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Mitigating gadolinium toxicity in guar (Cyamopsis tetragonoloba L.) through the symbiotic associations with arbuscular mycorrhizal fungi: physiological and biochemical insights

BMC Plant Biology volume 24, Article number: 877 (2024) Cite this article

Abstract

Background

Gadolinium (Gd) is an increasingly found lanthanide element in soil; thus, understanding its impact on plant physiology, biochemistry, and molecular responses is crucial. Here, we aimed to provide a comprehensive understanding of Gd (150 mg kg− 1) impacts on guar (Cyamopsis tetragonoloba L.) plant yield and metabolism and whether the symbiotic relationship with arbuscular mycorrhizal fungi (AMF) can mitigate Gd toxicity of soil contamination.

Results

AMF treatment improved mineral nutrient uptake and seed yield by 38–41% under Gd stress compared to non-inoculated stressed plants. Metabolic analysis unveiled the defense mechanisms adopted by AMF-treated plants, revealing carbon and nitrogen metabolism adaptations to withstand Gd contamination. This included an increase in the synthesis of primary metabolites, such as total sugar (+ 39% compared to control), soluble sugars (+ 29%), starch (+ 30%), and some main amino acids like proline (+ 57%) and phenylalanine (+ 87%) in the seeds of AMF-treated plants grown under Gd contamination. Furthermore, fatty acid and organic acid profile changes were accompanied by the production of secondary metabolites, including tocopherols, polyamines, phenolic acids, flavones, and anthocyanins.

Conclusions

Overall, the coordinated synthesis of these compounds underscores the intricate regulatory mechanisms underlying plant-AMF interactions and highlights the potential of AMF to modulate plant secondary metabolism for enhanced Gd stress tolerance.

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Introduction

The presence of potentially toxic elements in soil poses a significant threat to agroecosystems, jeopardizing soil health and plant productivity [1,2,3]. Among them, gadolinium (Gd), a highly toxic heavy metal and rare earth element, has long been utilized in the healthcare industry and medical fields [4]. While the primary focus of Gd research has centered on its effects on human health, recent studies have begun to shed light on its repercussions on plant health and agricultural ecosystems, mainly because this element has been detected in various environmental matrices, including soil and water [5]. Studies have shown that Gd exposure can disrupt essential physiological processes in plants, including photosynthesis, nutrient uptake, and enzymatic activity (e.g., Rubisco, amylase, and proline dehydrogenase) [6, 7]. It has been reported that the content of nutrients (e.g., N, Ca and Mg) in roots and shoot tissues significantly declined in response to the high levels of Gd in the soil, which in turn disrupted N assimilation and its involvement in synthesizing proteins, amino acids and other low-molecular-weight-organic-N compounds in the stressed plants [8]. Similarly, it has been proposed that the effects of Gd on various aspects of plant growth, morphology, metabolism, and genotoxicity may vary depending on the concentration of Gd [7]. Additionally, Gd contamination has been linked to plant growth, development, and yield alterations, raising concerns about its potential implications for global food security [9].

In recent years, research has increasingly focused on exploring biotechnological solutions to mitigate the adverse effects of heavy metal contamination on plants. Among these solutions, arbuscular mycorrhizal fungi (AMF) have emerged as promising allies due to their ability to form symbiotic associations with plant roots and enhance plant tolerance to heavy metal stress [10, 11]. AMF establish symbiotic relationships with roots to acquire essential nutrients from the host plant and reciprocally supply mineral nutrients such as N, P, K, Ca, Zn, and S and therefore offer nutritional assistance to the plants even under unfavorable conditions [12]. Studies have demonstrated the ability of AMF to alleviate the negative impacts of Gd on plant physiology and growth through the formation of symbiotic associations with plant roots and enhancement of nutrient acquisition, particularly phosphorus, which can help alleviate the nutrient imbalances induced by Gd contamination [13]. Furthermore, AMF has been shown to enhance plant tolerance to heavy metal stress through metal sequestration and the production of metal-detoxifying compounds and antioxidant metabolites [14].

Guar (Cyamopsis tetragonoloba L.), as an important leguminous crop cultivated extensively in arid and semi-arid regions, holds significant economic value due to its various applications in industries such as food, pharmaceuticals, cosmetics, and oil drilling [15]. Guar is presumed to be an alternative crop for arid and semi-arid regions of the world, as it exhibits an agronomically acceptable growth rate and productivity under conditions of poor and sporadic rainfall, abundant sunshine, low relative humidity, and warm temperatures, and is a short-duration plant species harvested approximately 3–4 months after sowing [15]. The average guar seed yield is 400 kg ha− 1, with high yields achieved from sowing dates that vary from May to August, and mid-May planting has been reported to produce the highest seed yields [16]. Moreover, the potential of guar as a biofuel feedstock and its role in phytoremediation are areas of growing interest, highlighting the multifaceted significance of this versatile crop [17]. Studies have shown that heavy metal contamination in soil can lead to various physiological and biochemical alterations in guar plants, including the inhibition of seed germination, decline of plant growth, impairment of photosynthesis, disruption of nutrient uptake, and inducing oxidative stress [18, 19].

Despite the growing awareness of the adverse effects of heavy metals on guar plant production, there is a need for comprehensive research to understand the mechanisms underlying rare earth elements’ toxicity and to develop mitigation strategies. The current study aimed to evaluate the physiological and biochemical impacts of Gd toxicity on guar plants and to investigate whether the symbiotic relationship with AMF can mitigate these toxic effects. We elucidated the defense mechanisms activated through AMF symbiosis, providing a comprehensive understanding of the coordinated biosynthesis of bioactive metabolites that enhance Gd stress tolerance and improve plant yield and quality. The changes in primary metabolites such as sugars and amino acids, and secondary metabolites such as tocopherols, polyamines, phenolic acids, flavones, and anthocyanins were measure to understand the metabolic adaptations in AMF-treated plants.

Materials and methods

Plant growth and experimental setup

The greenhouse experiment was conducted twice using agricultural topsoil for two consecutive years in 2022 and 2023. The soil samples underwent air drying and were then sieved through a 2 mm nylon sieve for soil pH determination and subsequent pot experiments. Subsequently, 15-gram subsamples were ground using an agate vibrating cup mill to pass through a 0.16-mm nylon sieve for chemical analysis. The chemical and physical properties of the soil before planting are depicted in Table S1.

Healthy guar seeds (Cyamopsis tetragonoloba L. var. Baldy) from the Agricultural Research station at Cairo (Egypt) were surface sterilized using a 1% sodium hypochlorite solution for 5 min [20]. The soil was divided into two sets: inoculated with Rhizophagus irregularis MUCL 41,833 (AMF) or left uninoculated. The AMF inoculum comprised 5 g of soil (approximately ∼50 spores g− 1 soil) [20]. Both soil types were subdivided, with some designated as polluted soil containing 150 mg kg− 1 of Gd, while others served as non-polluted controls. The concentration of 150 mg of Gd kg− 1 of soil was chosen based on preliminary experiments, indicating a 50% reduction in plant growth at this concentration [7]. Five plants per pot (25 × 40 cm) were arranged in a greenhouse and watered automatically twice a week with tap water for 3 min each time. Additionally, each plant received a single commercial organic slow-release fertilizer application at a rate of 13.9 g plant− 1. The pots were arranged in a completely randomized design, with each treatment having five replicates.

Plant leaves and seeds, crucial for our analysis, were collected at the flowering stage (about 7 weeks after sowing) and harvesting time (about 14 weeks after sowing), put in liquid nitrogen and stored at -80 °C for subsequent biochemical analyses [21].

Agronomic traits assessment

The plants were collected at harvest time to evaluate various growth and yield traits, including seed yield per plant, seed weight (in grams), and the number of pods and branches per plant.

Determination of minerals accumulation in seeds

The concentration of nitrogen (N), phosphorus (P), potassium (K), manganese (Mn), magnesium (Mg), sulfur (S), sodium (Na), iron (Fe) and zinc (Zn) in plants was determined using total-reflection X-ray fluorescence spectrometry (TXRF; Bruker Nano GmbH, Berlin, Germany), an ion chromatograph (Shimadzu, Japan), and the Kjeldahl method, as outlined by Yoshida et al. [22] and Bamrah et al. [23].

Seed composition

The crude fiber content was determined using the digestion method based on AOAC protocols [24]. Neutral detergent fiber (NDF), acid detergent fiber (ADF), and acid detergent lignin (ADL) were quantified using an ANKOM-200/220 Fiber Analyzer, following the methods described in USDA Agricultural Handbook No. 379 [25]. Tannin content was measured according to Maxson and Rooney [26], with samples extracted using HCl (1% v/v) in methanol, mixed with vanillin-HCl reagent, and absorbance read at 500 nm. Ash content was determined by weighing samples after incineration at 550 °C for about 7 h, following the procedure by Czaja et al. [27]. Total lipid content was assessed by gravimetric analysis using a modified protocol of Bligh and Dyer [28], with samples extracted in a chloroform-methanol mixture (1:2 v/v). Ergot alkaloids (EAs) were quantified using liquid chromatography with tandem mass spectrometry (LC-MS/MS), as described by Babič et al. [29], with EAs extracted in an acetonitrile and ammonium carbonate solution (1:1 v/v). Radical scavenging activity was determined by measuring 2,2-diphenyl-1-picryl-hydrazyl-hydrate (DPPH) content spectrophotometrically, following Diñeiro Garcia et al. [30] procedure.

Sugar metabolism

The sugars present in the seed samples were extracted using TAE buffer (50 mM; pH 7.5), supplemented with a combination of polyclar (0.15% v/v), sodium azide (0.02% v/v), PMSF (2 mM), sodium bisulfite (NaHSO3) (12 mM), mannitol (10 mM), and mercaptoethanol (1 mM), followed by centrifugation. Subsequently, the supernatant was passed through a mixed-bed Dowex column (300 µL Dowex H + and 300 µL Dowex Ac–; both 100–200 mesh). Quantification of various sugars, including glucose, sucrose, stachyose, verbascose, raffinose, galactomannan, and fructose, was performed using high-performance anion-exchange chromatography/pulsed amperometric detection (HPAEC-PAD) as outlined by Verspreet et al. [31]. Sugar separation was carried out on a CarboPac MA1 column at a flow rate of 0.3 mL min− 1 with an eluent gradient of NaOH (250–700 mM). Peak areas obtained from the calibration curve using authentic external standards were utilized for quantification. Additionally, not naturally present in the samples, maltotriose served as the internal standard to ensure the quality of extraction and purification, following the methodology described by AbdElgawad et al. [32].

Total soluble sugars in seeds were quantified spectrophotometrically by initially extracting them in 80% ethanol (v/v) and subsequently adding anthrone reagent (anthrone dissolved in 72% v/v H2SO4 solution), following the procedure outlined by Yaghoubi et al. [33]. The absorbance of the final extracted samples was then measured at 625 nm using a multi-mode microplate reader (Synergy Mx, Biotek, Santa Clara, USA), as described by de Sousa et al. [34], to determine both total soluble and insoluble sugar content. The residual pellet remaining after soluble sugar extraction was utilized for starch content determination, following the methodology detailed by Galtier et al. [35]. This involved hydrating and gelatinizing the starch solution with 90% dimethyl sulfoxide (v/v), precipitating and washing it with ethanol, and subsequently treating it with a mixture of α-amylase and amyloglucosidase to extract the starch.

Assessment of fatty acid, amino acid, and organic acid profile in seeds

Fatty acids in the seed samples were extracted and quantified based on the protocol outlined by Torras-Claveria et al. [36]. Samples were discolored in methanol at room temperature, and nonadecanoic acid was added as an internal standard. Gas chromatography-mass spectrometry (GC-MS) analysis was performed using a Hewlett-Packard 6890 gas chromatograph coupled with an MSD 5975 mass spectrometer. Fatty acids were identified using the NIST 05 database and the Golm Metabolome Database.

The amino acid profile was evaluated according to the methodology described by Zinta et al. [37]. Ground seed samples were homogenized in an 80% v/v ethanol solution and centrifuged at 14,000 rpm for 20 min. Following vacuum-evaporation of the supernatant, the pellet was re-suspended in chloroform. The supernatant phase obtained after a subsequent centrifugation step (14,000 rpm, 10 min) was filtered through a Millipore microfilter (0.2 µM pore size) and diluted with deuterium L-glutamine-2,3,3,4,4-d5 as an internal standard. A BEH amide column on a Waters Acquity UPLC-TQD system was used to detect, separate, and quantify amino acids [37].

Individual organic acids in the seed samples were quantified following extraction in a 0.1% v/v phosphoric acid solution supplemented with butylated hydroxyanisole, as described by AbdElgawad et al. [38]. The obtained supernatants were filtered using Millipore microfilters (0.2 µM pore size) and analyzed by high-performance liquid chromatography (HPLC) isocratically with 0.001 N sulfuric acid, set at 210 nm, and a flow rate of 0.6 mL min− 1. Separation was achieved using an Aminex HPH-87 H column with a Bio-Red IG Cation H pre-column at 65 °C.

Antioxidant metabolites and enzymes

The total polyphenols and flavonoids concentration in the fresh leaf samples was determined using gallic acid and quercetin standards, respectively, following the methodologies outlined by Zhang et al. [39] and Chang et al. [40]. The antioxidant capacity of the leaf samples was assessed using the ferric reducing/antioxidant power (FRAP) method, with 6-hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid (Trolox) as a standard, as described by George et al. [41]. Tocopherols in the leaves were quantified using high-performance liquid chromatography (HPLC) with Dimethyl tocol serving as an internal standard, as outlined by AbdElgawad et al. [42]. Additionally, the levels of reduced ascorbate (ASC) and reduced glutathione (GSH) were determined using HPLC, following the procedures described by Hartley-Whitaker et al. [43] and Potters et al. [44].

Proteins were extracted from leaf samples, and the resulting supernatant was utilized to evaluate the activity of antioxidant enzymes, following the methodology outlined by Murshed et al. [45]. The activity of superoxide dismutase (SOD) was assessed by measuring the inhibition of nitro-blue tetrazolium (NBT) reduction, utilizing an extinction coefficient (ε550 = 12.8 mM–1 cm–1) as described by Dhindsa et al. [46]. Peroxidase (POX) activity was determined based on the oxidation of pyrogallol in phosphate buffer at 430 nm, with an extinction coefficient (ε430 = 2.46 mM–1 cm–1) according to the protocol established by Kumar and Khan [47]. Catalase (CAT) activity was measured by analyzing the decomposition of hydrogen peroxide at 240 nm, utilizing an extinction coefficient (ε240 = 39.4 M− 1 cm− 1) as outlined by Kumar and Khan [47]. Ascorbate peroxidase (APX) activity was determined by monitoring the decrease in absorbance at 290 nm, following the procedure described by Nakano and Asada [48]. Glutathione reductase (GR) activity was assessed by recording the decrease in NADPH absorbance at 340 nm, in accordance with the methodology established by Murshed et al. [45]. The activity of glutathione peroxidase (GPX) was evaluated by measuring the reduction in NADPH absorbance at 340 nm in a coupled enzyme assay with GR, as outlined by Drotar et al. [49]. Glutaredoxin (Grx) activity was determined by monitoring the reduction of 2-hydroxy-ethyl-disulfide by reduced glutathione in the presence of NADPH, following the procedure described by Lundberg et al. [50]. Thioredoxin (Trx) content was assessed by measuring NADPH oxidation at 340 nm, according to the methodology established by Wolosiuk et al. [51].

Determination of the content of anthocyanins, phenolics, flavonoids, and polyamines

Anthocyanin content in leaves was assessed by homogenizing the samples in methanol: HCl (99:1 v/v) and measuring the absorbance of the resulting solution at 550 nm, following the methodology outlined by Wagner [52]. Individual phenolic acids and flavonoid compounds were quantified using high-performance liquid chromatography (HPLC) with a Lichrosorb Si-60 column (7 μm, 3 × 150 mm) and a diode array detector (DAD), as described by Hamad et al. [53]. Samples were homogenized in an acetone: water (4:1, v/v) solution for 24 h and subjected to HPLC with a flow rate of 0.8 mL min− 1, utilizing a mobile phase comprising water: formic acid (90:10 v/v) and acetonitrile: water: formic acid (85:10:5 v/v/v). Quantification of each compound was performed using a calibration curve of the related standard. Polyamines were extracted using 5% perchloric acid, followed by centrifugation to separate the supernatant from the pellet, which was then resuspended in the same solution. Both acid-soluble and acid-insoluble fractions underwent hydrolysis in 6 M HCl at 110 °C for 18 h to convert conjugated and bound polyamines into free forms. The resulting hydrolyzates were dried, dissolved in 5% perchloric acid, and quantified by HPLC using a µ-Bondapack C18 column (Waters, USA), with 1,6-hexanediamine as an internal standard; conjugated polyamine content was calculated as the difference between total acid-soluble and free polyamine levels, based on the weight of pollen grains before incubation. [54].

Statistical analysis

As the Bartlett test confirmed the homogeneity of variances for the dependent variables across different experiments, the results were analyzed collectively as a single experiment comprising six replicates. Data were presented as mean ± standard deviation (SD) and analyzed using two-way ANOVA with post-hoc Tukey HSD test (p ≤ 0.05) in IBM SPSS Statistics (V21.0; SPSS® Inc., Chicago, IL, USA).

Results

Agronomic traits

However, AMF treatment did not significantly affect seed yield in the control condition; it demonstrated a substantial improvement in seed yield under Gd contamination conditions, showing a 38% increase compared to non-treated plants under Gd stress (p < 0.05). While AMF-treated plants did not produce heavier seeds than non-treated plants (p > 0.05), they were able maintain the numbers of pods and seeds per plant under stress at levels comparable to those of unstressed plants (Fig. 1).

Fig. 1
figure 1

Yield and yield components (± standard deviation) of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test)

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Seed nutritive quality

Mineral concentration in seeds

The findings revealed notable increments (p < 0.05) in the concentration of N, K, Mg, and Ca within the seeds of plants subjected to Gd contamination, with levels being approximately 26%, 20%, 33%, and 46% higher than those in control unstressed plants, respectively (Fig. 2). Additionally, all examined minerals showed significantly greater accumulation in the seeds of AMF-treated plants under both control and contamination conditions. Specifically, mineral concentrations in seeds peaked in AMF-treated plants grown in Gd-contaminated soil, with P (+ 22%), K (+ 22%), S (+ 26%), Na (+ 35%), Zn (+ 22%), Fe (+ 43%), and Mn (+ 208%), showing significant increases compared to non-treated plants under Gd contamination (Fig. 2).

Fig. 2
figure 2

Mineral concentration (± standard deviation) in the seeds of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test)

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Seeds chemical composition and nutritional values

Gd contamination and AMF treatment led to significant increases in ADF (+ 29–53%), total lipid (+ 26–31%), and crude protein (+ 26–33%) levels in seeds compared to those in unstressed control plants (Fig. 3). Moreover, the NDF, ADL, and alkaloid contents in seeds peaked in AMF-treated plants under Gd contamination, with increases of 32%, 35%, and 76% respectively, compared to control plants under non-contamination conditions (p < 0.05) (Fig. 3). However, neither AMF nor Gd treatments had significant effects on ash levels in the seeds (p > 0.05) (Fig. 3).

Fig. 3
figure 3

The content of total sugar (A), crude protein (B), total lipid (C), ash (D), alkaloids (E), neutral detergent fiber (NDF; F), acid detergent fiber (ADF; G) and acid detergent lignin (ADL; H) in the seeds of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test)

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Primary metabolites

Sugar content and ingredient profile of seeds

Initial analysis of carbohydrate composition in seeds aimed to discern the effects of soil contamination and AMF symbiosis on carbohydrate synthesis. Results indicated that both AMF and Gd treatments significantly influenced the accumulation of total sugars in seeds (p < 0.05), with total sugar content being 18–33% higher than that of control plants (Fig. 2A). Both Gd and AMF treatments exerted strong impacts on starch (approximately + 25–40%) and total soluble sugars content (approximately + 17–40%) compared to unstressed controls (Fig. 4).

Fig. 4
figure 4

Sugar content and ingredient profile of seeds of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test)

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An examination of the major soluble sugar components revealed that sucrose content was unaffected by either Gd contamination or AMF treatment (p > 0.05). However, AMF-treated plants under contamination showed significantly higher fructose levels (+ 45%) compared to control plants (Fig. 4). Additionally, glucose content increased by 33–56% in seeds of plants treated with AMF and Gd compared to unstressed control plants (p < 0.05). The accumulation of verbascose and galactomannan in seeds was not influenced by Gd and AMF treatments (p > 0.05). In contrast, stachyose content significantly increased in AMF-treated plants under contamination conditions, while raffinose content significantly decreased (–36%) in seeds of AMF-treated plants under contamination compared to control plants (Fig. 4).

Amino acid, fatty acid and organic acid profiles in seeds

The present research also tried to reveal how the changes in sugar content can be linked to amino acid, fatty acid, and organic acid biosynthesis pathways. The amino acid profiling assessment in seeds showed varying responses to soil contamination and AMF treatments (Table 1). Accordingly, proline (+ 49%), phenylalanine (+ 37%), arginine (+ 68%), ornithine (+ 26%), glutamate (+ 54%), cysteine (+ 117%), and lysine (+ 80%) accumulated significantly higher in the seeds of plants grown in contaminated soils compared to those in control soils (p < 0.05). Conversely, Gd contamination led to significant decreases in serine (–41%), asparagine (–36%), leucine (–35%), and histidine (–40%) in seeds (p < 0.05). Furthermore, AMF-treated plants under soil contamination exhibited the highest accumulation of proline (+ 57%), phenylalanine (+ 87%), arginine (+ 97%), ornithine (+ 38%), glutamine (+ 26%), glutamate (+ 49%), cysteine (+ 149%), lysine (+ 104%), alanine (+ 261%), and valine (+ 44%), which were significantly higher than those in unstressed control plants (p < 0.05).

Table 1 Amino acids (mg mg− 1 protein ± standard deviation) composition in the seeds of guar plants in response to arbuscular mycorrhizal fungi (AMF) and Gadolinium (Gd) contamination in soil
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The analysis of organic acids in the seeds identified six distinct acids, including malate, lactate, and trans-aconitic, which were not significantly affected by soil contamination or AMF treatment (p > 0.05). However, citrate content increased in response to both Gd (+ 67%) and AMF (+ 130%) treatments. Additionally, AMF-treated plants under contamination conditions showed significant increases in oxalate (+ 69%) and succinate (+ 78%) levels (p < 0.05) (Fig. 5).

Fig. 5
figure 5

Organic acids (ng g− 1 FW ± standard deviation) composition in the seeds of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test)

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The results of 19 detected fatty acids in the seeds are provided in Table 2. Palmitic acid (C 16:0) and stearic acid (C18:0) were the major saturated fatty acids accounting for approximately 32% (control plants) to 12% (AMF-treated plants under Gd contamination) of total fatty acid content. Moreover, linoleic acid (C18:2) and oleic acid (C18:1) were found as predominant unsaturated fatty acids, accounting for about 41% and 56% of the fatty acid content in the control and AMF + Gd treatments, respectively. In fact, AMF treatment significantly increased the content of most unsaturated fatty acids in seeds under Gd stress compared to unstressed control plants (p < 0.05). Conversely, most saturated fatty acids were more accumulated in control plants compared to both AMF-treated and Gd-treated plants (p < 0.05) (Table 2).

Table 2 Fatty acids (mg g− 1 FW ± standard deviation) composition in the seeds of guar plants in response to arbuscular mycorrhizal fungi (AMF) and Gadolinium (Gd) contamination in soil
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Secondary metabolites

Phenolic, flavonoid and anthocyanain

Although total polyphenol content exhibited significant variations due to both AMF treatment and Gd stress, the highest content was obtained in the AMF + Gd treatment, which was about 38% higher than that in unstressed control plants (p < 0.05). Similarly, total flavonoid content was significantly (p < 0.05) affected by both AMF and Gd treatments, showing increases of 53%, 63%, and 67% in AMF, Gd, and AMF + Gd treatments, respectively, compared to control (Fig. 6).

Fig. 6
figure 6

The values of antioxidant capacity (FRAP; A), 2,2-Diphenyl-1-picrylhydrazy (DPPH; B), total flavonoids (C), total polyphenols (D), and anthocyanins (E) in the leaves of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test)

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Upon closer examination of phenolic compositions, 11 compounds were detected in the leaf samples. Notably, gallic acid, p-coumaric acid, and cinnamic acid were more concentrated in the leaves of AMF-treated and Gd-treated plants compared to control plants, while caffeic acid, protocatechuic acid, and syringic acid content were affected solely by AMF + Gd treatment (p < 0.05) (Table 3). Similarly, out of 13 detected flavon compounds in leaf samples, six (quercetin, quercitrin, apigenin, rutin, naringenin and daidzein) exhibited significantly higher content in AMF-treated plants under Gd contamination compared to unstressed control plants (p < 0.05), while the content of isoquercitrin, velutin and genistein significantly decreased. Anthocyanin content, a major group of flavonoids, was influenced by both AMF treatment and Gd contamination, in which the content in AMF, Gd, and AMF + Gd were 57%, 67%, and 70% higher than that in control leaves, respectively (p < 0.05) (Fig. 6).

Table 3 Phenolic acids and flavonoids (mg g− 1 DW) in the leaves of guar plants in response to arbuscular mycorrhizal fungi (AMF) and Gadolinium (Gd) stress
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Tocopherol and polyamine compounds in leaves

While AMF treatment did not significantly impact total tocopherol content under control conditions (p > 0.05), it did increase tocopherol levels by approximately 45% under Gd contamination compared to unstressed control plants (Fig. 7). Additionally, the detected polyamines, including putrescine (Put), spermidine (Spd), and spermine (Spm), reached their highest levels in the AMF + Gd treatment, showing increases of 63%, 150%, and 123%, respectively, compared to unstressed control leaves (p < 0.05) (Fig. 8). Similar trends were observed in the activity of enzymes involved in polyamine metabolism, which were more activated in AMF-treated plants under Gd contamination (Fig. 8). Specifically, the activity of key enzymes such as spermidine synthase (SPDS), spermine synthase (SPMS), and S-adenosyl-L-methionine decarboxylase (SAMDC) increased significantly in the AMF (+ 54–102%), Gd (+ 42–106%), and AMF + Gd (+ 119–189%) treatments compared to the control. Other enzymes in polyamine metabolism, including ornithine decarboxylase (ODC), arginine decarboxylase (ADC), polyamine oxidase (PAO), and diamine oxidase (DAO), also showed significantly higher activity in response to both AMF and Gd treatments, with the highest activities observed in the combined AMF and Gd treatment (p < 0.05).

Fig. 7
figure 7

The content of tocopherols in the leaves of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test)

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Fig. 8
figure 8

The content of polyamines (A) and the activity of enzymes involved in the polyamines metabolism (B) in the leaves of guar plants in response to arbuscular mycorrhizal fungi (AMF) and gadolinium (Gd) contamination in soil. Means in in each experiment followed by similar letter(s) are not significantly different at 5% probability level (Tukey test). SPDS: Spermidine synthase; SPMS: Spermine synthase; SAMDC: S-adenosyl-L-methionine decarboxylase; ADC: Arginine decarboxylase; ODC: Orinthnine decarboxylase; PAO: Polyamine oxidase; DAO: Diamine oxidase

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Antioxidant defense

ROS-scavenging enzymes and ASC/GSH cycle

The study highlights the crucial role of AMF in bolstering the antioxidant defense system of plants under Gd stress. AMF-treated plants exhibited significant improvements in the activity of various antioxidant enzymes and the accumulation of essential antioxidant molecules in their leaves compared to untreated plants (Table 4). Specifically, the activity of APX increased by 38% in the AMF + Gd treatment compared to control plants (p < 0.05), indicating enhanced hydrogen peroxide scavenging. POX activity rose by 35% in the AMF + Gd treatment (p < 0.05), suggesting better protection against oxidative damage. Furthermore, CAT activity increased by 47% in AMF-treated plants under stress, reflecting improved detoxification processes. SOD activity also saw a 38% increase in AMF-treated plants under stress, indicating enhanced dismutation of superoxide radicals. The accumulation of key antioxidant molecules in the leaves of AMF-treated plants further underscores their enhanced antioxidant defense system. In this regard, ASC and GSH levels surged by 84% and 93% in AMF + Gd treatment compared to control treatment (p < 0.05). Moreover, the activity of enzymes involved in the regeneration of antioxidant molecules, including GR, DHAR, and MDHAR, was substantially elevated in AMF-treated plants under Gd stress, which were 51%, 57% and 37% higher than control, respectively. Additionally, the increased activity of Grx by 72%, GPX by 23%, Trx by 69%, and Prx by 44% in AMF-treated plants signifies enhanced thiol-dependent antioxidant defense mechanisms under Gd contamination (Table 4).

Table 4 The responses of enzymatic (µmol min− 1 mg− 1 protein) and non-enzymatic (µmol g− 1 FW) components of the ascorbate-glutathione (ASC/GSH) and redox-dependent signaling pathways to arbuscular mycorrhizal fungi (AMF) and Gadolinium (Gd) contamination in soil
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Antioxidant capacity

The results clearly demonstrate the significant impact of AMF on boosting the antioxidant capacity of plants under stress conditions. This is evidenced by notable improvements in both ferric-reducing antioxidant power (FRAP) and 2,2-Diphenyl-1-picrylhydrazyl (DPPH) scavenging activity. Specifically, AMF-treated stressed plants showed a remarkable 112% increase in FRAP values compared to control plants (Fig. 6). Similarly, the DPPH scavenging activity in AMF-treated stressed plants was significantly higher, reaching 77% above the levels observed in control plants (Fig. 6).

Discussion

The results of this study clearly illustrate the alterations in mineral accumulation within guar seeds following AMF treatment application. This outcome was expected, given the established understanding that AMF-plant symbioses enhance nutrient uptake from the soil, especially in response to environmental stressors, thereby elevating levels of carbon fixation and maintaining ionic balance. This process primarily occurs by extending the root absorption surface area through AMF colonization [55,56,57].

However, it was somewhat unexpected to observe a greater accumulation of N, K, Mg, and Ca in Gd-stressed plants compared to their unstressed counterparts in the absence of AMF treatment. This is particularly unexpected for Ca content in the seeds since interacting rare earth elements (e.g., Gd) with Ca-dependent biological systems have been proven, which can result in leading to entry to the plant cells by blocking Ca binding sites, mainly because their ionic radii (about 85–122 pm) is almost the same ionic radii as the divalent Ca cation (106 pm) [58]. Such a significant increase in the accumulation of these elements in the seeds, in contrast to a significant decrease in seed yield under Gd stress, somehow indicates a negative correlation between these factors. This observation under Gd stress contradicts previous notions of decreased nutrient uptake and assimilation within plant tissues in response to environmental stress [8]. This contradiction may be elucidated by a stress tolerance mechanism in plants, wherein an increase in root biomass or absorption surface area facilitates the uptake of more dissolved nutrients from the soil to fulfill the physiological demands of plants in combating stressors, prioritizing this over the demands for high seed production in stressful conditions [59]. Furthermore, this increase in absorption was notably amplified in AMF-treated plants under Gd stress, particularly for nutrients such as N, K, Mn, Mg, and Ca, likely attributable to the expansion of extraradical hyphae and the surface area of AMF mycelial networks, thereby fostering greater root biomass and nutrient absorption [57]. Nevertheless, high accumulation of some nutrients, such as Mg and Ca in Gd-stressed plants, can justify the reduction in Mn content in seeds, mainly because of similarities in ionic radii or binding strength [60].

Enhanced nutrient accumulation may be a key factor influencing changes in sugar synthesis, thus affecting plants’ carbon and nitrogen metabolism. Our study observed increased total and soluble sugar content in AMF- and Gd-treated plants, accompanied by elevated accumulation of specific amino acids, such as proline and phenylalanine, and proteins in the seeds. These findings support previous research highlighting the role of AMF and stressor factors in regulating sugar metabolism and boosting the accumulation of compatible solutes like soluble sugars, proline, and proteins in response to heavy metal stress [11]. These compounds help manage the osmotic status within stressed plant cells, safeguard membranes, and stabilize the reaction center of photosystem II [61, 62].

Despite the notable accumulation of glucose and fructose in the seeds of plants treated with AMF and/or grown under Gd contamination, sucrose content remained unaffected by the treatments. This discrepancy may be attributed to variations in source and sink activities within treated plants. Among the three main synthesized soluble sugars in source tissues, sucrose is transported exclusively to sink tissues [63]. Additionally, a negative correlation between raffinose content in seeds and monosaccharides (glucose and fructose) suggests the potential hydrolysis of raffinose into these monosaccharides in AMF-treated plants under stress. Raffinose accumulation is more linked to its functional role, such as serving as part of a carbon storage mechanism [64]. Furthermore, starch synthesis, a major end product of photosynthesis, increased in response to stress and AMF treatments, underscoring its involvement in producing essential structural and metabolic compounds, including proteins [33]. Starch accumulation in treated plants may also occur gradually over time due to an imbalance in overnight conversion to sucrose [65].

Not only the accumulation of nutrients in seeds, as the critical elements in various molecules, but also the high content of soluble sugars and starch, as the source of the carbon skeleton, can provide a high level of biosynthesis of amino acids and antioxidant metabolites in plants under heavy metal stress [7, 57]. Our findings regarding shifts in the amino acid profile in the seeds of AMF-treated stressed plants support previous studies linking alterations in amino acid content to increased tolerance against heavy metal toxicity [66, 67]. The increased accumulation of N in the seeds and more synthesis of major amino acids involved in N metabolism, such as glutamine and glutamate, in response to AMF and Gd treatments in our study, underscores the connection between nitrogen assimilation and protein content in plants, particularly under stress conditions. Some certain amino acids like glutamine, lysine, and alanine, showing increased accumulation in response to AMF and/or Gd in the present research, are well known for their function as intermediate signals in regulating the expression of key transcription genes involved in plant stress responses [33, 68]. Moreover, the roles of proline and alanine are particularly prominent in heavy metal-stressed plants due to their involvement in stabilizing macromolecular structures, scavenging reactive oxygen species (ROS), acclimating to heavy metal toxicity by sequestering metal ions within plant cells, and regulating the solubility, adsorption, desorption, and migration of metals through processes like dissolution, chelation, and oxidation/reduction [69, 70]. The increased content of ornithine and glutamate amino acids, precursors of proline, also suggests the active involvement of both ornithine and glutamate pathways in proline biosynthesis in our study, serving as a crucial defense mechanism.

Significant changes in total lipid content and fatty acids composition in seeds of stressed plants corroborate the earlier findings in shifts in fatty acid profiles in response to environmental stress [33, 71]. Moreover, the application of AMF treatment had a notable impact on increasing the content of most unsaturated fatty acids in the seeds under Gd stress. Conversely, most saturated fatty acids were more abundant in the unstressed control seeds. This finding aligns with earlier studies suggesting that the symbiotic effects of beneficial soil microorganisms can enhance the accumulation of unsaturated fatty acids in plant cells, thereby maintaining proper membrane fluidity for required multiple membrane-dependent processes and signalling to regulate stress defence under diverse abiotic stresses [72, 73]. Similarly, tocopherols, lipid-soluble and non-enzymatic antioxidant molecules, were more synthesized in AMF-treated plants under stress, somehow confirming their crucial operation within the glutathione peroxidase pathway to safeguard the cell membranes of mycorrhizal plants from oxidative damage caused by rare earth elements contamination [7, 74].

Citrate, succinate and oxalate were the organic acids in the seeds that positively responded to the application of AMF under Gd contamination, which might be potentially serving as one of the mechanisms employed by plants to alleviate heavy metal stress by promoting precipitation, chelation, and sequestration of metal ions [75]. It has also been suggested that citrate acts as a ligand for heavy metals, affecting their redox behaviour by forming non-toxic compounds or impeding their plant uptake [75, 76]. However, caution is warranted in interpreting these results, as their role and concentration in seeds may differ from those in other tissues [33]. However, the responses of malate, lactate, and trans-aconitic acid to AMF and Gd stress treatments deviated from previous findings, indicating an elevated secretion of these organic acids in plants subjected to heavy metal stress [75, 77].

The elevated levels of antioxidant molecules and heightened activity of antioxidant enzymes observed in response to Gd-stressed leaves provide indirect evidence of oxidative damage induced by Gd contamination. Additionally, considerable evidence indicates that the increased accumulation and enhanced metabolism of soluble sugars in mycorrhizal plants can activate antioxidant systems, thereby mitigating heavy metal stress by scavenging ROS [7, 11, 78]. Accordingly, the elevated levels of ROS-detoxifying enzymes such as SOD, CAT, and POX, along with those involved in the ascorbate/glutathione pathway (APX, GR, GSH, ASC, MDHAR, DHAR, and GPX), have been identified as the primary mechanism, by which plants mitigate the adverse effects of oxidative stress induced by soil heavy metal contamination [79,80,81].

The substantial increase in the ferric reducing ability (FRAP), the hydrogen acceptor ability towards antioxidant (DPPH), various phenolic acids and their flavonoid derivatives (e.g., caffeic acid, gallic acid, quercetin, apigenin, etc.), alongside anthocyanins, was observed in the leaves of AMF-treated plants grown under stress. Prior studies have suggested that the elevated levels of antioxidant compounds in AMF- and heavy metal-treated plants serve as an adaptive mechanism to combat stress, particularly by safeguarding the photosynthetic machinery [11, 32, 82]. The increased content of phenylalanine amino acid in response to AMF treatment and Gd contamination in the present research may contribute to such elevation in the synthesis of antioxidant metabolites, given its role as a major precursor for various metabolites involved in plant defence strategies, including phenolic acids, flavonoids, and anthocyanins [83]. Similar findings have been reported that AMF-treated and heavy metal-stressed plants may redirect fixed carbon towards carbon-based secondary pathways, facilitating the synthesis of key phenols and flavons through phenylalanine deamination [32, 74].

The increased accumulation of amino acids such as ornithine and arginine in the leaves of both AMF- and Gd-treated plants may contribute to the elevated synthesis of phytohormone-like aliphatic amine compounds, including Put, Spm, and Spd [84]. Put serves as the starting point of the polyamines pathway, derived either from ornithine in the cytosol [85] or from arginine in the chloroplast [86], before becoming a precursor molecule in the subsequent synthesis of Spm and Spd [87]. Increased activity of ODC and ADC enzymes in the leaves of treated plants in the present research can confirm the activeness of both ornithine- and arginine-derived polyamine synthesis pathways. Moreover, the high activity of SPDS, SPMS, and SAMDC in the AMF- and Gd-treated plants in our research can be linked to their role in catalyzing the biosynthesis of SPD and SPM from Put, as previously reported by Raychaudhuri et al. [87]. The high activity of PAO and DAO in the leaves of AMF-treated plants under stress may have something to do with the catabolism of polyamines. In fact, the high activity of PAO and DAO in the leaves of AMF-treated plants under stress suggests that these enzymes play a significant role in breaking down polyamines. Polyamines, which are organic compounds associated with cell growth and stress responses, can become elevated during stress conditions. The increased activity of PAO and DAO indicates that the plants may be actively metabolizing these polyamines to manage stress, potentially converting them into other compounds that can help mitigate stress effects or regulate growth processes. This can result in the formation of hydrogen peroxide, ammonia, and 4-aminobutanal from Put, which can activate a process in which the byproduct is succinate to be used in the citric acid cycle [88]. The released hydrogen peroxide during polyamine catabolism serves as a signal transduction process of stressed plants [89]. Our findings regarding the increased content of Put, Spd, and Spm align with previous reports suggesting that plants can enhance their tolerance to heavy metal stress by modulating polyamine levels [67, 90]. These results also support the notion that elevated synthesis of molecules involved in nitrogen metabolism, such as polyamines and amino acids, represents a primary active mechanism employed by plants against heavy metal contamination.

Despite the activation of specific defence mechanisms by stressed plants, it is evident that soil Gd contamination negatively affected the seed yield of guar plants. The decline in yield may be associated with a substantial decrease in other yield components and agronomic characteristics, such as the seed weight, number of seeds per plant, and number of pods and branches per plant, as observed in the present study. Although mycorrhizal plants under stress produced significantly lower seeds, their production was higher than that of non-treated stressed plants.

Conclusion

By elucidating the mechanisms underlying the positive effects of AMF on plant tolerance to Gd, the present research aims to provide insights into the challenges posed by rare earth elements contamination and avenues for future research to enhance the resilience of guar plants to environmental stressors. The findings highlighted the beneficial effects of mycorrhizal treatment on mineral nutrient absorption and mitigation of the detrimental effects of Gd toxicity on plant yield compared to untreated plants. Metabolomics analysis provided insights into the defense mechanisms employed by AMF-treated plants, revealing modifications in carbon and nitrogen metabolisms to counteract Gd contamination. Specifically, there was an increase in the biosynthesis of primary metabolites, such as soluble sugars and certain amino acids, enhancing the antioxidant defense system as a robust protective mechanism for plants in contaminated soils. These alterations were accompanied by the activation of antioxidant enzymes and elevated levels of tocopherols, polyamines, phenolic acids, flavones, and anthocyanins in the plants, alongside shifts in fatty acids and organic acids profiling. Overall, the AMF-plant symbiotic association notably empowered guar plants to withstand Gd stress and enhance seed yield by producing essential metabolites.

Nevertheless, there might be several potential limitations and uncertainties in the present study. One limitation is the controlled greenhouse environment in which the study was conducted, which may not fully replicate field conditions where multiple variables can influence plant-mycorrhizal interactions and the impact of Gd stress. Another uncertainty is the specific concentration of Gd used (150 mg kg-1), which might not represent the range of contamination levels found in different agricultural settings, and the effects of varying concentrations of Gd on guar plants and AMF interactions remain uncertain. Additionally, the study focused on a specific cultivar of guar, and different cultivars may exhibit varying degrees of resilience to Gd stress and responsiveness to AMF treatment.

Considering the complexities of plant-mycorrhizal interactions and environmental stressors, these results provide valuable insights into practical applications and future research directions aimed at enhancing guar plant resilience in contaminated environments. These insights can inform the development of biotechnological and agronomic strategies to enhance the tolerance of guar and other crops to heavy metal contamination. Future research could explore the application of AMF in field conditions, investigate the responses of different guar cultivars, and assess the effects of varying Gd concentrations on plant health and yield. Additionally, the study opens avenues for exploring the role of AMF in mitigating other environmental stressors, further contributing to sustainable agriculture and soil health in contaminated environments.

Data availability

All data generated or analyzed during this study are included in this published article.

Abbreviations

ADC:

arginine decarboxylase

ADF:

acid detergent fiber

ADL:

acid detergent lignin

AMF:

arbuscular mycorrhizal fungi

APX:

ascorbate peroxidase

ASC:

reduced ascorbate

CAT:

catalase

DAO:

diamine oxidase

DPPH:

2,2-Diphenyl-1-picrylhydrazyl

EAs:

ergot alkaloids

FRAP:

ferric-reducing antioxidant power

Gd:

gadolinium

GPX:

glutathione peroxidase

GR:

glutathione reductase

Grx:

glutaredoxin

GSH:

reduced glutathione

NDF:

neutral detergent fiber

ODC:

ornithine decarboxylase

PAO:

polyamine oxidase

POX:

peroxidase

Put:

putrescine

SAMDC:

S-adenosyl-L-methionine decarboxylase

SOD:

superoxide dismutase

Spd:

spermidine

SPDS:

spermidine synthase

Spm:

spermine

SPMS:

spermine synthase

Trx:

thioredoxin

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Acknowledgements

The authors extend their appreciation to the Researchers Supporting Project number (RSP2024R376) King Saud University, Riyadh, Saud Arabia.

Funding

Open Access funding enabled and organized by Projekt DEAL.

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Authors and Affiliations

  1. Department of Botany and Microbiology, Faculty of Science, Beni-Suef University, Beni-Suef, 65541, Egypt

    Hamada AbdElgawad

  2. Department of Soil, Plant and Food Sciences, University of Bari ’Aldo Moro’, Via Amendola 165/A, Bari, 70126, Italy

    Carmine Crecchio & Mohammad Yaghoubi Khanghahi

  3. Botany & Microbiology Department, Faculty of science, Assiut University, P.O. Box 71516, Assiut, Egypt

    Mousa nhs

  4. Department of Pharmaceutics, College of Pharmacy, King Saud University, P.O. Box 2455, Riyadh, Riyadh Province, 11451, Saudi Arabia

    Mostafa A. Abdel-Maksoud & Abdul Malik

  5. Department of Integrative Agriculture, College of Agriculture and Veterinary Medicine, United Arab Emirates University, P.O. Box 15551, Al Ain, Abu Dhabi, United Arab Emirates

    Mohamed S. Sheteiwy, Saad Sulieman & Mohammed Alyafei

  6. The National Key Laboratory of Water Disaster Prevention, Hohai University, Nanjing, 210098, China

    Yousef Alhaj Hamoud

  7. College of Hydrology and Water Resources, Hohai University, Nanjing, 210098, China

    Yousef Alhaj Hamoud

  8. Department of Agronomy, Faculty of Agriculture, University of Khartoum, Shambat, Khartoum North, 13314, Sudan

    Saad Sulieman

  9. College of Environment, Hohai University, Nanjing, 210098, China

    Hiba Shaghaleh

  10. Department of European and Mediterranean Cultures: Architecture, Environment and Cultural Heritage (DiCEM), Università degli Studi della Basilicata, via Lanera 20, Matera, 75100, Italy

    Mohammad Yaghoubi Khanghahi

Authors
  1. Hamada AbdElgawad
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  2. Carmine Crecchio
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  3. Mousa nhs
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  5. Abdul Malik
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  6. Mohamed S. Sheteiwy
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  7. Yousef Alhaj Hamoud
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  11. Mohammad Yaghoubi Khanghahi
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Contributions

M.Y.K, H.A. and C.C.: conceptualization, methodology, investigation and writing; Y.A.H., H.S., M.n., M.A.A. and A.M.: methodology, investigation; M.S.S., S.S. and M.A.: Designed the experiment, performed the statistical analysis, Writing the first draft — review & editing and revised the final version of the manuscript. A.M. and M.A.: supervision, conceptualization, writing — review & editing, methodology, resources, funding acquisition.

Corresponding authors

Correspondence to Hamada AbdElgawad, Mohamed S. Sheteiwy or Mohammed Alyafei.

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AbdElgawad, H., Crecchio, C., nhs, M. et al. Mitigating gadolinium toxicity in guar (Cyamopsis tetragonoloba L.) through the symbiotic associations with arbuscular mycorrhizal fungi: physiological and biochemical insights. BMC Plant Biol 24, 877 (2024). https://doi.org/10.1186/s12870-024-05552-0

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BMC Plant Biology

ISSN: 1471-2229

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