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Article

Alleviation of Cadmium Adverse Effects by Improving Nutrients Uptake in Bitter Gourd through Cadmium Tolerant Rhizobacteria

by
Muhammad Zafar-ul-Hye
1,
Muhammad Naeem
1,
Subhan Danish
1,*,
Shah Fahad
2,3,*,
Rahul Datta
4,*,
Mazhar Abbas
5,
Ashfaq Ahmad Rahi
6,
Martin Brtnicky
4,7,8,
Jiří Holátko
8,
Zahid Hassan Tarar
9 and
Muhammad Nasir
10
1
Department of Soil Science, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan 60000, Pakistan
2
Department of Agronomy, The University of Haripur, Haripur 22620, Pakistan
3
College of Plant Sciences and Technology, Huazhong Agriculture University, Wuhan 430070, China
4
Department of Agrochemistry, Soil Science, Microbiology and Plant Nutrition, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech Republic
5
Institute of Horticultural Sciences, Faculty of Agriculture, University of Agriculture, Faisalabad 38000, Pakistan
6
Pesticide Quality Control Laboratory, Multan 60000, Pakistan
7
Institute of Chemistry and Technology of Environmental Protection, Brno University of Technology, Faculty of Chemistry, Purkynova 118, 62100 Brno, Czech Republic
8
Department of Geology and Pedology, Faculty of Forestry and Wood Technology, Mendel University in Brno, 61300 Brno, Czech Republic
9
Soil and Water Testing Laboratory, Mandi Bahauddin 50400, Pakistan
10
Soil and Water Testing Laboratory for Research, Multan 60000, Pakistan
*
Authors to whom correspondence should be addressed.
Environments 2020, 7(8), 54; https://doi.org/10.3390/environments7080054
Submission received: 16 May 2020 / Revised: 18 July 2020 / Accepted: 22 July 2020 / Published: 26 July 2020
(This article belongs to the Special Issue Soil Contamination by Heavy Metals and Metalloids)
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Abstract

:
Cadmium is acute toxicity inducing heavy metal that significantly decreases the yield of crops. Due to high water solubility, it reaches the plant tissue and disturbs the uptake of macronutrients. Low uptake of nutrients in the presence of cadmium is a well-documented fact due to its antagonistic relationship with those nutrients, i.e., potassium. Furthermore, cadmium stressed plant produced a higher amount of endogenous stress ethylene, which induced negative effects on yield. However, inoculation of 1-amino cyclopropane-1-carboxylate deaminase (ACCD), producing plant growth promoting rhizobacteria (PGPR), can catabolize this stress ethylene and immobilized heavy metals to mitigate cadmium adverse effects. We conducted a study to examine the influence of ACCD PGPR on nutrients uptake and yield of bitter gourd under cadmium toxicity. Cadmium tolerant PGPRs, i.e., Stenotrophomonas maltophilia and Agrobacterium fabrum were inoculated solely and in combination with recommended nitrogen, phosphorus, and potassium fertilizers (RNPKF) applied under different concentration of soil cadmium (2 and 5 mg kg−1 soil). Results showed that A. fabrum with RNPKF showed significant positive response towards an increase in the number of bitter gourds per plant (34% and 68%), fruit length (19% and 29%), bitter gourd yield (26.5% and 21.1%), N (48% and 56%), and K (72% and 55%) concentration from the control at different concentrations of soil cadmium (2 and 5 mg kg−1 soil), respectively. In conclusion, we suggest that A. fabrum with RNPKF can more efficaciously enhance N, K, and yield of bitter gourd under cadmium toxicity.

1. Introduction

High use of pesticides, inorganic fertilizers, and untreated sewage water has significantly contributed to the buildup of heavy metals in agricultural soils [1,2]. These heavy metals become part of soil at the exchange site and remain readily available for plants. Rapid industrialization and anthropogenic activities are also allied factors responsible for the accumulation of toxic metals beyond their threshold limit in cultivatable lands [3,4,5,6]. Among different heavy metals, cadmium (Cd) is an acute toxin due to its high resistance time, i.e., >1000 years and water solubility [7]. Presence of cadmium below 0.5 mg kg−1 soil is considered a safe limit, but depending upon parent material, it can be accumulated up to 3.0 mg kg−1 soil [8]. Being a part of phosphate fertilizers (up to 4.4 mg kg−1), it is easily taken up by crops as Cd-supplement [9,10].
Cadmium causes cardiovascular, respiratory, cancer, and renal, skeletal system in humans when taken up beyond the threshold limit [11,12]. The high concentration of Cd in plant tissues disturbs nutrient uptake and creates water imbalance that results in poor photosynthesis [13]. It also causes lipid membrane instability, alteration in membranes permeability, and chlorosis in plants [14,15]. Due to its divalent nature, it competes with divalent essential nutrients, i.e., P, Ca, Mg, and decreases their uptake in plants [16,17,18]. Bioavailability of K is also affected when Cd is present in higher concentration in soil [19]. Heavy metal toxicity and physiochemical properties soil depend on the land use [20,21,22]. Different crops, the biological adsorption factor (mg Cd/kg plant ash, mg Cd/kg soil) based on Cd content in plant ash, is different, i.e., winter wheat grains (5.97) and straw (2.50), barley grains (4.06) and straw (2.50), sugar beet roots (4.63) and tops (1.41), pea beans (3.22) and straw (0.88), corn grains (8.75) and straw (2.53), soya beans (4.31) and straw (4.63), sunflower seeds (10.8) and stem (4.28) [23]. Moreover, biosynthesis of endogenous stress ethylene under Cd toxicity plays a notorious role that aids in poor root growth [24,25,26].
In addition, ethylene (C2H4) is a plant-signaling molecule. It is involved in seed germination flower senescence, root elongation, fruit ripening, and leaf abscission. Mostly ethylene is synthesized in a two-step process, i.e., (1) enzymatic conversion of S-adenosyl methionine (SAM) to 1-amino cyclopropane-1-carboxylic acid (ACC); (2) conversion of ACC to ethylene, which is catalyzed by ACC-oxidase [27]. However, synthesis of endogenous ethylene level is significantly enhanced upon exposure of plants to abiotic stresses, including low soil fertility [28,29]. This endogenous stress ethylene negatively affects gas exchange attributes, nutrients and water uptake, and yield of different crops under any stress conditions [30,31].
To overcome these problems, inoculation of ACC deaminase producing plant growth promoting rhizobacteria (PGPR), could be an efficacious and nature friendly technique [32,33,34,35,36]. Certain PGPRs can improve growth attributes of crops under heavy metals toxic conditions by secretions of ACC deaminase, siderophores, indole acetic acid, gibberellins, and better availability of water and nutrients [37,38,39,40]. Enzyme ACC deaminase cleaves stress ethylene into intermediate compounds; thus, decreases the stress generating factors in plants [41,42].
Among different crop plants, bitter gourd is a rich source of vitamins, carbohydrates, and proteins [43,44]. As compared to cucumber and tomato, one cup of bitter gourd juice (94 g) has 93% reference daily intake (RDI) of vitamin C [45]. It is cultivated in Pakistan (6107 hectares), with an annual production of 57,190 tons [46]. However, the yield of bitter gourd is negatively affected when cultivated in Cd pollution. As improvement in N, P, and K can mitigate the stress of Cd toxicity in plants [3], which is why the current study was conducted to explore the efficacy of ACC deaminase producing PGPR with recommended NPK fertilizers (RNPKF) on bitter gourd nutrients uptake and yield under Cd toxicity.
The present study aimed to explore (1) effectiveness of rhizobacteria in the improvement of nutrients uptake; (2) effect of nutrients on bitter gourd yield under cadmium-induced stress; (3) correlation of inorganic fertilizer with rhizobacteria on yield and nutrients attributes of bitter gourd under Cd stress. We hypothesized that ACC deaminase-producing PGPRs could improve nutrient uptake and alleviate adverse effects of Cd in bitter gourd for yield improvement.

2. Materials and Methods

2.1. Experimental Site and Treatments

A pot experiment was conducted in the Department of Soil Science research area, Bahauddin Zakariya University, Multan, Pakistan. The soil was characterized as dark brown and saline with JAKHAR soil series [42]. Six treatments were applied in four replication by following two factorial completely randomized designs (CRDs). The treatments were control (without NPK or bacterial strains), recommended NPK fertilizers (RNPKF), Stenotrophomonas maltophilia, Agrobacterium fabrum, RNPKF + S. maltophilia, and RNPKF + A. fabrum. All treatments were added in the soil at 2 and 5 mg Cd kg−1 soil. Artificial toxicity of Cd was developed by using analytical grade salt of CdCl2 [25]. As per treatment plan, two levels of Cd were maintained, i.e., 2 and 5 ppm (mg kg−1 soil), keeping in mind the Cd concentration of pre-experimental soil. Rhizobacteria were inoculated at the time of sowing. However, required fertilizers were applied at the time of pot preparation.

2.2. Collection of Bacterial Strains and Broth

ACC deaminase producing PGPRs S. maltophilia (ACC deaminase activity = 71.78 μmol α- ketobutyrate mg−1 protein h−1) and A. fabrum (ACC deaminase activity = 432.6 µmol α-ketobutyrate mg−1 protein h−1) were taken from the Laboratory of Soil Microbiology, Department of Soil Science. Both PGPRs were documented Cd tolerant previously, i.e., survive over 5.0 mg Cd kg−1 soil toxicity [25]. For seeds inoculation, Dworkin and Foster (DF) media without agar was used for inoculum preparation [47]. Loop of each rhizobacteria was taken in the sterilized flask and incubated at 25 ± 3 °C and 100 rpm for 48 h. After that, broth optical density (OD) was measured by spectrophotometer (540 nm wavelength). Finally, dilution was made with sterilized distilled water to achieve 0.45 nm OD, to achieve a uniform population of 107–108 colony forming units (CFU) mL–1.

2.3. Seeds Sterilization and Sowing

HgCl2 (0.1%) solution was used for sterilization of seeds. All seeds were placed for 5 min in the solution followed by, three times, washing with sterilized deionized water [48]. Moreover, 1mL respective PGPR inoculum was used for seeds inoculation along with sugar (30% sucrose), peat, and clay (1:1) in 1:2:6 ratio for 100 g seeds. Four inoculated seeds were sown in each pot. Sowing of bitter gourd seeds was done by hand. After 20 days of sowing, only three healthy seedlings were maintained in each pot by thinning.

2.4. Irrigation and Fertilizer Application

In pots, 65% field capacity was maintained on a weight basis during the experiment. To fulfil the requirement of crop nutrients (187N, 75P, and 225K kg ha−1) urea, K2HPO4 and K2SO4 were applied.

2.5. Harvesting and Samples Analyses

Harvesting was done at the time of fruit maturity. Samples were digested for the determination of biochemical attributes. The number of bitter gourds was counted manually. For fruit length, standard measuring tape was used. For determination of yield per plant, fruits were collected and weighed on the analytical balance. With the help of diacid mixture nitric acid and perchloric acid (2:1 ratio), the tissues of the plant were digested for P and K analyses [49]. Phosphorus in the samples was determined by using ammonium molybdate and ammonium metavanadate yellow color method [50]. However, for analyses of K in samples, the digested solution was run on flame photometer [51]. For determination of nitrogen, samples were digested in concentrated H2SO4, and digestion mixture (K2SO4 (100):CuSO4.5H2O (10):FeSO4 (1)). Distillation was performed in Kjeldahl distillation apparatus, using boric acid as a collector [52].

2.6. Statistical Analyses

One-way ANOVA was used to assess the effects of treatments. Two factorial ANOVA was conducted separately to compare PGPRs and RNPK interaction under different levels of Cd. Treatment comparison was computed at p ≤ 0.05 by Tukey’s Test.

3. Results

3.1. Number of Bitter Gourds per Plant

Effects of PGPRs and RNPKF under different levels of Cd were significant (p ≤ 0.05) on the number of bitter gourds per plants (BDP). Inoculation of PGPRs and RNPKF have significant main and interactive effects on BDP at 2 and 5 mg kg−1 soil. Application of RNPKF + S. maltophilia, RNPKF + A. fabrum, RNPKF, S. maltophilia and A. fabrum showed significant positive effect over control at 2 and 5 mg Cd kg−1 soil for BDP (Figure 1). Interaction between PGPRs and RNPKF at 2 mg Cd kg−1 soil (Figure 2A) and 5 mg Cd kg−1 soil (Figure 2B) were significant ordinal for BDP (Figure 2B). It was noted that Cd showed non-significant negative correlation (−0.1451; p = 0.3986) with BDP. However, PGPR (0.5863; p = 0.0002) and RNPKF (0.3237; p = 0.0541) showed positive significant correlation with BDP (Figure 3). The maximum increase of 34% and 68% in BDP was observed from control where RNPKF + A. fabrum was applied at 2 and 5 mg Cd kg−1 soil, respectively.

3.2. Bitter Gourd Fruit Length

Effects of PGPRs inoculation and application of RNPKF under various Cd levels were significant (p ≤ 0.05) on bitter gourd fruit length (FL). Application of RNPKF + S. maltophilia and RNPKF + A. fabrum were significantly different from control at 2 and 5 mg Cd kg−1 soil for FL. It was observed that RNPKF showed a positive significantly better response at 2 mg Cd kg−1 soil but remained non-significant at 5 mg Cd kg−1 soil over control for FL (Figure 4). Main effects of PGPRs and RNPKF were significant, but their interaction remained non-significant for FL at 2 and 5 mg kg−1 soil. Disordinal non-significant interaction was found between PGPRs and RNPKF at 2 mg Cd kg−1 soil, but the interaction was non-significant ordinal at 5 mg Cd kg−1 soil for FL. Cadmium showed significant but negative correlation (−0.6399; p = 0.0001) with FL. Inoculation of PGPRs (0.2239; p = 0.1893) gave non-significant positive correlation, while RNPKF (0.3835; p = 0.021) showed positive significant correlation with FL (Figure 5). The maximum increase of 19 and 29% in FL was observed from control where RNPKF + A. fabrum was applied at 2 and 5 mg Cd kg−1 soil, respectively.

3.3. Bitter Gourd Yield per Plant

PGPRs S. maltophilia and A. fabrum and RNPKF under 2 and 5 mg Cd kg−1 soil significantly (p ≤ 0.05) affect bitter gourd yield per plant (YP). At 2 mg Cd kg−1 soil, inoculation of PGPRs has significant main and interactive effects on YP. Application of RNPKF has a significant main effect on YP at 5 mg Cd kg−1 soil. Treatment RNPKF + A. fabrum was significantly different as compared to control at 2 and 5 mg Cd kg−1 soil Cd for YP (Figure 6). It was observed that the interaction of PGPRs and RNPKF was significant ordinal at 2 mg Cd kg−1 soil (Figure 7A) but non-significant ordinal at 5 mg Cd kg−1 soil for YP (Figure 7B). Heavy metal Cd showed significant negative correlation (−0.4385; p = 0.0075) with YP. However, PGPRs (0.5035; p = 0.0017) and RNPKF (0.3829; p = 0.0212) showed positive significant correlation with YP (Figure 8). The maximum increase of 26.5 and 21.1% in YP was observed from control, where RNPKF + A. fabrum was applied at 2 and 5 mg Cd kg−1 soil, respectively.

3.4. Nitrogen Concentration in Bitter Gourd

PGPRs and RNPKF significantly (p ≤ 0.05) changed the nitrogen concentration of bitter gourd (NB) under different levels of Cd. Main effects of PGPRs and RNPKF were significant on NB at 2 and 5 mg kg−1 soil. However, the interaction of PGPRs and RNPKF was non-significant, ordinal at 2 and 5 mg Cd kg−1 soil for NB. It was observed that RNPKF + S. maltophilia and RNPKF + A. fabrum were significantly different as compared to control at 2 and 5 mg Cd kg−1 soil for NB (Figure 9). Heavy metal Cd showed significant negative correlation (−0.4812; p = 0.0030) with NB. However, PGPRs (0.4391; p = 0.0074) showed significant and RNPKF (0.2041; p = 0.2324) showed non-significant positive correlation with NB (Figure 10). The maximum increase of 48 and 56% in NB was observed from control where RNPKF + S. maltophilia was applied at 2 and 5 mg Cd kg−1 soil, respectively.

3.5. Phosphorus Concentration in Bitter Gourd

Effect of PGPRs and RNPKF under 2 and 5 mg kg−1 soil was significant (p ≤ 0.05) on phosphorus concentration of bitter gourd (PB). Treatments RNPKF, RNPKF + S. maltophilia, RNPKF + A. fabrum, and RNPKF differed significantly at 5 mg Cd kg−1 soil over control for PB (Figure 11). Application of RNPKF and PGPRs showed a significant main effect on PB at 2 mg Cd kg−1 soil. At 5 mg Cd kg−1 soil, PGPRs and RNPKF have a significant main and interactive effect on PB. Ordinal interaction was found between PGPRs and RNPKF at 2 mg Cd kg−1 soil but significant ordinal interaction was observed at 5 mg Cd kg−1 soil (Figure 12A,B) for PB. Cadmium showed a significant negative correlation (−0.6614; p = 0.0001) with BDP. However, PGPR (0.2537; p = 0.1953) showed non-significant and RNPKF (0.4422; p = 0.0069) showed significant positive correlation with PB (Figure 13). The maximum increase of 29.5% in PB was observed from control where RNPKF + A. fabrum was applied at 2 mg Cd kg−1 soil.

3.6. Potassium Concentration in Bitter Gourd

Influence of PGPRs and RNPKF 2 and 5 mg kg−1 soil was significant (p ≤ 0.05) on potassium concentration of bitter gourd (KB). It was also observed that RNPKF + S. maltophilia and RNPKF + A. fabrum differed significantly for KB at 5 mg Cd kg−1 soil (Figure 14). Both PGPRs and RNPKF have a significant main effect on KB at 2 and 5 mg Cd kg−1 soil. Disordinal non-significant interaction was found between PGPRs and RNPKF at 2 mg Cd kg−1 soil and but ordinal interaction was observed at 5 mg Cd kg−1 soil for KB. Different levels of Cd showed significant negative correlation (−0.4904; p = 0.0024) with KB. However, PGPR (0.5516; p = 0.0005) and RNPKF (0.3840; p = 0.0208) showed significant positive correlation with KB (Figure 15). Application of RNPKF + S. maltophilia, RNPKF + A. fabrum, RNPKF, S. maltophilia and A. fabrum were significantly different as compared to control at 2 mg Cd kg−1 soil for KB. The maximum increase of 72 and 55% in KB was observed from control where RNPKF + A. fabrum was applied at 2 and 5 mg Cd kg−1 soil, respectively.

4. Discussion

A significant decrease in fruit length, fresh weight, and yield per plant of bitter gourd were observed in control at 5 mg Cd kg−1 soil. Low uptake of N, P, and K in bitter gourd under Cd toxicity might be a major factor for reduction in yield, fruit length, and fresh weight. Higher biosynthesis of stress ethylene might be an allied factor responsible for a significant decline in yield of bitter gourd under Cd stress. According to Sanita di Toppi and Gabbrielli [7], accumulation of Cd beyond safe limit disturbed the nutrients homeostasis which played an imperative role in reduction of root and shoot elongation. Cadmium in plants also competes with divalent nutrients ions and decreases their uptake in plants [16]. Under Cd toxicity, transmembrane carriers in roots become unable to distinguish between non-essential Cd and essential divalent nutrients during their uptake [53,54]. Glick et al. [55] also documented that biosynthesis of endogenous stress ethylene under abiotic stress conditions, negatively affects the productivity of the crop. Toxicity of heavy metals causes abnormal division of cell thus induced chromosomal aberration in plants [56]. This resulted in a decrease of protochlorophyllide reductase activity. Such disturbance in plants also induced chlorosis in leaves [57]. Furthermore, Matile et al. [58] suggested the decomposition of lipids in cell wall when ethylene concentration is increased. They argued that ethylene when contact with chlorophyllase (chlase) gene it degrades chlorophyll caused in chlorosis. Furthermore, application of RNPKF + A. fabrum differed significantly better from the sole application of control for improvement in N, P and K. The improvement in N, P, and K mitigate the adverse impacts of Cd in bitter gourd. Panković et al. [59] observed that improvement in N uptake of sunflower alleviants the inhibitory influences of Cd [22,23,27,28,32]. Higher N facilitates in activity of Rubisco by an increase in soluble protein contents. Application of N in NH4 form is efficacious in decreasing the Cd uptake due to antagonistic relationship [60]. Findings of the current experiment also support the above argument. Better N in bitter gourd was observed where yield was improved over control even under Cd toxicity. Under Cd stress, plants start producing N metabolites, i.e., proline that causes phytochelation and decreases the intake of Cd [61]. Application of phosphorus neutralizes the adverse impacts of Cd and improve the yield of crops [62]. Improvement of P uptake in plants enhances the synthesis of glutathione that prevents membrane damages caused by Cd [63]. Balance K concentration decreases the generation of reactive oxidative species (ROS) and inhibits the NADPH oxidase [64]. Moreover, less generation of stress ethylene by inoculation of A. fabrum and RNPKF + A. fabrum might be another major factor responsible for the enhancement in bitter gourd growth and yield in the current study. Both PGPRs were capable to produce ACC deaminase, which cleaves ethylene into intermediate compounds. Similar kinds of results were also documented by many scientists [25,26,30,31]. Glick et al. [44] proposed that enzyme ACC deaminase break ethylene into α-ketobutyrate and ammonia [65,66]. Accumulated ethylene in roots moved towards rhizosphere; thus, ethylene becomes low in plant roots, and stress is alleviated. Similarly, Tripathi et al. [67] reported growth hormones, indole acetic acid, improved the root elongation for better uptake of nutrients [24].

5. Conclusions

It is concluded that PGPR, A. fabrum has more potential over S. maltophilia to alleviate Cd induced stress in bitter gourd. Inoculation of A. fabrum with RNPKF is an efficacious approach to improve N, P, and K concentration in bitter gourd. The combined use of RNPKF and A. fabrum can increase the number of bitter gourds per plant, bitter gourd fruit length, and yield per plant by alleviating 5 mg Cd kg−1 soil induced toxicity. However, more investigations are suggested at field level to declare A. fabrum + RNPKF as an efficacious technique to mitigate Cd stress in bitter gourd.

Author Contributions

M.Z.-u.-H. and S.D. designed and supervised the experiment and wrote the manuscript; M.N. (Muhammad Naeem) conducted research, collected data; S.D., M.B., J.H., and R.D. wrote the manuscript and conducted statistical analyses; S.F., M.A., A.A.R., Z.H.T., and M.N. (Muhammad Nasir) assisted in the preparation of manuscript and reviewed manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Acknowledgments

This research article is part of Muhammad Naeem Thesis for the award of M.Sc. Hons. Agriculture (Soil Science) Degree.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Number of bitter gourds per plant (BDP) treated with plant growth promoting rhizobacteria (PGPRs), recommended NPK fertilizers (RNPKF), and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
Figure 1. Number of bitter gourds per plant (BDP) treated with plant growth promoting rhizobacteria (PGPRs), recommended NPK fertilizers (RNPKF), and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
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Figure 2. Interaction graph of S. maltophilia (NS1), A. fabrum (NS2), and RNPKF at 2 (A) and 5 mg Cd kg−1 soil (B) for number of bitter gourd per plant (BDP).
Figure 2. Interaction graph of S. maltophilia (NS1), A. fabrum (NS2), and RNPKF at 2 (A) and 5 mg Cd kg−1 soil (B) for number of bitter gourd per plant (BDP).
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Figure 3. Pearson correlation of Cd, PGPRs, and RNPKF for number of bitter gourd per plant (BDP). * = significant (p ≤ 0.05); ns = non-significant.
Figure 3. Pearson correlation of Cd, PGPRs, and RNPKF for number of bitter gourd per plant (BDP). * = significant (p ≤ 0.05); ns = non-significant.
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Figure 4. Bitter gourd fruit length (cm) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences at p ≤ 0.05.
Figure 4. Bitter gourd fruit length (cm) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences at p ≤ 0.05.
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Figure 5. Pearson correlation of Cd, PGPRs, and RNPKF for fruit length (FL). * = significant (p ≤ 0.05); ns = non-significant.
Figure 5. Pearson correlation of Cd, PGPRs, and RNPKF for fruit length (FL). * = significant (p ≤ 0.05); ns = non-significant.
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Figure 6. Bitter gourd yield (kg) per plant treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences at p ≤ 0.05.
Figure 6. Bitter gourd yield (kg) per plant treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences at p ≤ 0.05.
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Figure 7. Interaction graph of S. maltophilia (NS1), A. fabrum (NS2), and RNPKF at 2 (A) and 5 mg Cd kg−1 soil (B) for bitter gourd yield per plant (YP).
Figure 7. Interaction graph of S. maltophilia (NS1), A. fabrum (NS2), and RNPKF at 2 (A) and 5 mg Cd kg−1 soil (B) for bitter gourd yield per plant (YP).
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Figure 8. Pearson correlation of Cd, PGPRs, and RNPKF for yield per plant (YP)* = significant (p ≤ 0.05); ns = non-significant.
Figure 8. Pearson correlation of Cd, PGPRs, and RNPKF for yield per plant (YP)* = significant (p ≤ 0.05); ns = non-significant.
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Figure 9. Nitrogen concentration in bitter gourd (%) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
Figure 9. Nitrogen concentration in bitter gourd (%) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
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Figure 10. Pearson correlation of Cd, PGPRs, and RNPKF for bitter gourd nitrogen concentration (NB) * = significant (p ≤ 0.05); ns = non-significant.
Figure 10. Pearson correlation of Cd, PGPRs, and RNPKF for bitter gourd nitrogen concentration (NB) * = significant (p ≤ 0.05); ns = non-significant.
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Figure 11. Phosphorus concentration in bitter gourd (%) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
Figure 11. Phosphorus concentration in bitter gourd (%) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
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Figure 12. Interaction graphs of S. maltophilia (NS1), A. fabrum (NS2), and RNPKF at 2 (A) and 5 mg Cd kg−1 soil (B) for phosphorus concentration in bitter gourd (PB).
Figure 12. Interaction graphs of S. maltophilia (NS1), A. fabrum (NS2), and RNPKF at 2 (A) and 5 mg Cd kg−1 soil (B) for phosphorus concentration in bitter gourd (PB).
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Figure 13. Pearson correlation of Cd, PGPRs, and RNPKF for bitter gourd phosphorus concentration (NB). * = significant (p ≤ 0.05); ns = non-significant.
Figure 13. Pearson correlation of Cd, PGPRs, and RNPKF for bitter gourd phosphorus concentration (NB). * = significant (p ≤ 0.05); ns = non-significant.
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Figure 14. Potassium concentration in bitter gourd (%) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
Figure 14. Potassium concentration in bitter gourd (%) treated with PGPRs, RNPKF, and their combination under 2 and 5 mg Cd kg−1 soil. Different small letters express significant differences (p ≤ 0.05).
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Figure 15. Pearson correlation of Cd, PGPRs, and RNPKF for bitter gourd potassium concentration (NB). * = significant (p ≤ 0.05); ns = non-significant.
Figure 15. Pearson correlation of Cd, PGPRs, and RNPKF for bitter gourd potassium concentration (NB). * = significant (p ≤ 0.05); ns = non-significant.
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Zafar-ul-Hye, M.; Naeem, M.; Danish, S.; Fahad, S.; Datta, R.; Abbas, M.; Rahi, A.A.; Brtnicky, M.; Holátko, J.; Tarar, Z.H.; et al. Alleviation of Cadmium Adverse Effects by Improving Nutrients Uptake in Bitter Gourd through Cadmium Tolerant Rhizobacteria. Environments 2020, 7, 54. https://doi.org/10.3390/environments7080054

AMA Style

Zafar-ul-Hye M, Naeem M, Danish S, Fahad S, Datta R, Abbas M, Rahi AA, Brtnicky M, Holátko J, Tarar ZH, et al. Alleviation of Cadmium Adverse Effects by Improving Nutrients Uptake in Bitter Gourd through Cadmium Tolerant Rhizobacteria. Environments. 2020; 7(8):54. https://doi.org/10.3390/environments7080054

Chicago/Turabian Style

Zafar-ul-Hye, Muhammad, Muhammad Naeem, Subhan Danish, Shah Fahad, Rahul Datta, Mazhar Abbas, Ashfaq Ahmad Rahi, Martin Brtnicky, Jiří Holátko, Zahid Hassan Tarar, and et al. 2020. "Alleviation of Cadmium Adverse Effects by Improving Nutrients Uptake in Bitter Gourd through Cadmium Tolerant Rhizobacteria" Environments 7, no. 8: 54. https://doi.org/10.3390/environments7080054

APA Style

Zafar-ul-Hye, M., Naeem, M., Danish, S., Fahad, S., Datta, R., Abbas, M., Rahi, A. A., Brtnicky, M., Holátko, J., Tarar, Z. H., & Nasir, M. (2020). Alleviation of Cadmium Adverse Effects by Improving Nutrients Uptake in Bitter Gourd through Cadmium Tolerant Rhizobacteria. Environments, 7(8), 54. https://doi.org/10.3390/environments7080054

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