at 10 and 20 mg/kg Cd stress level (Table 2). The application of 5% SPM increased 100 grain weight (11.28% and 8.41% and), grain yield (13.62% and 20.69%) and biological yield (12.25% and 10.45%) under modest (10 mg/kg) and stronger Cd (20 mg/kg) stress conditions (Table 2).

3.8. Cadmium Concentration Different Plant Parts

The Cd concentration in tested plant parts (root, stem, leave and grain) was significantly increased under Cd stress; however, maximum accumulation of Cd in different plant parts was recorded under stronger Cd levels (20 mg/kg) (Table 3). The maximum Cd concentration in mash beans root (26.13 µg g−1 DW) and stem (12.17 µg g−1 DW) was noted under 20 mg/kg Cd stress without application of OA (Table 3). Conversely, minimum Cd concentration in root (1.70 µg g−1 DW) and stem (1.33 µg g−1 DW) was noted in control (no Cd) with the application of 5% SPM (Table 3). Likewise, maximum Cd concentration in mash beans leaf (9.82 µg g−1 DW) and grain (4.73 µg g−1 DW) was recorded in maximum Cd stress conditions (20 mg/kg) without application of any OA, whereas the lowest Cd concentration in mash beans leaf (0.95 µg g−1 DW) and grain (0.72 µg g−1 DW) was recorded in no Cd stress with the application of 5% SPM (Table 3).

4. Discussion

Cadmium is a highly mobile and very toxic metal that negatively affects plant growth and physiological processes [63]. Cadmium stress significantly reduced the root and shoot growth and biomass production of mash beans plants (Figure 1 and Figure 2). Cadmium stress disturbs plant metabolic processes, nutrient uptake, photosynthetic pigments, biological structures, and anti-oxidant activities which, therefore, reduces the root and shoot growth and subsequent biomass production [64,65]. Additionally, Cd stress also inhibits cell expansion and elongation, which is also a major reason for Cd-induced reduction in root and shoot growth and biomass production (Figure 1 and Figure 2) [66]. Nonetheless, the application of OA including SPM and CM markedly improved the root and shoot growth and biomass production of mash beans plants (Figure 1 and Figure 2) under control and Cd stress. Organic amendments improve soil carbon contents and nutrients uptake which improved the root and shoot growth and biomass production under Cd stress [67,68]. The application of SPM changes soil pH, which increases the binding and sorption sites for Cd immobilization thus induced significant increase in plant growth by reducing Cd availability [31,68,69]. Additionally, OA also reduced the Cd uptake owing to the formation of insoluble phosphorus-Cd complexes (Figure 6) which resultantly enhanced the Cd immobilization and nutrient uptake and increased the root and shoot growth and biomass production under Cd stress [31].
Photosynthesis is an important physiological process; however, Cd stress severely inhibits the photosynthetic process and causes a significant reduction in assimilates production [12,70]. The results indicated that Cd stress induced a serious reduction in chlorophyll and carotenoid contents nonetheless, more reduction was noted under higher Cd stress level (Table 1). Cadmium stress disturbs the Mg uptake which is considered to play a major role in chlorophyll synthesis [71], Moreover, Cd also denatures enzymes responsible for chlorophyll biosynthesis; therefore, Cd-induced reduction in photosynthetic pigments in this study can be attributed to reduced Mg uptake and denaturation of enzymes responsible for chlorophyll biosynthesis [71,72]. Nonetheless, OA particularly, SPM appreciably improved the photosynthetic pigments (Table 1). The application of SPM and CM reduced the Cd uptake (Table 3) which protected the photosynthetic apparatus from the damaging effects of Cd [7,73], resulting in a significant increase in photosynthetic pigments (Table 1). Moreover, OA had beneficial impacts on soil characteristics, and improve root growth, nutrient and water uptake and reduce the Cd uptake (Table 3) which also favors a significant increase in the synthesis of photosynthetic pigments [74].
A significant reduction in the RWC of mash beans plants was recorded with increasing amounts of Cd in growth media (Figure 3). Cadmium toxicity damages the membrane integrity, which increases the water loss and reduces the leaf water status [12]. Nonetheless, application of OA, particularly 5% SPM, appreciably improved the RWC of mash beans plants (Figure 3). Organic amendments improve the anti-oxidant activities which protect the membrane from oxidative damages maintain/increase the leaf water status by preventing water loss [75]. The results indicated that Cd significantly increased the EL, H2O2 and MDA and this increase was more pronounced at a higher level of Cd stress (Figure 1). The increase in EL can be ascribed to reduced membrane permeability and cellular damage caused due to an increase in lipid per-oxidation and H2O2 accumulation, which increased the EL. The application of SPM induced a marked reduction in EL and H2O2 and MDA accumulation (Figure 3). The application of OA significantly increased anti-oxidant activities (Figure 3) which scavenge the ROS and protected membranes from oxidative damage and reduced the EL as indicated by lower MDA accumulation (Figure 3) [27,75].
Cadmium stress significantly reduced the activity of tested anti-oxidant enzymes (CAT, POD, APX and AsA) (Figure 4). The reduction in anti-oxidant activities under Cd stress can be ascribed to inactivation and reduction in synthesis of enzymes and change in the assembly of enzymes subunits [76]. However, the application of OA considerably increased anti-oxidant activities (Figure 4). The improved activities of anti-oxidants help the plants to cope with oxidative stress [77]. The application of OA improves soil fertility and provides favorable conditions for plants which in turn improved anti-oxidant activities [65]. The increase in anti-oxidant activities following the addition of OA reduced ROS (Figure 3), which protects membranes and enhanced the plant’s resistance against stress conditions [27,75]. Proteins and amino acids play various roles in plants; however, the concentration of both TSP and FAA significantly decreased under Cd stress (Figure 5). Cadmium stress increases activity of the protease enzyme which stimulates protein degradation [78], thus resulting in a reduction in TSP accumulation under Cd stress (Figure 5). Cadmium stress also disturbs the amino acid metabolism and amino acids play a crucial role against Cd stress [79]. The application of OA significantly increased the TSP and FAA under Cd stress (Figure 5). The present increase in TSP and FAA by OA can be attributed to improved anti-oxidant activities which protected the proteins and amino acids from damaging effects of Cd thus ensured better protein and amino acid accumulation under Cd stress. However, more studies are direly needed to underpin the mechanism linked with OA induced increase in TSP and FAA under Cd stress.
The Cd concentration in various plant parts significantly increased with increasing the Cd concentration in the growth medium (Table 3). However, the maximum Cd concentration was noted in roots followed by stem, leaves and grains (Table 3). The increase in Cd concentration in mash beans roots can be due to fact roots are the first organ that come in contact with Cd and or due to Cd compartmentalization in root vacuoles [6]. Moreover, the results also indicated a lower Cd concentration in mash beans grain as compared to vegetative parts, which indicate that less Cd was trans-located to the above plant parts. Nonetheless, the application of OA significantly reduced the Cd concentration in roots, stem, leaves and grain (Table 3). Sugarcane press mud increases soil pH and nutrient availability due to the presence of calcium oxide (CaO) and base cations which reduces the Cd toxicity in plants [80]. Because of the alkaline nature of SPM, OH- ions are released into the soil solution, which increases the soil pH and creates binding sites for Cd adsorption and complexation, consequently reduced Cd uptake by plants [81,82,83,84] Moreover, the presence of organic matter present in SPM reduces the Cd uptake and availability by forming organic complexes with Cd [84]; therefore, PMS decreased the Cd accumulation in plant roots and above ground parts (Table 3). The precipitation is considered to be a main mechanism of Cd immobilization as metal-phosphate, owing to the presence of phosphate in OA [32]. This mechanism supports our study where phosphorus enriched SPM might reduce the Cd uptake and accumulation in plants by forming Cd-phosphate complexes. Another possibility was that SPM application could release a good quantity of carbonates, oxides and hydroxides into the soil solution, which increased soil pH and enhanced the Cd precipitation as Cd(OH)2 and CdCO3 [68,85] and this precipitation induced a significant reduction in Cd accumulation in rice plant parts (Table 3). Additionally, SMP also contains an appreciable amount of silicon [86] which considerably immobilizes Cd and reduced Cd uptake and toxic effect on crops [86].
The results indicated that Cd stress induced a serious reduction in yield traits and yield of mash beans crop (Table 2). The reduction in yield and yield contributing under Cd stress can be attributed to combined effects of Cd-induced oxidative stress (Figure 3), reduced photosynthetic pigments (Figure 3), nutrient uptake, accumulation of MDA and H2O2 (Figure 3), protein degradation (Figure 5), and disturbed plant physiological and biochemical processes owing to enhanced Cd uptake. However, OA showed a marked increase in the yield and yield contributing traits under Cd stress (Table 2). The improvement in yield attributes by OA can be attributed to the presence of an appreciable amount of organic matter and nutrients in OA which improve the overall soil fertility and, subsequently, crop production [87,88]. The CM and SPM act as buffers and contain a significant amount of essential nutrients which pointedly increase the crop yield [87]. Moreover, OA could also release nutrients and increase the metals adsorption/participation which tackles the mobility of toxic metals in polluted soils thus improved the growth and yield [87]. Additionally, OA improved photosynthetic activities and anti-oxidant activities, protect the plants from oxidative stress which therefore, reduce the Cd toxicity and improve the growth and yield [28,89,90].

5. Conclusions

In the present study, Cd stress induced a significant reduction in growth and yield attributes of mash beans crop through a reduction in photosynthetic pigments, and increase in Cd uptake and stimulated H2O2 production, electrolyte leakage and MDA accumulation owing to reduction in anti-oxidant activities. However, the application of organic amendments induced a significant increase in growth and yield attributes of mash beans under Cd stress. The application of 5% sugarcane press mud remained the best organic amendment for increasing the growth and yield by inducing an increase in photosynthetic pigments, leaf water status, accumulation of soluble proteins and free amino acids, and by reducing Cd accumulation, H2O2 production, electrolyte leakage and MDA accumulation due to enhanced activities of anti-oxidant enzymes. Thus, these outcomes suggested that sugarcane press mud strengthens the anti-oxidant activities, and alleviates the Cd induced devastating impacts on mash beans crop.

Author Contributions

Conceptualization, M.U.C. and I.K.; methodology, W.A.; investigation, W.A.; writing—original draft preparation, M.U.C., I.K., M.U.H.; writing—review and editing, N.U., M.B.C., S.H.Q., W.S., A.E.S.; Funding Equation, W.S. All authors have read and agreed to the published version of the manuscript.

Funding

The authors extend their appreciation to the Researchers Supporting Project number (RSP-2021/390), King Saud University, Riyadh, Saudi Arabia.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors extend their appreciation to the Researchers Supporting Project number (RSP-2021/390), King Saud University, Riyadh, Saudi Arabia.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Effect of organic amendments on root length (A), shoot length (B), and leaves per plant (C) of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
Figure 1. Effect of organic amendments on root length (A), shoot length (B), and leaves per plant (C) of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
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Figure 2. Effect of organic amendments on root fresh weight (A) root dry weight (B) shoot fresh weight (C) and shoot dry weight (D) of mash beans plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
Figure 2. Effect of organic amendments on root fresh weight (A) root dry weight (B) shoot fresh weight (C) and shoot dry weight (D) of mash beans plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
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Figure 3. Effect of organic amendments on RWC (A), electrolyte leakage (B), MDA (C) and H2O2 (D) contents of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
Figure 3. Effect of organic amendments on RWC (A), electrolyte leakage (B), MDA (C) and H2O2 (D) contents of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
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Figure 4. Effect of organic amendments on CAT (A), POD (B), APX (C) and AsA (D) activities of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
Figure 4. Effect of organic amendments on CAT (A), POD (B), APX (C) and AsA (D) activities of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
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Figure 5. Effect of organic amendments on total soluble protein (A) and free amino acid contents (B) activities of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
Figure 5. Effect of organic amendments on total soluble protein (A) and free amino acid contents (B) activities of mash bean plants subjected to different levels of Cd stress (0, 10 and 20 mg/kg). The vertical bars in each figure are the mean of three replications with ± S.E. and different letters on bars indicating the significant difference at p < 0.05.
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Figure 6. Proposed model for the effect of SPM in reducing the Cd toxicity in mash beans. SPM increases soil pH, Cd precipitation, Cd complexes with organic, anti-oxidant activities, TSP, FAA and RWC, photosynthetic pigments and reduce electrolyte leakage, MDA and H2O2 accumulation and thereby reduce the Cd toxicity in mash beans.
Figure 6. Proposed model for the effect of SPM in reducing the Cd toxicity in mash beans. SPM increases soil pH, Cd precipitation, Cd complexes with organic, anti-oxidant activities, TSP, FAA and RWC, photosynthetic pigments and reduce electrolyte leakage, MDA and H2O2 accumulation and thereby reduce the Cd toxicity in mash beans.
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Table
Table 1. Effect of different organic amendments on photosynthetic pigments of mash bean grown under different levels of Cd stress.
Table 1. Effect of different organic amendments on photosynthetic pigments of mash bean grown under different levels of Cd stress.
Cadmium StressOAChlorophyll a (mg/g FW)Chlorophyll b (mg/g FW)Carotenoid (mg/g FW)
(Control)Control2.13c ± 0.011.40e ± 0.031.60e ± 0.03
CM 5%2.27b ± 0.0091.67d ± 0.051.88c ± 0.06
SPM 5%2.40a ± 0.022.80a ± 0.082.40a ± 0.07
CM 2.5% + SMP 2.5%2.33ab ± 0.022.12c ± 0.122.04b ± 0.02
10 mg/kgControl1.48e ± 0.021.15f ± 0.031.13h ± 0.06
CM 5%1.52e ± 0.0091.32e ± 0.091.54e ± 0.05
SPM 5%1.66d ± 0.022.37b ± 0.092.10b ± 0.07
CM 2.5% + SMP 2.5%1.58de ± 0.0062.14c ± 0.051.76d ± 0.07
20 mg/kgControl0.90h ± 0.090.77g ± 0.60.73i ± 0.08
CM 5%1.13g ± 0.061.08f ± 0.021.25g ± 0.03
SPM 5%1.34f ± 0.061.72d ± 0.111.88c ± 0.04
CM 2.5% +SMP 2.5%1.20g ± 0.0051.37e ± 0.081.44f ± 0.06
OM: Organic amendments, CM: cow manure, SPM: sugarcane press mud. The values given above are the means of three replications with ± S.E and different letter with each mean value indicating the significant difference at p < 0.05.
Table
Table 2. Effect of different organic amendments on yield attributes of mash bean grown under different levels of Cd stress.
Table 2. Effect of different organic amendments on yield attributes of mash bean grown under different levels of Cd stress.
Cadmium StressOAPod Length (cm)Grains/Pod100-Grain Weight (g)Grain Yield/PotBiological Yield/Pot
(Control)Control11.38b ± 0.0710.67bcd ± 0.336.31b ± 0.0640.00bc ± 1.7371.67b ± 1.67
CM 5%11.71b ± 0.1011.00bc ± 0.586.40b ± 0.1143.00b ± 1.0072.33b ± 1.45
SPM 5%12.63a ± 0.1513.33a ± 0.396.90a ± 0.0548.00a ± 1.5380.67a ± 2.19
CM 2.5% + SMP 2.5%12.38a ± 0.1211.67b ± 0.296.72a ± 0.0746.67a ± 0.3378.00a ± 1.53
10 mg/kgControl9.57d ± 0.159.00fgh ± 0.345.11e ± 0.1431.00ef ± 0.5859.00d ± 2.08
CM 5%10.00d ± 0.449.33efg ± 0.265.43d ± 0.0733.33de ± 0.8864.33c ± 1.20
SPM 5%10.87c ± 0.1210.33cde ± 0.275.96c ± 0.0936.67cd ± 2.0367.67bc ± 1.76
CM 2.5% + SMP 2.5%10.57c ± 0.049.67def ± 0.415.67d ± 0.0835.67d ± 1.2066.67c ± 1.20
20 mg/kgControl7.92f ± 0.068.00i ± 0.494.14h ± 0.0422.00i ± 1.0045.67f ± 0.67
CM 5%8.10ef ± 0.157.67hi ± 0.354.37gh ± 0.0724.33hi ± 0.6747.33f ± 1.33
SPM 5%8.80e ± 0.218.33ghi ± 0.324.67f ± 0.01129.33fg ± 1.4554.00e ± 1.00
CM 2.5% + SMP 2.5%8.40f ± 0.258.00hi ± 0.244.45fh ± 0.0726.00gh ± 0.5850.00ef ± 2.89
OA: Organic amendments, CM: cow manure, SPM: sugarcane press mud. The values given above are the means of three replications with ± S.E and different letter with each mean value indicating the significant difference at p < 0.05.
Table
Table 3. Effect of different organic amendments on yield attributes of mash bean grown under different levels of Cd stress.
Table 3. Effect of different organic amendments on yield attributes of mash bean grown under different levels of Cd stress.
Cadmium StressOARoot Cd (µg g−1 DW)Stem Cd (µg g−1 DW)Leaf (µg g−1 DW)Grain Cd (µg g−1 DW)
(Control)Control2.24g ± 1.441.60f ± 0.0871.04h ± 0.0540.89f
CM 5%2.10g ± 1.461.48f ± 0.0601.04h ± 0.0420.83f
SPM 5%1.70g ± 1.921.33f ± 0.0440.95h ± 0.0210.72f
CM 2.5% + SMP 2.5%1.95g ± 1.821.45f ± 0.0211.01h ± 0.0860.78f
10 mg/kgControl17.73d ± 3.2611.17b ± 0.6016.83e ± 0.2033.73d
CM 5%14.87e ± 1.959.96cd ± 0.1256.65e ± 0.1183.64d
SPM 5%11.70f ± 1.718.57e ± 0.4706.21g ± 0.0673.10e
CM 2.5% + SMP 2.5%14.00e ± 8.259.29de ± 0.1626.44fg ± 0.1573.22e
20 mg/kgControl26.13a ± 3.8812.17a ± 0.4419.82a ± 0.0554.73a
CM 5%24.43b ± 2.3711.53ab ± 0.4379.06b ± 0.1424.43b
SPM 5%22.10bc ± 3.8510.73bc ± 0.3938.31d ± 0.0554.10c
CM 2.5% + SMP 2.5%23.17c ± 2.8710.86bc ± 0.1978.69c ± 0.1424.15c
OM: Organic amendments, CM: cow manure, SPM: sugarcane press mud. DW: dry weight. The values given above are the means of three replications with ± S.E and different letter with each mean value indicating the significant difference at p < 0.05.
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Umer Chattha, M.; Arif, W.; Khan, I.; Soufan, W.; Bilal Chattha, M.; Hassan, M.U.; Ullah, N.; Sabagh, A.E.; Qari, S.H. Mitigation of Cadmium Induced Oxidative Stress by Using Organic Amendments to Improve the Growth and Yield of Mash Beans [Vigna mungo (L.)]. Agronomy 2021, 11, 2152. https://doi.org/10.3390/agronomy11112152

AMA Style

Umer Chattha M, Arif W, Khan I, Soufan W, Bilal Chattha M, Hassan MU, Ullah N, Sabagh AE, Qari SH. Mitigation of Cadmium Induced Oxidative Stress by Using Organic Amendments to Improve the Growth and Yield of Mash Beans [Vigna mungo (L.)]. Agronomy. 2021; 11(11):2152. https://doi.org/10.3390/agronomy11112152

Chicago/Turabian Style

Umer Chattha, Muhammad, Warda Arif, Imran Khan, Walid Soufan, Muhammad Bilal Chattha, Muhammad Umair Hassan, Najeeb Ullah, Ayman El Sabagh, and Sameer H. Qari. 2021. "Mitigation of Cadmium Induced Oxidative Stress by Using Organic Amendments to Improve the Growth and Yield of Mash Beans [Vigna mungo (L.)]" Agronomy 11, no. 11: 2152. https://doi.org/10.3390/agronomy11112152

APA Style

Umer Chattha, M., Arif, W., Khan, I., Soufan, W., Bilal Chattha, M., Hassan, M. U., Ullah, N., Sabagh, A. E., & Qari, S. H. (2021). Mitigation of Cadmium Induced Oxidative Stress by Using Organic Amendments to Improve the Growth and Yield of Mash Beans [Vigna mungo (L.)]. Agronomy, 11(11), 2152. https://doi.org/10.3390/agronomy11112152

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