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. 2024 Apr 12;30(4):605–618. doi: 10.1007/s12298-024-01446-5

Effects of mycorrhizal symbiosis and Ulva lactuca seaweed extract on growth, carbon/nitrogen metabolism, and antioxidant response in cadmium-stressed sorghum plant

Anass Kchikich 1,2,✉, Zoulfa Roussi 1, Azzouz Krid 6, Nada Nhhala 1, Abdelhamid Ennoury 1, Bouchra Benmrid 3, Ayoub Kounnoun 4, Mohammed El Maadoudi 5, Naima Nhiri 7, Nhiri Mohamed 1
PMCID: PMC11087393  PMID: 38737317

Abstract

In our study on the effect of cadmium (Cd) toxicity (200 µM) on the growth of Sorghum bicolor (L.) Moench plants, cultivated with arbuscular mycorrhizal fungi (AMF) (Glomus intraradices) and/or under seaweed treatment (3% Ulva lactuca extract) (U. lactuca), we found that AMF increased the tolerance of sorghum to cadmium stress, either alone or in combination with the seaweed treatment. Morphological parameters were higher in these two culture conditions, with increased chlorophyll content. AMF reduced Cd accumulation in roots and inhibited its translocation to the aerial part, while seaweed treatment alone significantly increased Cd accumulation in leaves and roots without affecting plant growth compared to stressed witnesses. Treatment with AMF and/or U. lactuca attenuated oxidative stress, measured by activation of superoxide dismutase, and resulted in a significant decrease in malondialdehyde and superoxide ions (O2−) in treated plants. Furthermore, it induced significant alterations in carbon and nitrogen metabolic pathways, with a significant increase in the activity of enzymes such as glutamine synthetase, glutamate synthase (GOGAT), glutamate dehydrogenase, phosphoenolpyruvate carboxylase, aspartate aminotransferase and isocitrate dehydrogenase in the leaves of each treated plant. These results confirm that AMF, U. lactuca algae extract and their combination can improve the biochemical parameters of sorghum under Cd stress, through modification of the antioxidant response on one hand, and improved nitrogen absorption and assimilation efficiency on the other.

Keywords: Sorghum, Cadmium, Carbon nitrogen enzymes, Ulva lactuca, Mychorrizal plants, Mycorrhiza-Ulva synergy

Introduction

Sorghum is a cereal of significant interest due to its ability to adapt to current environmental challenges through its physiological and metabolic characteristics (Hadebe et al. 2017). However, the intensification of anthropogenic activities has led to heavy metal pollution in urban and agricultural soils worldwide (Zhang and Wang 2020), which can disrupt sorghum growth, causing chlorosis and root growth inhibition, thereby reducing nutrient assimilation, photosynthesis, and carbon and nitrogen metabolism (Zulfiqar et al. 2019). High concentrations of Cd can also lead to plant death (Hatamian et al. 2019). It contributes to increased oxidative stress at the cellular level, manifested by increased lipid peroxidation, hydrogen peroxide (H2O2) generation, and ion leakage (Anjum et al. 2011).

Plants combat metal stress by developing potential mechanisms such as selective immobilization of heavy metals at the root level, efflux of heavy metals, intracellular chelation of metal complexes with phytochelatins, and compartmentalization in vacuoles (Sharma and Chakraverty 2013). The synergistic interaction of plants with soil microorganisms also plays a crucial role in enhancing plant resistance mechanisms against abiotic stress.

AMF are important ecological partners in agroecosystems, forming symbiotic associations with many vascular plant species. The impact of AMF on reducing heavy metal (HM) stress in plants growing in metal-contaminated soils has been extensively studied and well recognized (Riaz et al. 2021). It has been shown that the association between mycorrhizal fungi and metal-stressed host plants provides improved nutritional status and reduced or altered heavy metal uptake (Bisht et al. 2022). Furthermore, AMF enhances the performance of host plants under metal stress conditions through physiological changes (Riaz et al. 2021). However, the mechanisms of HM detoxification by AMF in host plants are not yet fully understood, and debatable results are obtained depending on specific plant/fungus/metal species interactions (Andrade et al. 2010). AMF are also known for their positive effects in enhancing tolerance to oxidative stress, resulting in better protection of host plants. It has been demonstrated that plants infected with AMF show overactivation of enzymes and antioxidant compounds, which plays a crucial role in improving stress tolerance by increasing the antioxidant capacity of plants (El Defrawy and Hesham 2020).

On the other hand, naturally derived plant growth stimulants are a source of great interest. Indeed, raw materials such as algal biomass leading to the synthesis of plant biostimulants have garnered particular attention (Calvo et al. 2014). Natural products based on algal extracts, especially their application as biostimulants in sustainable agriculture, have received significant interest (Tuhy et al. 2013). These natural products are known to have competitive efficacy in removing HM from simulated and raw wastewater (Foday et al. 2021). From an agricultural perspective, the beneficial properties of using algae stem from their living conditions constantly confronted with biotic and abiotic stresses. These stress conditions have contributed to the development of algae protection mechanisms against various types of stress. Algal cells contain high levels of bioactive compounds such as carbohydrates, minerals, trace elements, growth hormones, betaines, and sterols, which are capable of protecting plants (Tuhy et al. 2013).

To better understand the effect of AMF (G. intraradices) and U. Lactuca on sorghum growth under stress conditions, physiological alterations, activities of key enzymes involved in nitrogen and carbon assimilation, and antioxidant response were studied.

Materials and methods

Plant material, experimental treatments, and growth conditions

The seeds of the Moroccan sorghum ecotype (4p11) (Sorghum bicolor L.) were sterilized with 5% NaOCl for 15 min and washed thoroughly with sterile water. The plants were then grown under simulated field conditions in pots containing vermiculite in a growth chamber. The temperature was 28 °C during the day and 21–22 °C at night, with a photoperiod of 16 h of light and 8 h of darkness. Five culture conditions were studied. Before sowing, vermiculite was mixed with AMF (Glomus intraradices).

Cadmium was added to the nutrient solution at a concentration of 200 µM. Control plants were grown without Cd, AMF, or U. Lactuca. Five treatment conditions were performed and are summarized in Table 1.

Table 1.

Description of the conditions studied

Condition Control (−) Control (+) Cd AMF + Cd U. lactuca + Cd U. lactuca + AMF + Cd
Pot number 1 2 3 4 5
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A treatment with nitrogen in the form of potassium nitrate (KNO3) was carried out at 5 mM as optimum concentration for sorghum growth. A nutrient solution marketed from the Sigma-Aldrich company, composed of KNO3 5 mM, KH2PO4 0.375 mM, K2HPO4 0.125 mM, MgSO4 0.375 mM, CaSO4 1.25 mM and NaCl 0.1 mM and micronutrients (Ben Mrid et al. 2018), was provided one week after seed germination and applied twice a week. Leaves and roots were harvested from 4-week-old plants and stored at − 80 °C until use. The experiment was repeated six times under the same conditions.

The Glomus intraradices fungus was marketed by Agrogeniaas a solution containing the spores and inoculated by applying a quantity of 12 g of the solution to each pot containing the seeds grown in vermiculite.

Leaves were harvested from 5-week-old plants, frozen in liquid nitrogen, and stored at − 80 °C until analysis.

Determination of total protein and chlorophyll

Total proteins content were estimated according to Ben Mrid et al. (2018) using BSA as the standard.

Total Chlorophyll content was estimated according to Kchikich et al. (2021a).

Glutamine synthetase, glutamate dehydrogenase, and aspartate aminotransferase assays

Glutamine synthetase activity was measured using the protocol described by (Ben Mrid et al. 2018). Glutamate dehydrogenase activity, and AAT activity was measured using the method described by Kchikich et al. (2021b).

Phosphoenolpyruvate carboxylase and NADP + -Isocitrate dehydrogenase assays

PEPC and NADP+-ICDH activity were measured as described by (Benmrid et al. 2018).

Superoxide dismutase assays

Superoxide dismutase (SOD) enzyme activity (EC 1.15.1.1) was determined using the protocol established by (Roussi et al. 2022).

Determination of MDA and O2− content

The MDA content in the leaves of the plants was revealed according to the protocol of Bouchmaa et al. (2019) with some modifications.

The content of superoxide ions (O2−) was estimated following the protocol described by Roussi et al. (2022).

Estimation of mycorrhiza presence

Unpigmented roots of the sorghum plant were cleaned by heating (90 °C for 1 h) in 10% KOH, then rinsed and acidified with dilute HCL and stained by simmering (5 min) in Trypan Blue in Lactophenol as described by Kchikich et al. (2021b). Root mycorrhization was estimated by Motic optical microscopy, B3 range (Hong Kong, China).

Determination of cadmium content

Reagents and chemicals

69% nitric acid, 35% hydrogen peroxide from Panreac (Barcelona, Spain). Ultrapure water was purified by a Purelab Ultra System (ELGA LabWater, Wycombe, United Kingdom).

Determination of cadmium concentration

Speedwave XPERT microwave digestion system was used to prepare dried leaves and root samples. 250 mg of the homogenized samples were weighed into a digestion vessel. Then, 5.0 mL and 3.0 mL of HNO3 and H2O2 were added, respectively. Next, the digestion was performed according to the following program (Table 2).

Table 2.

Description of the digestion program

Temperature program Step T (°C) P (bar) Ta (min) Time (min) Power (%)
1 150 30 10 5 50
2 190 35 5 15 80
3 50 25 1 10 0
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Once the digestion was completed, the vessels were cooled to room temperature (about 20 min), then carefully opened in the fume hood. Clear solution of each digested sample was added into 50 mL polypropylene tubes; then, the volume was brought to 50 mL with ultrapure water.

The analysis was carried out by a graphite furnace atomic absorption spectrometry SAA600 equipped with AS 800 autosampler (PerkinElmer, USA) and argon gas. The signals were measured at 228.8 nm with electrodeless discharge lamp, and the analysis were performed in duplicate.

Statistical analyses

Data are mean ± S.D. Results were subjected to one-way analysis of variance (ANOVA) followed by Tukey's test using PASW statistics (version 18). Different letters indicate significant differences in the ten N treatments at the 5% level. *, and indicate a significant difference between the two varieties at the same level of N at P < 0.05, P < 0.01, and P < 0.001, respectively. Six biological and technical repetitions were made for each test.

Results

Root colonization

In this experiment, we observed significant root colonization rate (88%) by the AMF G. intraradices used in the form of spores, by applying 12 g of the solution containing the spores to each pot at a distance not exceeding 2 cm from the seeds grown in vermiculite, both in the presence and absence of U. Lactuca treatment (Fig. 1). There was no apparent effect of Cd treatment on G. intraradices colonization rates. On the other hand, the sensitivity of G. intraradices to algal treatment was not revealed.

Fig. 1.

Fig. 1

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An observation of colonization of roots by AMF; a colonized roots, b normal roots (scale bars ×50)

Growth parameter

Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05.

Table 3 presents the results of the morphological parameters studied in the leaves of sorghum grown under different conditions. Leaf length was the greatest in plants treated with AMF alone, followed by the control plants treated with water only, then the combination of AMF and U. lactuca, and finally, U. lactuca treatment alone. Plants grown in the presence of cadmium alone showed the lowest leaf length (Fig. 2).

Table 3.

Morphological parameters and chlorophyll content of sorghum leaves under the different studied conditions

Control (−) Control (+) Cd AMF + Cd U. lactuca + Cd U. lactuca + AMF + Cd
Shoot length (cm) 40 ± 1.52ab 22 ± 2.51c 42 ± 2a 28 ± 1.52c 35 ± 3.05b
Fresh weight (g) 1.11 ± 0.04a 0.29 ± 0.02e 0.85 ± 0.02b 0.38 ± 0.02d 0.77 ± 0.02c
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Fig. 2.

Fig. 2

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Influence of AMF and U. lactuca on sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd

For fresh leaf weight, control plants grown in the absence of cadmium present the greatest weight (1.11 g), followed by plants grown with cadmium in the presence of AMF alone (0.85 g), and then plants stressed by cadmium in the presence of AMF and U. lactuca (0.38 g). In the presence and absence of U. lactuca, plants grown with cadmium showed the lowest fresh weights of 0.38 and 0.29 g, respectively.

Carbon/nitrogen enzyme assays

In this study, we observed that plants treated with AMFs in the presence of Cd (200 µM) increased GS activity in sorghum leaves to 35.37 µmol/min, which was the highest among all the treatments (Fig. 3). In addition, the results showed that U. lactuca extract alone or combined with AMF increased GS activity in stressed plants’ leaves compared to Cd control plants (Fig. 3). On the other hand, sorghum plants grown in the presence of Cd alone presented the lowest GS activity (7.4 µmol/min) (Fig. 3).

Fig. 3.

Fig. 3

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Influence of AMF and U. lactuca on glutamine synthetase (GS) activity in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

GDH activity increased from 207.83 µmol/min in the control plants to 290.6 mmol/min in Cd-stressed plants not treated with any biostimulant (Fig. 4). Moreover, treatment of sorghum plants with AMF and/or U. lactuca extract influenced GDH activity positively in the leaves. In fact, AMF + U. lactuca extract gave the highest GDH activity as it reached 648.2 µmol/min (Fig. 4). Foliar application of U. lactuca was also effective in increasing GDH activity to 403.5 µmol/min (Fig. 4).

Fig. 4.

Fig. 4

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Influence of AMF and U. lactuca on glutamate dehydrogenase (GDH) activity in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

The PEPC activity in sorghum leaves growth conditions was assayed (Fig. 5). The treatment of plants with cadmium decreased the PEPC activity in the leaves, which presented the lowest value out of all the studied conditions (185.96 µmol/min). The control plants (water only) showed a strong activity compared to the stressed plant without biostimulants (772.47 µmol/min). Treatment of cadmium-stressed plants with AMF, U. lactuca, and AMF + U. lactuca increased PEPC activity to 606.76, 556.7, and 865.1 µmol/min, respectively, compared to Cd-stressed plants (Fig. 5).

Fig. 5.

Fig. 5

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Influence of AMF and U. lactuca on phosphoenolpyruvate carboxylase (PEPC) activity in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

Figure 6 reports the NADH-MDH activity in plants treated with different types of biostimulant/biofertilizer in the presence and/or absence of Cd. In the presence of AMFs, whether as a single treatment or in synergy with U. lactuca, there was a significant increase in this activity in sorghum leaves, this increase was more pronounced under AMF with U. lactuca, and reached its highest in this treatment condition. This activity was also induced by the single supply of AMFs where the NADH-MDH increased significantly, the NADH-MDH activity was lower compared to the control plants and reached the lowest value obtained, the plants’ treatment by Cd led to a small increase in this activity compared to the control plants (Fig. 6).

Fig. 6.

Fig. 6

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Influence of AMF and U. lactuca on phosphoenolpyruvate carboxylase (NAD+-MDH) activity in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

The ICDH activity in sorghum leaves was calculated, and the result obtained showed that this activity increased to 6.4, 8.97, and 11.79 µmol/min under treatment with AMF, U. lactuca, and AMF combined with U. lactuca, respectively, in the presence of Cd, compared to plants stressed by cadmium without biostimulant (3.39 µmol/min) (Fig. 7).

Fig. 7.

Fig. 7

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Influence of AMF and U. lactuca on isocitrate dehydrogenase (ICDH) activity in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

The AAT activity in sorghum leaves was calculated, and Fig. 8 presents an important influence of this activity by biostimulants in case of stress. AAT presented a value of 883.82 µmol/min in the control plants, and the treatment of the sorghum plants with cadmium decreased this value to 605.1 µmol/min. AMF, U. lactuca, and AMF + U. lactuca in the presence of cadmium increased AAT activity to 996, 1281, and 1395.2 µmol/min, respectively, compared to the cd control (605.1 µmol/min) (Fig. 8).

Fig. 8.

Fig. 8

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Influence of AMF and U. lactuca on aspartate aminotransferase (AAT) activity in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

The total chlorophyll content in the five conditions shows that cadmium stress decreases the chlorophyll content in the leaves (20.57 µg/g FW), compared to the control plant (29 µg/g FW) (Fig. 9). However, AMF alone increased the total chlorophyll content despite the presence of cadmium (28.01 µg/g FW). Foliar treatment with U. lactuca alone and combined with AMF showed a significant decrease in total chlorophyll content; 15.78 and 11.80 µg/g FW, respectively, compared to the Cd control (Fig. 9).

Fig. 9.

Fig. 9

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Influence of AMF and U. lactuca on chlorophyll content in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

Cd-induced oxidative stress

In the present study, malondialdehyde (MDA), an indicator of lipid peroxidation, showed a substantial increase of 1816% in Cd-stressed plants compared to control plants (Fig. 10). Treatment of plants with AMFs alone or in synergy with U. Lactuca significantly reduced the Cd-induced increase in MDA, with 58% and 116%, respectively. On the other hand, foliar spraying using U. lactuca showed low efficiency in reducing the MDA content. An increase of 525% was recorded compared to the control plant (Fig. 10).

Fig. 10.

Fig. 10

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Influence of AMF and U. lactuca on MDA (a) and O2− (b) content in sorghum shoots growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

The O2− superoxide radical formation had the same evolutionary trend as the MDA content (Fig. 10). A 296% increase was recorded in Cd-stressed control plants. AMF inoculation, as a single treatment and in synergy with U. lactuca, led to a strong reduction in O2− accumulation in plants grown under Cd toxicity; an increase of 18% and 32%, respectively, was recorded compared to the control plants, however U. lactuca in single treatment presented an increase of 227% compared to the control plants (Fig. 10).

Superoxide dismutase assays

Figure 11 shows that plants treated with the synergy of AMF and U. lactuca had the highest enzymatic activity compared to control plants (untreated and unstressed). However, there was no remarkable difference between the plants treated only with U. lactuca extract and those inoculated with AMFs; the two conditions showed an increase of 4% and 10%, respectively, compared to the non-control plants. Stressed plants showed the lowest value of this activity; a 23% decrease was recorded compared to unstressed control plants.

Fig. 11.

Fig. 11

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Influence of AMF and U. lactuca on SOD activity in shoots of sorghum growing under Cd stress (200 µM). 1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd. Each value represents the mean of three or four independent observations ± SD. Means with the same letter are not significantly different at p ≥ 0.05

Cadmium dosage

The control plants show an absence of Cd content in the leaves and a negligible amount in the roots. AMFs play a vital role in blocking and inhibiting the rise of cadmium to the leaves, whether alone or in combination with U. lactuca (Table 4).

Table 4.

Cadmium content in the leaves and roots of sorghum under treatments with AMF and U. lactuca

Cadmium content ppm 1 2 3 4 5
Shoots 0.94 ± 0.39b 58.88 ± 0.64a 1.03 ± 0.21b 72.88 ± 1.49a 1.066 ± 0.45b
Roots 2.08 ± 0.05d 72.13 ± 0.89ca 59.6 ± 1.35cb 321.9 ± 10.8a 95.77 ± 0.83b
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1. Water control; 2. Cd (200 µM); 3. AMF + 200 µM Cd; 4. U. lactuca + 200 µM Cd; 5. AMF + U. lactuca + 200 µM Cd

U. lactuca, unlike AMF, contributes to strong foliar assimilation of Cd from the roots, as presented in Table 3. Plants treated with U. lactuca have a very high content of Cd, which is even greater than that of plants grown only with Cd.

Discussion

In the present study, sorghum leaves' length and fresh weight showed a substantial decrease in Cd-stressed control plants compared to non-stressed plants. Similar results were found by López et al. (2005) in tomato and by Wu and Zhang (2002) in barley. Nonetheless, Individual application of AMF showed a significant increase in leaves’ length and fresh weight, highlighting mycorrhizal symbiosis's positive influence in confronting Cd stress. Pawlowska et al. (2000) showed that the increase in the concentration of Cd and Pb, even at concentrations partially inhibiting spore germination, is correlated with the increase in the extension of the mycorrhizal hyphae of G. intraradices. It should be noted that the germination of spores, the density of hyphae and the expansion of symbiotic extra-radical hyphae differ substantially in different genus of AMF (Dodd et al. 2000). A significant alteration in the physiological and biochemical properties of the host is caused by mycorrhizal symbiosis. Such alterations lead to an increase in morphological parameters of plants, an enhancement of the host's competitive ability, causing an increase in growth rate. This is the result of the evolution of biochemical pathways and the improvement of the capacities of nutrients uptake by the plant. Other plant species have shown similar results under heavy metal stress conditions (Rabie 2005; Andrade et al. 2010). Mycorrhizal colonization of G. intraradices is strongly correlated with the increase in morphological parameters of host plants compared to control plants. Other researchers confirm the results obtained (Waller et al. 2005; Sun et al. 2010).The positive effect is probably attributed to improved P and N nutrition, water uptake by hyphae, and increased root length density (Wu et al. 2011).

It can also be seen that U. lactuca application significantly improved plant shoot length in all Cd treatments, which was the case for soybean (Rathore et al. 2009), where there was an increase in vegetative growth upon applying seaweed extract. Another seaweed (Ulva rigida) tested by Latique et al. (2021a, b) at different concentrations (0, 12.5, 25, 50%) appeared to improve the growth parameters of wheat significantly. Also, the extract of Kappaphycus alvarezii, applied as foliar spray (5.0%), increased tomato fruit yield (60.89%) compared to control plants sprayed with water (Zodape et al. 2011). Fresh weight and shoot length of sorghum decreased in Cd-treated plants. However, this decrease was less evident in plants treated with liquid seaweed extract alone. This constructive effect could be due to the macronutrient content of U. rigida, such as potassium, magnesium, and phosphorus, and the auxin content of U. rigida extracts (Latique et al. 2021a, b), which plays a vital role in the division and the cell enlargement and can lead to increased plant biomass and growth.

The presence of AMF alone significantly increased the chlorophyll content. On the contrary, foliar treatment with U. lactuca alone or in synergy with AMF decreased the chlorophyll content. According to Muradoglu et al. (2015), the decreasing effect induced by Cd on the chlorophyll content could be explained by the inhibitory effect of Cd on the enzymes involved in the biosynthesis of pigments. These results are in agreement with previous reports where Cd inhibited chlorophyll biosynthesis and generated a kind of senescence (Muradoglu et al. 2015) In the same line, Yang et al. (2011) reported that the leaves of Potamogeton crispus under Cd stress showed decreased chlorophyll a and b contents. The same was true for garden grasses and almond seedlings (Nada et al. 2007). Therefore, chlorophyll pigments appear to be one of the main reasons for heavy metal damage to plants.

The determination of the level of Cd accumulated in sorghum plants provides information on the effect of AMF on the reduction of the accumulation of Cd at the root level as well as the prevention of the translocation of the Cd accumulated in the roots towards the leaves. AMF can block Cd at root levels probably through chelation of Cd within AMF or through adsorption of Cd into fungal cell wall chitin. The detoxification mechanisms allowing the storage of toxic compounds are contained in the components of the AMF hyphae (Han et al. 2021). In contrast, foliar spraying with U. lactuca’s extract increased Cd uptake in roots and leaves of plants grown without AMF. Plants grown in the presence of AMF have an increased tolerance to heavy metals, thus increasing the survival rate in contaminated soils, which explains the increase in the morphological parameters of plants grown with the addition of AMF and Cd compared to those grown only with Cd. The adsorption of heavy metals by AMF beyond the rhizosphere of the plant is possibly due to glomalin, an insoluble glycoprotein released by AMFs playing a role in the immobilization of heavy metals at the interphase of the system of fungal plants (Yasmeen et al. 2019). It has been reported that G. mosseae contributes to the tolerance of wheat against Cd by reducing its accumulation in the roots (Rascio el al. 2008). The exclusion and/or reduction of the rate of entry of heavy metals into the host plant is associated with the significant capacity of AMFs to adsorb heavy metals through the cell wall of extraradical hyphae associated with plant roots. This may explain the reduction in the Cd content in the leaves of plants under treatment with G. intraradices.

In addition, the roots of the plants inoculated with AMF presented 59.6 ± 1.35 ppm of Cd, of which only 1.67% could reach the aerial part. Moreover, by adding treatment with U. lactuca, an increase in root assimilation was revealed (95.77 ± 0.83 ppm), but only 1.1% could be translocated to the leaves. AMFs are considered to be able to reduce the concentration of heavy metals in the leaves of non-hyperaccumulative plants (Zhang and Chen 2021) they contribute to the stimulation of plant roots and the increase in the production of heavy metal chelating agents such as cysteine ​​and glutathione, thus causing a reduction in the toxicity of these compounds towards the host plant (Dhalaria el al. 2020). Additionally, Yang et al. (2015) found that phytostabilization of AMFs can attenuate the adverse negative effects of Cd on plant growth. The mycorrhizal plants presented a significantly lower Cd content compared to the non-mycorrhizal plants; this is due to the accumulating power of the mycorrhizal hyphae which allows the adsorption/accumulation of large quantities of Cd; 10 to 20 times higher than plant roots. AMFs appear to be effective in stress attenuation under conditions of high heavy metal stress, which was also evident by increased root colonization (Liu et al. 2022).

High concentrations of heavy metals lead to their displacement and accumulation in the parenchyma cells of the internal root of host plants; the inoculation site of arbuscules, vesicles, and fungal hyphae (Nasri et al. 2011). Studies indicate that AMFs express certain genes in the host plant upon exposure to heavy metals that may mitigate their adverse negative effects on the plant (Raklami et al. 2022). Other research has provided information on the ability of mycorrhizal fungi to attenuate Cd and Cu stress through the induction of gene expression (GintABC1) of related transporters, thus causing the attenuation of toxic effects at the level of fungal hyphae. The expression of genes of related transporters in the presence of HMs and the production of metallothioneins also allows the detoxification of the harmful effects of HMs at the levels of G. intraradices hyphae (Dhalaria et al. 2020). AMFs contribute to the protection and improvement of the growth of plants exposed to heavy metals through the action of their structures which allows the immobilization of HMs in the mycorrhizosphere or the uptake of HMs in fungal tissues such as vacuoles (Riaz et al. 2021). AMFs produce different compounds contributing to the phytostabilization of HMs in the rhizosphere by causing their precipitation in the soil, they can also chelate HMs in their different cellular structures or absorb them in their cell walls, AMFs can also produce through their hyphae the glomalin; insoluble glycoprotein that helps phytostabilize heavy metals in the rhizosphere (Gaur and Adholeya 2004; Göhre and Paszkowski 2006).

Carbon and nitrogen metabolism are widely influenced by stress which induces numerous physiological and biochemical changes in plants (Hussain et al. 2020). The nitrogen and carbon metabolic pathways are linked since carbohydrates are crucial for energy production and for supplying the carbon skeletons, thus, providing the assimilation of nitrogen via the action of the GS/GOGAT pathways. Similarly, for ammonium assimilation, the availability of carbon skeletons is necessary in order to increase the carbon flux of the TCA cycle (El Omari et al. 2016). The detoxification and ammonium tolerance of sorghum plants is due to the power of PEPC which allows the supply of oxaloacetic acid and L-malate to the TCA in response to the demand of the main ammonium receptor for the biosynthesis of organic nitrogen; α-ketoglutarate (El Omari et al. 2016). MDH catalyzes the interconversion of malate and oxaloacetate (OAA) coupled with the reduction/oxidation of organelles in the NAD pool (Wang et al. 2015) (Fig. 12). In the present study, it was highlighted that the effect of AMFs leads to a significant increase in MDH activity in sorghum leaves. In addition, the increase in this activity was more pronounced under synergistic treatment of AMF and U. lactuca. The increase in this activity can also be caused by the increase in enzymatic activities linked to the assimilation of nitrogen (GS and GDH), therefore the increase in the intake of nitrates is due to the treatments with AMF and/or U. lactuca. Exposure to Cd can also induce an increase in this activity as shown by another study done by Chaoui and El Ferjani (2005), on Pisum sativum L. who also revealed an increase in this activity, which demonstrates the stimulatory effect of Cd for MDH activity (Chaoui and El Ferjani 2005).

Fig. 12.

Fig. 12

Open in a new tab

representative scheme of the interaction between carbon and nitrogen metabolic pathways

MDH plays a central role in replenishing the TCA cycle which ensures the supply of an adequate amount of keto acids, especially 2-oxoglutarate and oxaloacetate necessary for the synthesis of amino acids, hence proteins, and therefore the increase in MDH under the effect of the treatments used seems to be favourable for the plants’ growth processes since they allow the TCA cycle to continue (Kchikich et al. 2021b).

In the current work, out of the five conditions studied, the third condition: single treatment by AMFs in the presence of Cd, showed the strongest GS activity compared to the other conditions, which provides information on the great stimulatory effect of AMFs on this activity. U. lactuca treatment alone or combined with the AMFs also increased the GS activity compared to the control plants. The increased enzyme activities of GS in sorghum leaves indicate that treatment with AMF and foliar application of U. lactuca enhanced N uptake and assimilative capacity. Nakmee et al. (2016) confirm the results obtained in the present study. Indeed, mycorrhizal symbiosis leads to a significant increase in the nitrogen content in the leaves, as well as a strong uptake of nitrogen in the roots and leaves of sorghum inoculated with AMF (Nakmee et al. 2016). A regulation of root nitrate transporters in host plants is probably caused by mycorrhizal symbiosis. Nutrient delivery transformed from direct to symbiotic uptake may likely be responsible for modulating transporter gene expression (Beuve et al. 2004). On the other hand, the increase in GDH activity has long been associated with plant mycorrhization (Kchikich et al. 2021b), which is what we observed upon treatments with AMF. On top of this, AMFs were found to significantly facilitate photosynthetic metabolism by inducing certain key enzymatic activities and genes encoding key Calvin cycle enzymes. Increased stomatal conductance and CO2 assimilation intensity were observed using mycorrhizal fungi of the genera Funneliformis, Claroideoglomus, Rhizophagus, and Diversispora in cucumber culture (Kchikich et al. 2021b).

Isocitrate dehydrogenases (ICDH) and aspartate aminotransferases (AAT) are two essential enzymes for the assimilation of ammonium via the direct synthesis of organic acids (Ben Mrid et al. 2018). It has been recorded that the cytosolic ICDH is the main enzyme whose role is to produce 2-oxoglutarate; used for amino acid synthesis (Ben Mrid et al. 2018) and AAT activity in plants. AAT, by assimilating NH4+ to aspartate, plays an essential role in the metabolism of glutamate which in turn leads to the biosynthesis of other amino acids (De La Torre et al. 2014). A high content of free amino acids was revealed by Abdel-Fattah and Mohamedin (2000) in sorghum plants treated with G. intraradices. A similar result was obtained in tomatoes grown in the presence of G. fasciculatum. The increase in ICDH and AAT activities was also noted in plants sprayed with U. lactuca extract, with or without AMF. Foliar application of seaweeds allows for the assimilation of bioactive compounds through the leaves, such as growth hormones, amino acids, and other metabolites responsible for improving the activity of nitrate reductase, synthetic chlorophyll, and proteins, and consequently, improving plants' tolerance to abiotic stresses (Latique et al. 2013).

High Cd content is strongly linked to an increase in free radicals (Elobeid et al. 2012), which can cause protein, amino acid, and nucleic acid degradation and induce lipid peroxidation (Atabayeva et al. 2020). High accumulation of MDA shows severe lipid peroxidation (Jiang et al. 2016). In the present work, the content of MDA and O2− in the plants inoculated in the presence and the absence of the extract of U. lactuca were obviously reduced compared to the plants not inoculated and sprayed by the extract of U. lactuca, which further showed that mycorrhizal inoculation reduced Cd-induced oxidative stress in sorghum. Similar results were found by Jiang et al. (2016) in L. japonica; fungal inoculation reduced MDA content in Cd-stressed plants. Abdelhameed and Metwally (2019) had similar results in Trigonella leaves, suggesting that AMFs increase antioxidant activity, resulting in less lipid peroxidation where antioxidants scavenge radical production before reacting with membrane lipids (Abdelhameed and Metwally 2019).

Superoxide dismutase is an enzyme considered to be the first barrier against ROS (latique et al. 2021a, b), and it is responsible for the disproportionation of superoxide anion radicals (O2−) into hydrogen peroxide (H2O2) and O2 resulting in less lipid peroxidation (Hashem et al. 2016). AMFs applied in the presence and absence of U. lactuca extract increased the antioxidant potential of stressed plants compared to untreated control plants. Foliar application of U. lactuca also led to an increase in this activity. The results of the present study provide information on the positive effect of AMFs against oxidative stress. The work of Garg and Chandel (2012) confirms that mycorrhizal colonization significantly increased SOD activities in Cajanus cajan grown in Cd-contaminated soils. Chaturvedi et al. (2018) also had similar results on tomatoes.

U. lactuca extract appears to be effective in increasing the antioxidant potential of stressed plants. This may be due to the presence of certain biochemical compounds in the seaweed extract, such as soluble sugar, polyphenol, and proteins which could be responsible for stimulating antioxidant enzymes (Latique et al. 2021a, b).

Conclusion

In conclusion, the results of our investigation showed that cadmium stress negatively affected the sorghum bicolor plants. Growth parameters were significantly decreased, cadmium content was increased, and carbon nitrogen enzymes were altered. However, the mycorrhizal and algal treatments successfully repaired the damage caused by Cd through decreasing its content, significantly increasing the growth parameters, and regulating the activities of the enzymatic system in order to restore the natural state of these plants as represented in the control. Our study also showed that the synergy between the mycorrhizal fungus and the algal extract had a very positive impact on sorghum plants, and thus, boosted their tolerance to Cd stress.

In summary, the use of mycorrhiza, the algal extract, and the synergy between them for reducing the harmful effects of Cd can be an effective approach to enhance the tolerance of sorghum plants against cadmium.

Author contributions

Conceptualization: Anass Kchikich; Methodology: Anass Kchikich, Reda Ben Mrid, Ennoury Abdelhamid, Zoulfa Roussi, Nada Nhhala, Bouchra Ben Mrid, Ayoub kounnoun, Mohammed EL-Maadoudi. Formal analysis investigation: Nhiri Mohamed, Reda BenMrid, Anass Kchikich; writing original draft: Anass Kchikich, Zoulfa Roussi, Nada Nhhala, Bouchra Benmrid; Writing-review and editing: Reda Ben Mrid, Anass Kchikich, Mohamed Nhiri.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Data availability

The data used to support the finding of this study are include in the article.

Declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. Abdel-Fattah GM, Mohamedin AH. Interactions between a vesicular-arbuscular mycorrhizal fungus (Glomus intraradices) and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils. 2000;32:401–409. doi: 10.1007/s003740000269. [DOI] [Google Scholar]
  2. Abdelhameed RE, Metwally RA. Alleviation of cadmium stress by arbuscular mycorrhizal symbiosis. Int J Phytoremediat. 2019;21(7):663–671. doi: 10.1080/15226514.2018.1556584. [DOI] [PubMed] [Google Scholar]
  3. Andrade SA, Gratão PL, Azevedo RA, Silveira AP, Schiavinato MA, Mazzafera P. Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot. 2010;68:198–207. doi: 10.1016/j.envexpbot.2009.11.009. [DOI] [Google Scholar]
  4. Anjum NA, Umar S, Iqbal M, Khan NA. Cadmium causes oxidative stress in mung bean by affecting the antioxidant enzyme system and ascorbate-glutathione cycle metabolism. Russ J Plant Phys. 2011;58:92–99. doi: 10.1134/S1021443710061019. [DOI] [Google Scholar]
  5. Ben Mrid R, El Omari R, Bouargalne Y, El Mourabit N, Nhiri M. Activities of carbon and nitrogen metabolism enzymes of sorghum (Sorghum bicolor L. Moench) during seed development. J Crop Sci Biotechnol. 2018;21:283–289. doi: 10.1007/s12892-017-0140-0. [DOI] [Google Scholar]
  6. Beuve N, Rispail N, Lainé P, Cliquet JB, Ourry A, Le Deunff E. Putative role of γ-aminobutyric acid (GABA) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant Cell Environ. 2004;27:1035–1046. doi: 10.1111/j.1365-3040.2004.01208.x. [DOI] [Google Scholar]
  7. Bisht A, Bhalla S, Kumar A, Kaur J, Garg N (2022) Arbuscular mycorrhizae impart Cd tolerance in Cajans cajan (L.) Millsp. by upregulating the expression of metallothionein (CcMT1) and phytochelatin synthase (CcPCS1) genes. J Plant Growth Regul. 10.1007/s00344-022-10864-2
  8. Bouchmaa N, BenMrid R, Boukharsa Y, Bouargalne Y, Nhiri M, Idir A, Zyad A. Reactive oxygen species-mediated apoptosis and cytotoxicity of newly synthesized pyridazin-3-ones in P815 (Murin mastocytoma) cell line. Drug Res. 2019;69(10):528–536. doi: 10.1055/a-0762-3775. [DOI] [PubMed] [Google Scholar]
  9. Calvo P, Nelson L, Kloepper JW. Agricultural uses of plant biostimulants. Plant Soil. 2014;383:3–41. doi: 10.1007/s11104-014-2131-8. [DOI] [Google Scholar]
  10. Chaoui A, El Ferjani E. Effects of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. Comptes Rendus Biol. 2005;328:23–31. doi: 10.1016/j.crvi.2004.10.001. [DOI] [PubMed] [Google Scholar]
  11. Chaturvedi R, Favas PJ, Pratas J, Varun M, Paul MS. Effect of Glomus mosseae on accumulation efficiency, hazard index and antioxidant defense mechanisms in tomato under metal (loid) stress. Int J Phytoremediat. 2018;20(9):885–894. doi: 10.1080/15226514.2018.1438360. [DOI] [PubMed] [Google Scholar]
  12. De La Torre F, Cañas RA, Pascual MB, Avila C, Cánovas FM. Plastidic aspartate aminotransferases and the biosynthesis of essential amino acids in plants. J Exp Bot. 2014;65:5527–5534. doi: 10.1093/jxb/eru240. [DOI] [PubMed] [Google Scholar]
  13. Dhalaria R, Kumar D, Kumar H, Nepovimova E, Kuča K, Torequl Islam M, Verma R. Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy. 2020;10(6):815. doi: 10.3390/agronomy10060815. [DOI] [Google Scholar]
  14. Dodd JC, Boddington CL, Rodriguez A, Gonzalez-Chavez C, Mansur I. Mycelium of arbuscular mycorrhizal fungi (AMF) from different genera: form, function and detection. Plant Soil. 2000;226:131–151. doi: 10.1023/A:1026574828169. [DOI] [Google Scholar]
  15. El Defrawy MM, Hesham A. G-protein-coupled receptors in fungi. Fungal Biotechnol Bioeng. 2020 doi: 10.1007/978-3-030-41870-0_3. [DOI] [Google Scholar]
  16. El Omari R, Ben Mrid R, Chibi F, Nhiri M. Involvement of phosphoenolpyruvate carboxylase and antioxydants enzymes in nitrogen nutrition tolerance in sorghum bicolor plants. Russ J Plant Physiol. 2016;63:719–726. doi: 10.1134/S102144371606008X. [DOI] [Google Scholar]
  17. Foday JR, Edward Hingha BO, Bai XU, Xiaohui A. Removal of toxic heavy metals from contaminated aqueous solutions using seaweeds: a review. Sustainability. 2021;13(21):12311. doi: 10.3390/su132112311. [DOI] [Google Scholar]
  18. Garg N, Chandel S. Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. Plant Growth Reg. 2012;31:292–308. doi: 10.1007/s00344-011-9239-3. [DOI] [Google Scholar]
  19. Gaur A, Adholeya A. Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci. 2004;86:528–534. [Google Scholar]
  20. Göhre V, Paszkowski U. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta. 2006;223:1115–1122. doi: 10.1007/s00425-006-0225-0. [DOI] [PubMed] [Google Scholar]
  21. Hadebe ST, Modi AT, Mabhaudhi T. Drought tolerance and water use of cereal crops: a focus on sorghum as a food security crop in sub-Saharan Afric. J Agric Crop Sci. 2017;203(3):177–191. doi: 10.1111/jac.12191. [DOI] [Google Scholar]
  22. Han Y, Zveushe OK, Dong F, Ling Q, Chen Y, Sajid S, Dios VR. Unraveling the effects of arbuscular mycorrhizal fungi on cadmium uptake and detoxification mechanisms in perennial ryegrass (Lolium perenne) Sci Total Environ. 2021;798:149222. doi: 10.1016/j.scitotenv.2021.149222. [DOI] [PubMed] [Google Scholar]
  23. Hashem A, Abd Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D, Wirth S (2016) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23(2):272–281. 10.1016/j.sjbs.2015.11.002 [DOI] [PMC free article] [PubMed]
  24. Hatamian M, Nejad AR, Kafi M, Souri MK, Shahbazi K (2019) Growth characteristics of ornamental judas tree (Cercis siliquastrum L.) seedlings under different concentrations of lead and cadmium in irrigation water. Acta Sci Pol Hortic Cultus 18(2):87–96. 10.24326/asphc.2019.2.8
  25. Hussain S, Khaliq A, Noor MA, Tanveer M, Hussain HA, Hussain S, Mehmood T. Metal toxicity and nitrogen metabolism in plants: an overview. Carbon Nitrogen Cycl Soil. 2020;66:221–248. doi: 10.1007/978-981-13-7264-3_7. [DOI] [Google Scholar]
  26. Jiang Q, Zhuo F, Long S, Zhao H, Yang D, Ye Z, Jing Y. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Sci Rep. 2016;6(1):21805. doi: 10.1038/srep21805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kchikich A, Ben Mrid R, Kabach I, Nhiri M, El Omari R (2021a) Arbuscular mycorrhizal fungi enhance sorghum plant growth under nitrogen-deficient conditions through activation of nitrogen and carbon metabolism enzymes. Int J Agric Biol 26:201–208. 10.17957/IJAB/15.1825
  28. Kchikich A, El Omari R, Kabach I, Yasri A, Nhiri M, Ben Mrid R. Effect of arbuscular mycorrhizal fungus and the γ-aminobutyric acid treatment in nitrate assimilation under nitrogen deficiency in sorghum plant. Russ J Plant Physiol. 2021;68:901–908. doi: 10.1134/S102144372105006X. [DOI] [Google Scholar]
  29. Latique S, Chernane H, Mansori M, El Kaoua M. Seaweed liquid fertilizer effect on physiological and biochemical parameters of bean plant (phaesolus vulgaris variety paulista) under hydroponic system. Eur Sci J. 2013;9:1857–7881. [Google Scholar]
  30. Latique S, Ben Mrid R, Kabach I, Kchikich A, Sammama H, Yasri A, Nhiri M, El Kaoua M, Douira A, Elmaoui K. Foliar application of Ulva rigida water extracts improves salinity tolerance in wheat (Triticum durum L) Agronomy. 2021 doi: 10.3390/agronomy11020265. [DOI] [Google Scholar]
  31. Latique S, BenMrid R, Kabach I, Kchikich A, Sammama H, Yasri A, Selmaoui K. Foliar application of Ulva rigida water extracts improves salinity tolerance in wheat (Triticum durum L.) Agronomy. 2021;11(2):265. doi: 10.3390/agronomy11020265. [DOI] [Google Scholar]
  32. Liu D, Zheng K, Wang Y, Zhang Y, Lao R, Qin Z, Zhao Z. Harnessing an arbuscular mycorrhizal fungus to improve the adaptability of a facultative metallophytic poplar (Populus yunnanensis) to cadmium stress: physiological and molecular responses. J Hazard Mater. 2022;424:127430. doi: 10.1016/j.jhazmat.2021.127430. [DOI] [PubMed] [Google Scholar]
  33. López ML, Peralta-Videa JR, Benitez T, Gardea-Torresdey JL. Enhancement of lead uptake by alfalfa (Medicago sativa) using EDTA and a plant growth promoter. Chemosphere. 2005;61:595–598. doi: 10.1016/j.chemosphere.2005.02.028. [DOI] [PubMed] [Google Scholar]
  34. Muradoglu F, Gundogdu M, Ercisli S, Encu T, Balta F, Jaafar HZ, Zia-Ul-Haq M. Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biol Res. 2015;48(1):1–7. doi: 10.1186/s40659-015-0001-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Nada E, Ferjani BA, Ali R, Bechir BR, Imed M, Makki B. Cadmium-induced growth inhibition and alteration of biochemical parameters in almond seedlings grown in solution culture. Acta Physiol Plant. 2007;6:66. [Google Scholar]
  36. Nakmee PS, Techapinyawat S, Ngamprasit S. Comparative potentials of native arbuscular mycorrhizal fungi to improve nutrient uptake and biomass of Sorghum bicolor Linn. Agric Nat Resour. 2016;50:173–178. doi: 10.1016/j.anres.2016.06.004. [DOI] [Google Scholar]
  37. Nasri N, Tlili N, Elfalleh W, Cherif E, Ferchichi A, Khaldi A, Triki S. Chemical compounds from Phoenician juniper berries (Juniperus phoenicea) Nat Prod Res. 2011;25:1733–1742. doi: 10.1080/14786419.2010.523827. [DOI] [PubMed] [Google Scholar]
  38. Pawlowska TE, Chaney RL, Chin M, Charvat I. Effects of metal phytoextraction practices on the indigenous community of arbuscular mycorrhizal fungi at a metal-contaminated landfill. Appl Environ Microbiol. 2000;66:2526–2530. doi: 10.1128/AEM.66.6.2526-2530.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rabie GH. Contribution of arbuscular mycorrhizal fungus to red kidney and wheat plants tolerance grown in heavy metal-polluted soil. Afr J Biotechnol. 2005;4:332–345. [Google Scholar]
  40. Raklami A, Meddich A, Oufdou K, Baslam M. Plants microorganisms-based bioremediation for heavy metal cleanup: recent developments, phytoremediation techniques, regulation mechanisms, and molecular responses. Int J Mol Sci. 2022;23(9):5031. doi: 10.3390/ijms23095031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rascio N, Dalla Vecchia F, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnell C, Gabbrielli R. Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot. 2008;62(3):267–278. doi: 10.1016/j.envexpbot.2007.09.002. [DOI] [Google Scholar]
  42. Rathore SS, Chaudhary DR, Boricha GN, Ghosh A, Bhatt BP, Zodape ST, Patolia JS. Effect of seaweed extract on the growth, yield and nutrient uptake of soybean (Glycine max) under rainfed conditions. South Afr J Bot. 2009;75:351–355. doi: 10.1016/j.sajb.2008.10.009. [DOI] [Google Scholar]
  43. Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Wang X. Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review. J Hazard Mater. 2021;402:123919. doi: 10.1016/j.jhazmat.2020.123919. [DOI] [PubMed] [Google Scholar]
  44. Roussi Z, Kchikich A, Nhhala N, Krid A, Ennoury A, Asri SE, Nhiri M. Cistus monspeliensis extract as a prospective biostimulant in enhancing tolerance to cadmium in sorghum plant. Biomass Convers Biorefinery. 2022;66:1–15. doi: 10.1007/s13399-022-03542-6. [DOI] [Google Scholar]
  45. Sharma J, Chakraverty N (2013) Mechanism of plant tolerance in response to heavy metals. Molecular stress physiol of plants. Springer, India, pp 289–308. 10.1007/978-81-322-0807-5_12
  46. Tuhy L, Chowañska J, Chojnacka K. Seaweed extracts as biostimulants of plant growth: review. Chemik. 2013;67(7):636–641. [Google Scholar]
  47. Waller F, Achatz B, Baltruschat H. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA. 2005;102:13386–13391. doi: 10.1073/pnas.0504423102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wang XM, Soetaert K, Peirs P, Kalai M, Fontaine V, Dehaye JP, Lefevre P. Biochemical analysis of the NAD+-dependent malate dehydrogenase, a substrate of several serine/threonine protein kinases of Mycobacterium tuberculosis. PLoS ONE. 2015;10:247–253. doi: 10.1371/journal.pone.0123327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wu F, Zhang G. Genotypic variation in kernel heavy metal concentrations in barley and as affected by soil factors. J Plant Nutr. 2002;25:1163–1173. doi: 10.1081/PLN-120004380. [DOI] [Google Scholar]
  50. Wu QS, Zou YN, Wang GY. Arbuscular mycorrhizal fungi and acclimatization of micropropagated citrus. Commun Soil Sci Plant Anal. 2011;42:1825–1832. doi: 10.1080/00103624.2011.587570. [DOI] [Google Scholar]
  51. Yang HY, Shi GX, Xu QS, Wang HX. Cadmium effects on mineral nutrition and stress in Potamogeton crispus. Russ J Plant Physiol. 2011;58:253–260. doi: 10.1134/S1021443711020245. [DOI] [Google Scholar]
  52. Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang M. The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS ONE. 2015;10(12):e0145726. doi: 10.1371/journal.pone.0145726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yasmeen T, Li A, Iqbal S, Arif MS, Riaz M, Shahzad SM, Ali S (2019) Biotechnological tools in the remediation of cadmium toxicity. In: Cadmium tolerance in plants. Ac Prs., pp 497–520. 10.1016/B978-0-12-815794-7.00018-7
  54. Zhang C, Chen Z. Advances in study on the effects of arbuscular mycorrhizal fungi on plants in remediation of arsenic-contaminated soil. Acta Agric Scan Sec B Soil Plant Sci. 2021;71(9):825–834. doi: 10.1080/09064710.2021.1952300. [DOI] [Google Scholar]
  55. Zhang QI, Wang CH. Natural and human factors affect the distribution of soil heavy metal pollution: a review. Water Air Soil Poll. 2020;231:1–13. doi: 10.1007/s11270-020-04728-2. [DOI] [Google Scholar]
  56. Zodape ST, Gupta A, Bhandari SC, Rawat US, Chaudhary DR, Eswaran K, Chikara J (2011) Foliar application of seaweed sap as biostimulant for enhancement of yieldand quality of tomato (Lycopersicon esculentum Mill.)
  57. Zulfiqar F, Navarro M, Ashraf M, Akram NA, Munné-Bosch S. Nanofertilizer use for sustainable agriculture: advantages and limitations. Plant Sci. 2019;289:110270. doi: 10.1016/j.plantsci.2019.110270. [DOI] [PubMed] [Google Scholar]

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