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Exploring the benefits of AMF colonization for improving wheat growth, physiology and metabolism, and antimicrobial activity under biotic stress from aphid infection

BMC Plant Biology volume 25, Article number: 198 (2025) Cite this article

Abstract

Background

This study examines the effectiveness of arbuscular mycorrhizal fungi (AMF, Rhizophagus irregularis) as a bioprotection strategy to improve wheat’s physiological and biochemical responses. This study utilized soil inoculation with AMF and plant-controlled infestation with aphids, conducted over four weeks with three replicates per treatment.

Results

Although aphid infestation reduced root colonization by 26.8% and hyphal length by 30.7%, with no effect on arbuscular numbers (p < 0.05), AMF treatment improved growth, physiology, and metabolism of AMF-treated plants, especially under aphid infestation. AMF-treated plants showed a 51% increase in fresh weight and a 38% improvement in photosynthetic rates under infestation, indicating enhanced photosynthetic efficiency compared to controls. At the metabolism level, AMF application, particularly in infested plants, increased the levels of several amino acids, such as asparagine and glutamine, which increased by 23% and 20%, respectively. AMF treatment significantly boosted nitrogen metabolism enzymes, with activity increasing up to 4.8-fold in infested plants and arginase activity rising by 49% in infested and 290% in non-infested conditions. This metabolic shift elevated antioxidant levels, increasing flavonoids by 40% and polyphenols by 95% under aphid infestation. Additionally, antimicrobial efficacy improved, with AMF-treated plant extracts showing 30–67% larger inhibition zones against pathogens like Staphylococcus epidermidis and Salmonella typhimurium than untreated plants (p < 0.05).

Conclusions

This research examined the potential of AMF as a sustainable pest management tool, specifically focusing on its ability to enhance crop health and boost defenses against biotic stress. The study further highlights how AMF treatment improves antimicrobial efficacy, which can be integrated into farming practices to maintain plant growth while offering distinct advantages over conventional pest management strategies.

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Introduction

The increasing prevalence of agricultural pests, such as grain aphids (Sitobion avenae), poses significant challenges to crop production worldwide. These insects feed on plant sap and induce physiological stress, reducing plant growth and yield losses and increasing vulnerability to other pests and diseases [1, 2]. In particular, aphid infestations can disrupt nutrient transport, compromising photosynthesis and overall plant health [2]. Thus, there is an urgent need for effective and sustainable pest management strategies that enhance plant resilience against aphid stress.

Using microorganisms associated with soil and plants represents a significant advancement in the field of microbial natural products applicable for biofertilization and bioprotection [3, 4]. Among these microorganisms, arbuscular mycorrhizal fungi (AMF) are particularly valued for their ability to endure stress, as they promote plant growth by improving mineral absorption from the soil and mitigating the adverse effects of environmental stressors, thereby enhancing plant resilience [5, 6]. Although research into the molecular mechanisms of biotic stress tolerance in AMF-plant interactions is still in its infancy, extensive documentation highlights the remarkable potential of AMF to bolster plant resilience under abiotic stress, modify root architecture, and stimulate the production of antioxidant compounds [7]. In this regard, critical areas that require further exploration include the identification of key signaling molecules involved in AMF-plant communication, the characterization of genetic responses in plants upon AMF colonization, and the role of AMF in modulating plant immune responses at the molecular level. By enhancing the plant’s physiological responses, it has been reported that AMF can trigger systemic resistance mechanisms, leading to increased production of defensive compounds such as phytoalexins and secondary metabolites that deter aphids [8, 9]. Moreover, mycorrhizal associations alter root exudate profiles, which can attract natural enemies of aphids, further mitigating infestations [10]. As a result, plants colonized by AMF exhibit improved resilience against aphid attacks, demonstrating the importance of these fungi in sustainable agriculture and pest management strategies [9, 10].

Given the established ability of AMF to enhance plant physiological responses and increase defensive compound production, it follows that such improvements could have significant implications for photosynthesis. Photosynthesis is a critical physiological process that ensures plant growth and productivity, and any impairment can lead to significant reductions in crop yield [11]. Research has shown that plants experiencing aphid infestation often exhibit reduced photosynthetic rates due to chlorophyll degradation and nutrient deficiencies caused by aphid feeding [12]. By potentially enhancing the plant’s physiological status and promoting an efficient nutrient uptake during stress, AMF could serve as a valuable tool for offsetting the negative impacts of aphids on photosynthesis and yield. Thus, by enhancing both photosynthesis and nutrient uptake, AMF not only can mitigate the negative effects of aphid infestations on plant growth but also can play a crucial role in supporting nitrogen metabolism and the production of defensive compounds essential for effective pest management. The importance of nitrogen metabolism and amino acid composition in plants cannot be overstated in the context of pest management. Nitrogen is a key element in the synthesis of amino acids and proteins in plants, which play vital roles in various physiological and metabolic processes, including defense responses [13]. Enhanced nitrogen assimilation could provide the necessary compounds for synthesizing defensive proteins and secondary metabolites [14]. This relationship highlights the intricate link between nutrient status and plant resilience to pest pressures. Furthermore, the role of antioxidant metabolites in mitigating oxidative stress induced by herbivore feeding is well established. Antioxidants neutralize reactive oxygen species (ROS) produced during stress, protecting plant cells from damage [15]. The connection between AMF treatment and enhanced antioxidant levels could present a vital pathway through which plants can bolster their defenses against aphid attacks.

The present study aims to unravel the multifaceted effects of AMF treatment on wheat (Triticum aestivum L.) plants under infestation by grain aphid conditions. By investigating key physiological and biochemical parameters in plants, including photosynthesis, nitrogen metabolism, amino acid composition, antioxidant defenses, and mineral content, the present research tried to provide insights into the potential of AMF as a bioprotection agent for enhancing crop resilience in the face of biotic stresses. Additionally, the implications of these responses on aphid population dynamics will be assessed. Integrating this knowledge can contribute to developing more sustainable pest management strategies in agriculture.

Materials and methods

Experimental setup

Wheat seeds (Triticum aestivum L. var. Giza 119) were collected from the Agricultural Research Centers in Egypt. The seeds were soaked for 10 min in 10 g L− 1 of sodium hypochlorite for disinfection, and then they were washed with distilled water. The experiment was conducted in a controlled environment chamber with regulated temperature (22/18°C), light (16-hour photoperiod at 400 µmol m− 2 s− 1), and humidity (60%).

Two experimental treatments were applied, in which the first was seed soil inoculation with AMF at two levels (inoculated vs. control). Accordingly, the non-sterilized soil was separated into two groups: one group was inoculated with Rhizophagus irregularis MUCL 41,833 (AMF), while the other group was left un-inoculated. This AMF strain was sourced from the Glomeromycota in vitro Collection (GINCO; www.mycorrhiza.be/ginco-bel), which is a commercially available strain of AMF. The inoculum was applied at a rate of 10 g per pot (20 × 17.5 cm), with each gram of soil containing roughly 50 spores. The non-inoculated control treatment used autoclaved inoculum that provided the same nutrients as the experimental treatment but did not contain any mycorrhizal spores. Following AMF treatment, seeds were planted into individual pots containing a standard potting mix of peat and perlite. Plants were grown for two weeks under optimal conditions to ensure recovery and growth before infestation treatments. The second treatment was the infestation with grain aphids (Sitobion avenae) at two levels (infested vs. non-infested). Accordingly, wheat seedlings were artificially infested by placing a controlled density of 20 aphids per seedling onto the abaxial side of the leaves (the first fully expanded leaf) to ensure uniform distribution. Non-infested control groups were maintained in the same conditions without introducing aphids. We performed stringent measures to prevent cross-contamination between aphid-infested and non-infested plants, including the use of separate growth chambers and dedicated tools for each group. Frequent monitoring was conducted to promptly address any signs of cross-contamination, thereby enhancing the validity of our experimental outcomes.

In addition, each plant received a one-time dosage of 16.5 g per plant of a commercial organic fertilizer with a balanced N-P-K ratio of 4-4-4, along with micronutrients including calcium, magnesium, iron, manganese, and zinc, to enhance nutrient availability without overwhelming the plants or confounding the effects of AMF inoculation. Throughout the experiment, the pots were consistently watered. After two weeks of the application of infestation treatment, the plants were harvested and subjected to biochemical and physiological assessment. The experiment was conducted in three replicates to ensure reliability and accuracy of the results.

Assessment of mycorrhizal colonization

The method developed by Giovannetti and Mosse [16] was used to evaluate the mycorrhizal colonization in the roots. The procedure began with dividing root samples into segments measuring 1 cm each. These segments were then preserved in a fixing solution containing formalin, acetic acid, and alcohol, mixed in a 5:5:90 ratio. Subsequently, they were autoclaved in a 10% potassium hydroxide (KOH) solution for 15 min. After clearing, we neutralized the samples using a 1% hydrochloric acid (HCl) solution for approximately 5 min.

Next, the roots were stained by heating them in a 0.05% trypan blue lactoglycerol solution for 10 min. Following staining, we selected ten random 1 cm root segments to place on a microscope slide for further analysis. Under microscopic observation, we searched for fungal structures, including hyphae and arbuscules. We then measured the length of fungal infection in centimeters for each root segment, calculated the average length across all ten segments, and expressed the results as a percentage reflecting the overall extent of mycorrhizal colonization.

Assessment of photosynthetic rate and pigment

Photosynthesis rates of the treated wheat seedlings were measured using a LI-COR portable photosynthesis system, as expressed in µmol CO2 m− 2 s− 1 [17]. To prepare plant samples for analyzing photosynthesis pigments, tissue homogenization was performed using a MagNALyser (Roche, Vilvoorde, Belgium) at 7000 rpm for one minute, followed by centrifugation at 14,000× g for 20 min at 4 °C. The resulting supernatant was filtered through an Acrodisc GHP filter (0.45 μm, 13 mm; Gelman, Ann Arbor, MI, USA) to remove particulate matter. The filtered samples were then analyzed by high-performance liquid chromatography (HPLC) using a Shimadzu SIL10-ADvp system (Kyoto, Japan) with a reversed-phase setup maintained at 4 °C. Pigments were separated on a C18 silica column (Waters Spherisorb, 5 μm ODS1, 4.6 × 250 mm) heated to 40 °C. The mobile phases employed were (A) a mixture of 81:9:10 acetonitrile/methanol/water and (B) a mixture of 68:32 methanol/ethyl acetate, with a flow rate set at 1.0 mL/min at room temperature [18]. Pigments were detected using a diode-array detector (Shimadzu SPD-M10Avp, Kyoto, Japan). Concentrations of the pigments were calculated using Shimadzu Lab Solutions Lite software.

Mineral content analysis

The mineral content analysis began with the digestion of 200 mg samples collected from treated and control wheat plants, following the established protocols from previous studies [19, 20]. The shoot tissue samples were digested using a mixture of nitric acid (HNO3) and distilled water in a ratio of 5:1. Following digestion, the macro- and micro-elements present in the samples were quantified using inductively coupled plasma mass spectrometry (ICP-MS) with a Finnigan Element XR system (Scientific, Bremen, Germany). A 1% nitric acid solution was employed as the standard during the analysis process to ensure accurate measurements. This methodology allowed for a precise determination of the mineral composition in both treated and control plant samples.

Analysis of antioxidant molecules and total antioxidant capacity (FRAP)

The polyphenol content was measured using the Folin-Ciocalteu assay, with gallic acid as the standard reference [21]. Flavonoid content was assessed using a modified aluminum chloride colorimetric method, with quercetin as the standard [22]. For this analysis, the powdered shoot tissues (1 g) were mixed with 10 mL of methanol or a methanol-water mixture and subjected to ultrasonic extraction for 30 min to facilitate the release of bioactive compounds. HPLC was employed to identify and quantify the phenols and flavonoid compounds, utilizing their standards and relative retention times; the peak areas of standards corresponded to the amounts of each compound present. HPLC analysis was performed to detect tocopherols in shoot tissues following the protocols outlined in the references [22]. Tocopherols were separated using a Particil Pac 5 μm column (250 mm length, 4.6 mm diameter), and quantification was achieved with a Shimadzu system operating in normal phase conditions, coupled with a fluorometric detector (excitation at 290 nm, emission at 330 nm). HPLC was also used to determine reduced glutathione (GSH) and ascorbate (ASC) levels [23, 24].

The total antioxidant capacity was assessed using the ferric-reducing antioxidant power (FRAP) method. Sample extraction was conducted using 80% ethanol, and the extracts were centrifuged for 20 min at 4 °C and 14,000× g. The FRAP reagent was prepared by mixing 20 mM FeCl3 with acetate buffer (0.25 M). Approximately 0.25 mL of the FRAP reagent was combined with 0.1 mL of the sample extract, and absorbance was measured at 593 nm, as described in [25]. The results were expressed in micromoles of Trolox per gram of fresh weight (µmol trolox g− 1 FW).

Amino acid analysis

To assess the amino acid profile, shoot samples were homogenized in an 80% v/v ethanol solution. The homogenate was centrifuged at 14,000 rpm for 20 min to separate the solid residue from the liquid fraction. After removing the supernatant, it underwent vacuum evaporation to concentrate the extract. The remaining pellet was subsequently resuspended in chloroform for further extraction. Another centrifugation at 14,000 rpm for 10 min generated a new supernatant filtered through a Millipore microfilter with a pore size of 0.2 μm to ensure clarity. To facilitate accurate quantification, deuterium L-glutamine-2,3,3,4,4-d5 was added as an internal standard. The filtering and dilution steps prepared the sample for analysis. For the detection, separation, and quantification of amino acids, a BEH amide column was employed using a Waters Acquity UPLC-TQD system [26]. This setup allowed for precise analysis of the amino acid profile present in the shoot samples.

Determination of nitrogen content and metabolism

Total nitrogen content in shoot samples was determined by digesting 0.2 g of the samples in sulfuric acid at 260 °C, followed by analysis with a CN element analyzer (NC-2100, Carlo Erba Instruments, Milan, Italy) [18]. To measure the activity of glutamine synthetase (GS) and glutamine 2-oxoglutarate aminotransferase (GOGAT), fresh samples were homogenized with pre-chilled Tris–HCl buffer and then centrifuged to obtain supernatants. GS activity was measured using a reaction mixture containing multiple substrates and components, in which the reaction was incubated at 35 ºC for 30 min and terminated with FeCl3 [27]. The absorbance was recorded at 540 nm, and GS activity was calculated based on the formation of γ-glutamyl hydroxamate, with one unit defined as 1 µmol produced per mg of fresh tissue per hour. For GOGAT activity, enzyme solution was combined with specific substrates and incubated at 30 ºC. The reaction was halted by boiling, and the absorbance was measured at 340 nm. One unit of GOGAT activity was defined as the decrease of 1 µmol of NADH per minute [28].

Nitrate reductase (NR) enzyme activity was assessed using a modified method from Khator and Shekhawat [29]. Fresh shoot samples were homogenized in a pre-cooled mortar with a potassium phosphate buffer containing cysteine, EDTA, and BSA, followed by centrifugation to obtain the supernatant for analysis. The NR activity assay involved mixing the enzyme solution with additional buffer, potassium nitrate, and NADH, and incubating the mixture at 25 °C for 30 min. After incubation, sulphanilamide and α-naphthylamine were added, and the reaction was allowed to proceed for another 15 min before centrifugation. The supernatant was then measured for absorbance at 540 nm.

Arginase activity was assessed based on the conversion of arginine to urea. The reaction mixture comprised manganese chloride, Tris buffer, and mM L-arginine. The mixture was incubated for 30 min at 37 °C. The reaction was initiated by adding the enzyme and terminated by adding 50% trichloroacetic acid. Following centrifugation to remove proteins, the urea concentration in the supernatant was measured calorimetrically, with one unit of arginase activity defined as the production of 1 µmol of urea per minute [30]. Threonine synthase (TS) activity was assessed by measuring threonine production from homoserine, utilizing assays based on HPLC [31]. Methionine synthase (MS) activity measurement involved conducting anaerobic assays using titanium citrate as a reductant. The assay mixture included potassium phosphate buffer, homocysteine, AdoMet, NADPH, and radiolabeled H4folate, with the reaction incubated at 37 °C before being terminated by heating. Methionine production is then quantified through chromatography, with activity expressed as the formation of 1 pmol of methionine per minute [32]. Serine acetyltransferase, which catalyzes the synthesis of acetylserine from serine and acetyl-CoA, can be evaluated using spectrophotometric methods that rely on the formation of acetylserine measured through absorbance at 412 nm [33]. Total protein content was quantified using the Lowry method [34].

Antimicrobial activity assessment

The antimicrobial activity of plant extracts was assessed using the disc diffusion method. Microbial suspensions (100 µL) were spread on Muller-Hinton and MRS agar plates, onto which filter paper discs containing the plant extracts (5 mg mL− 1 in ethanol) were placed. The plates were held at room temperature for 30 min before incubation. The extracts were tested against both bacteria and fungi pathogens, with positive controls, including standard antibiotics. These strains were selected due to their significance as pathogens and their differing structural characteristics that influence their susceptibility to antimicrobial agents. Inhibition zones surrounding the discs were measured to determine the extracts’ microbicidal effects [35].

Aphid dynamics

The intrinsic rate of natural increase (rm) is calculated using the formula rm = (ln(Nt) - ln(N0)) / t, where Nt is the number of individuals at time t, and N0 is the initial population size, providing insight into population growth over a defined period [36]. The apterous rate was assessed by examining morphotype distributions within the population after two weeks [37]. For body weight measurement, newly matured aphids were individually weighed, ensuring that all measurements were conducted under identical conditions to eliminate variability.

Statistical analyses

Statistical analyses were completed using IBM SPSS Statistics version 19 (SPSS Inc., Chicago, IL, USA). Each treatment was replicated three times to ensure sufficient data for reliable statistical evaluation. The one-way and two-way analysis of variance (ANOVA) was performed to assess the differences between the means of the various treatments. This method was appropriate as it allowed us to examine the effects of individual treatments (such as AMF inoculation) on measured parameters, thereby controlling for variations within the experimental groups. Following the ANOVA, Tukey’s Honestly Significant Difference (HSD) test was employed as a post hoc test for separation of means, with a significance threshold set at p < 0.05. This test is particularly useful for identifying which specific means are statistically different from each other when we reject the null hypothesis in ANOVA. Moreover, a t-test was utilized to analyze specific parameters related to aphid populations, including body weight, intrinsic rate of natural increase, and apterous rate. This statistical test was conducted to determine significant differences between the groups, again maintaining a significance level of 0.05.

Results

Mycorrhizal colonization

The findings of the analysis of AMF root colonization are given in Fig. 1. The data indicates that infestation of the plants with grain aphids resulted in a considerable decrease in root colonization, which showed a 26.8% reduction in infested plants compared to those non-infested (p < 0.05). In addition to root colonization, the length of fungal hyphae also significantly decreased, experiencing a 30.7% reduction compared to non-infestation conditions (p < 0.05). However, there was no significant difference in the number of arbuscules in infected and non-infected plants (Fig. 1).

Fig. 1
figure 1

AMF root colonization (%), hyphal length (cm g− 1 soil) and number of arbuscules (no. cm− 1 root) in plants in response to grain aphids infestation. * and ns indicate significant difference at 0.05 statistical level (p < 0.05) and non-significant based on a t-test, respectively

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Plant biomass and photosynthesis parameters

The results showed that AMF significantly improved various physiological parameters in wheat plants subjected to grain aphid infestation compared to the control groups. In this regard, AMF application enhanced plant fresh weight, indicating a robust growth response, with an approximate increase of 51.2% compared to the control treatment in infested plants (p < 0.05) (Fig. 2, Supp Table 1). Moreover, photosynthetic rate measurements revealed a notable increase of 37.9% in AMF-treated plants under infestation conditions compared to un-treated infested plants (p < 0.05), suggesting improved photosynthetic efficiency. Although this photosynthetic rate was significantly lower (− 28.3%) compared to plants treated with AMF in non-infested conditions (Fig. 2, Supp Table 1).

Fig. 2
figure 2

Effects of arbuscular mycorrhizal fungi (AMF) on wheat plants’ fresh weight and photosynthetic parameters under infestation by grain aphid and non-infested conditions. At a 5% probability level, the Tukey HSD test reveals that means sharing the same letter(s) are not significantly different

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The chlorophyll content, specifically chlorophyll a, was also significantly higher in AMF-treated plants under infestation, showing a 47.5% increase over control values in infested plants (p < 0.05), however, non-infected plants did not show a significant reaction to the application of AMF (p ≥ 0.05). For chlorophyll b, the opposite results were obtained, in which the treatment of AMF only increased chlorophyll b’s concentration in non-infested plants (p < 0.05). In contrast, the accumulation of β-carotene pigment was influenced by infestation treatment, which was about 80–100% higher in infested plants than those in non-infested (p < 0.05). However, the same results were observed for lutein content in infested plants, which were significantly higher (+ 72–192%) than those in non-infested (p < 0.05, Supp Table 1), AMF application improved lutein content under non-infested conditions compared to the control group (p < 0.05). The content of neoxanthin and violaxanthin reached the highest values in the control plants and AMF-treated plants under infestation conditions, respectively, which were significantly greater than other treatments (p < 0.05) (Fig. 2, Supp Table 1).

Amino acids composition

Then we investigate the amino acid composition after assessing nitrogen metabolism since amino acids are direct products of nitrogen metabolism and serve as key indicators of plant stress responses and adaptations. In this regard, notable changes were observed under both infested and non-infested conditions (Fig. 3). Under infestation by grain aphids, the application of AMF led to significant increases in the concentrations of several amino acids compared to the non-treated plants under both infestation and non-infestation treatments. For instance, asparagine levels increased by approximately 23% in AMF-treated infested plants compared to the control. Similarly, glutamine content showed a rise of 20%, reflecting the enhancing effect of AMF under infestation conditions. The heat map generated from hierarchical clustering analysis illustrated these differential responses, highlighting the considerable shifts in amino acid composition due to infestation treatment (Fig. 3). It particularly emphasized the elevated asparagine, proline, glutamine, and serine levels, which exhibited increases of around 38–46%, 136–178%, 139–164%, and 24–53%, respectively under infestation conditions when compared to non-infested plants.

Fig. 3
figure 3

A heat map generated using hierarchical clustering analysis with Ward’s method illustrated the variations in amino acid content that were distinctly affected by both grain aphid infestation and AMF treatment in the wheat plants. The accompanying color gradient at the bottom of the panel, spanning values from 0 to 3, indicates the levels of the measured parameters

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Nitrogen metabolism

The effects of AMF on nitrogen metabolism were evaluated to determine its potential role in enhancing plant resilience and metabolic responses in wheat under both normal and infested conditions. The results interestingly showed that although the nitrogen content in the control treatment in the infected plants reached its highest level, this treatment had the lowest total protein content, which was almost half of the content in the other treatments (p < 0.05) (Table 1). The activity of NR, GS, GOGAT, and TS was significantly increased by about 3.2, 1.9, 4.3, and 4.8 times in infested plants treated with AMF compared to those non-treated, respectively, while it remained stable in non-infested plants (p ≥ 0.05, Supp Table 1). Although the activity of the arginase enzyme decreased significantly in response to the infestation treatment in untreated plants (p < 0.05), the application of AMF caused a significant increase in its activity in infested (+ 48.6%) and non-infested (+ 290.5%) conditions. Moreover, both infestation treatment and application of AMF increased MS enzyme activity, the effect of which was more pronounced in plants treated with AMF under infestation conditions. Also, the activity of GDH and SAT was increased in response to AMF treatment, in which the highest activity was observed in AMF-treated plants under infestation conditions (p < 0.05) (Table 1, Supp Table 1).

Table 1 Effects of arbuscular mycorrhizal fungi (AMF) on nitrogen metabolism (± standard deviation) of wheat plants under infestation by grain aphid and non-infested conditions
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Antioxidant metabolites

Moreover, the present study assessed the content of antioxidant molecules as they collectively elucidate the plant’s physiological responses to biotic stress. The results indicated that in non-infested plants, AMF application significantly enhanced flavonoids (by 40.0%), the FRAP (by 37.1%), GSH (by 43.3%), alpha tocopherols (by 33.9%), and gamma tocopherols (by 35.5%) compared to the non-treated plants (p < 0.05). Under infestation by grain aphids, AMF treatment resulted in pronounced increases in polyphenols (+ 95.1%), alpha tocopherols (+ 42.7%), beta tocopherols (+ 41.4%) and gamma tocopherols (+ 36.9%) compared to those non-treated (p < 0.05). Nevertheless, all antioxidant parameters reached the highest value in the AMF-treated plants under infestation conditions (Table 2, Supp Table 1).

Table 2 Effects of arbuscular mycorrhizal fungi (AMF) on antioxidants content (± standard deviation) of wheat plants under infestation by grain aphid and non-infested conditions
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Mineral content in shoot tissues

The mineral content in shoot tissues was assessed in the present research as these nutrients are vital for plant physiological processes and stress responses. The results indicated that AMF significantly enhanced the mineral content of wheat plants under both non-infested and infested conditions (Fig. 4). While the infestation treatment significantly decreased P content in control plants (p < 0.05), the application of AMF effectively maintained P level without any significant reduction when compared to non-infested conditions (p ≥ 0.05). K levels rose by 48.9% in non-infested conditions and by 65.5% when infested in response to AMF application (p < 0.05). Although Mg, Zn, and Ca showed no significant change in non-infested plants (p ≥ 0.05), they did exhibit a significant rise of 49.1%, 58.3%, and 62.5% in infested plants treated with AMF treatment, respectively (p < 0.05). The higher Fe level was found in AMF-treated plants under infestation conditions, which was significantly higher than that in control plants under non-infestation conditions (+ 41.1%), while it had not a significant difference with the control group in infested plants (Fig. 4).

Fig. 4
figure 4

Effects of arbuscular mycorrhizal fungi (AMF) on wheat plants’ mineral content (mg g-1 DW) under infestation by grain aphid and non-infested conditions. At a 5% probability level, the Tukey HSD test reveals that means sharing the same letter(s) is not significantly different

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Antimicrobial activity

The effects of AMF on the antimicrobial potential of plant extracts were evaluated under both infested and non-infested conditions, with results summarized in Table 3. In non-infested conditions, the antimicrobial activity against 8 studied pathogens increased with AMF treatment, among which, the inhibition zone in the Staphylococcus epidermidis and Enterobacter aerogenes treated plates was more pronounced than others (p < 0.05). Almost similar results were observed under infested conditions. In this regard, the significant antimicrobial effects of AMF were found against Staphylococcus epidermidis, Enterococcus faecalis, Streptococcus salivarius, Proteus vulgaris, Salmonella typhimurium, Candida albicans, and Aspergillus flavus, which were about 30–67% higher than those in the plant extracts from non-treated plants (p < 0.05).

Table 3 Effects of arbuscular mycorrhizal fungi (AMF) on antimicrobial potential of plant extract (± standard deviation) under infestation by grain aphid and non-infested conditions by assessing the inhibition zones (mm)
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Aphid dynamics

The intrinsic rate of natural increase (rm), apterous rate, and body weight of aphids were investigated in infested plants, as these parameters provide insights into the population dynamics and potential impacts of aphid infestations on crop health. The results indicated that in infested plants treated with AMF, the intrinsic rate of natural increase (rm) of aphids decreased significantly from 0.25 per day in the control treatment to 0.16 per day, representing a 36% reduction (p < 0.05) (Fig. 5, Supp Table 1). The apterous rate also showed a notable decline, dropping from 84% in the control to 61%, indicating a 27.4% decrease (p < 0.05). Additionally, the body weight of the aphids was affected, with averages decreasing from 268 µg in the control group to 178 µg in the AMF-treated infested plants, reflecting a 33.8% reduction (p < 0.05) (Fig. 5, Supp Table 1).

Fig. 5
figure 5

Effects of arbuscular mycorrhizal fungi (AMF) on intrinsic rate of natural increase (rm) of aphid, apterous rate and aphid body weight in the infestation wheat plants. * indicates p < 0.05 based on a t-test

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Discussion

The results presented in this study highlight the multifaceted effects of AMF on wheat plants subjected to both grain aphid infestation and non-infested conditions. Our findings suggest that AMF acts through various physiological and biochemical pathways to enhance plant resilience against aphid stress, impacting photosynthesis parameters, nitrogen metabolism, amino acid composition, antioxidant metabolites, and mineral content in shoot tissues.

The infestation of grain aphids produces various detrimental effects on plants. Feeding by aphids disrupts phloem function, reducing nutrient transport and allocation and impairing overall plant growth and development [38]. Moreover, aphids often induce physiological changes in plants that make them more vulnerable to secondary infections from pathogens [39]. This secondary effect can further complicate the plant’s defensive responses. Grain aphids also excrete honeydew on which black sooty mold can grow, reducing photosynthetic efficiency by blocking light [40].

Photosynthesis is a critical process underlies plant growth and productivity [41]. Our results indicate that AMF application significantly enhanced photosynthetic efficiency in wheat plants, even under aphid infestation. Improved chlorophyll content and parameters like photosynthetic rate were observed, which aligns with previous studies that found AMF enhances chlorophyll biosynthesis and optimizes light absorption [42, 43]. This increase in photosynthetic activity may be attributed to the protective roles of AMF against disruptions caused by aphid feeding. Aphid infestation can lead to decreased chlorophyll content and consequently reduced photosynthesis, resulting from physical damage to plant tissues and the potential induction of stress responses [44]. AMF’s facilitation of enhanced photosynthetic parameters suggests it may help stabilize or even elevate photosynthesis in stressed plants, leading to more significant biomass accumulation and improved stress mitigation.

The results demonstrate that N metabolism was positively influenced by AMF application. As established in prior research, AMF can regulate the activity of enzymes involved in nitrogen metabolism (e.g., NR, GDH, GOGAT, and GS), enhancing nitrogen assimilation, which is crucial for photosynthesis and plant growth [45]. The increase in nitrogen metabolites is particularly important during aphid stress, as aphid feeding often leads to mineral deficiencies due to nutrient diversion to herbivorous pests [46]. Enhanced amino acid levels, particularly essential amino acids such as glutamate and aspartate, contribute to stress tolerance by serving as precursors for signaling molecules and protective compounds in plants [47, 48]. This augmentation in amino acid pool can bolster the plant’s defense mechanisms against aphids, potentially enhancing the synthesis of phenolic compounds and other secondary metabolites involved in plant defense [46, 49].

Interestingly, as nitrogen content increased, the total protein content in infected plants decreased. An explanation can be the effects of stress factors, which can impair nitrogen assimilation and utilization, leading to reduced protein synthesis despite sufficient nitrogen availability [50]. In such situations, plants may prioritize energy and resources for survival rather than protein production, causing discrepancies between nitrogen content and total protein levels. Moreover, stress can affect the pathways responsible for amino acid synthesis and protein accumulation [51], lowering protein levels even when nitrogen levels are adequate. Therefore, while nitrogen is essential for protein synthesis, its effective utilization can be compromised under stress, potentially leading to decreased protein levels in stressed plants.

The role of antioxidants in plant defense is well-documented, and our findings indicate that AMF-treated wheat exhibited elevated levels of antioxidant metabolites. The increase in antioxidant content suggests that AMF enhances the oxidative stress response, thereby protecting the plant from damage inflicted by aphids. Aphid feeding can lead to localized oxidative stress due to the injection of salivary proteins which trigger defense responses, creating an environment rich in reactive oxygen species (ROS) [52]. Therefore, the observed increase in antioxidant compounds in AMF-treated plants likely plays a crucial role in quenching these ROS, mitigating oxidative damage. These results underscore the potential of AMF to improve plant resilience not only through direct enhancement of antioxidant pathways but also by buffering the oxidative effects of aphid infestation. Moreover, the link between antioxidant molecules and nitrogen metabolism in infested plants lies in the fact that nitrogen is a crucial element for the synthesis of amino acids, which are precursors to many antioxidants [53], thereby influencing the plant’s ability to produce these protective compounds in response to stress from grain aphid infestation. Furthermore, the results showed that the AMF treatment significantly promotes the antimicrobial potential of plant extracts. This enhancement appears to correlate with a rise in phytochemical content, especially flavonoids and polyphenols, found in the present research. These phytochemicals are recognized for their ability to improve antimicrobial effectiveness, as supported by previous studies [54, 55].

Mineral content analysis revealed a significant increase in essential nutrients such as N, P, and K in AMF-treated plants. These minerals play crucial roles in plant metabolism, growth, and stress response [56]. AMF possibly enhances root development and promotes efficient nutrient uptake, as previous studies suggest that AMF can stimulate root architecture and function [57]. Aphid infestation can disrupt nutrient flow within the plant, often leading to imbalances in essential nutrients and deficiencies that may compound the stress on the host [58]. By improving mineral content, AMF-treated plants can better withstand aphid attacks under a balanced nutrient status.

Based on the results, the application of AMF is associated with reduced aphid body weight and decreased intrinsic increase rates, providing strong evidence for heightened plant resistance. This reduction in aphid population dynamics can be attributed to a multifaceted enhancement of the plant’s physiological and biochemical defences. Firstly, improved nutritional status is a key factor. AMF enhances nutrient uptake efficiency, particularly nitrogen, which is crucial for synthesizing amino acids and proteins necessary for plant defense mechanisms [59]. Enhanced nitrogen assimilation likely leads to the production of specific proteins that can function as defensive compounds, helping to deter aphid feeding [60]. Secondly, the enhanced antioxidant capacity observed in AMF-treated plants plays a critical role. Aphid feeding is known to induce oxidative stress within the plant due to the introduction of salivary proteins that trigger defense responses and increase ROS levels [52]. The elevated antioxidant metabolites, such as flavonoids and polyphenols, in AMF-treated plants are believed to counteract this oxidative damage, maintaining plant health and vigor [61]. This oxidative stress response not only protects the plant from direct damage but may also facilitate a more robust growth environment, allowing for improved defense strategies against subsequent aphid attacks [62]. Further, AMF treatment has been shown to boost the production of secondary metabolites, which include defensive compounds [63]. These metabolites serve dual roles as direct repellents or toxins against herbivores and as signaling molecules that can activate further defense mechanisms within the plant [64]. The increased synthesis of these compounds in response to AMF colonization indicates a well-prepared defensive architecture, ready to respond to herbivore pressure more effectively. As a result, AMF not only mitigates the impact of aphid feeding but also reinforces the plant’s defensive structures, creating a feedback loop that enhances resilience. Increased levels of these defensive compounds, along with improved growth and nutrient status, lead to decreased aphid population dynamics, as evidenced by lower aphid body weights and growth rates.

The results of the present research support the fact that AMF has emerged as a promising biocontrol agent in pest management, particularly in promoting plant health and enhancing nutrient uptake. Compared to chemical pesticides, which often provide immediate but potentially harmful effects on non-target organisms and the environment, AMF offers a more sustainable and environmentally friendly alternative [65]. While chemical pesticides can rapidly reduce pest populations, their residual toxicity can lead to ecosystem imbalances [66]. Compared to other biocontrol methods, such as predatory insects or parasitoids, AMF can have a broader impact on plant health and soil fertility but may require longer periods to establish and effect change [67]. While our research demonstrates the beneficial effects of AMF on wheat plants in terms of enhancing resistance to grain aphid infestation, several limitations should be considered. Firstly, the study primarily focuses on a single crop species in controlled conditions, which may not fully capture the complexities of field dynamics, including variations in environmental factors and other biotic interactions present in natural settings. Additionally, while we observed significant improvements in physiological and biochemical parameters, the underlying molecular pathways and the long-term effects of AMF application on pest dynamics remain to be elucidated. Future research should aim to explore these molecular mechanisms and assess the efficacy of AMF in diverse agricultural systems and other crop species to determine its broader applicability in integrated pest management strategies.

Conclusion

Utilizing AMF in wheat cultivation stimulates significant physiological and biochemical enhancements that fortify the plants’ resilience to grain aphid infestations. The noted advancements in photosynthesis, nitrogen metabolism, antioxidant defenses, and mineral content, alongside their impact on aphid population dynamics, highlight AMF’s potential role as a biocontrol agent within sustainable agricultural practices. This research sets the groundwork for creating integrated pest management strategies aimed at boosting crop resistance to pests, which can, in turn, contribute to environmental sustainability by reducing chemical pesticide use, and economic sustainability through improved crop growth.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2025R83), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

Funding

Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2025R83), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

Author information

Authors and Affiliations

  1. Department of Biology, College of Sciences, Princess Nourah bint Abdulrahman University, P.O. Box 84428, Riyadh, 11671, Saudi Arabia

    Hana Sonbol & Shereen Magdy Korany

  2. Botany and Microbiology Department, Faculty of Science, Assiut University, Cairo, 71515, Egypt

    Mousa nhs

  3. Department of Basic Sciences, Deanship of Preparatory Year and Supporting Studies, Imam Abdulrahman Bin Faisal University, P.O. Box 4030, Jubail, 35816, Saudi Arabia

    Insaf Abdi

  4. Centro de Investigaciones Biotecnológicas del Ecuador (CIBE), Escuela Superior Politécnica del Litoral, ESPOL, Campus Gustavo Galindo, Km. 30.5 Vía Perimetral, Guayaquil, 090902, Ecuador

    Maria Gabriela Maridueña-Zavala

  5. Department of Botany and Microbiology, Faculty of Science, Beni-Suef University, Beni-Suef, 62511, Egypt

    Emad A. Alsherif

  6. Public Health Department, College of Health Sciences, Saudi Electronic University, Riyadh, 23442, Saudi Arabia

    Danyah A. Aldailami

  7. College of Science, Arar, Department of Biological Science, Northern Border University, Arar, 25698, Saudi Arabia

    Salma Yousif Sidahmed Elsheikh

Authors
  1. Hana Sonbol
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  2. Shereen Magdy Korany
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  3. Mousa nhs
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  4. Insaf Abdi
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  5. Maria Gabriela Maridueña-Zavala
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  6. Emad A. Alsherif
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  7. Danyah A. Aldailami
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  8. Salma Yousif Sidahmed Elsheikh
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Contributions

H.S.: Conceptualization, investigation, writing—original draft preparation. S. M. K.: methodology, investigation, writing— review & editing. M.N.: writing— review & editing. I.A.: methodology, investigation. M.G.M.Z.: Writing - review & editing. E.A.A.: Writing - review & editing. D.A.A.: Conceptualization, data curation, supervision, project administration. S.Y.S.E.: Conceptualization, data curation, supervision, project administration,

Corresponding author

Correspondence to Maria Gabriela Maridueña-Zavala.

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Sonbol, H., Korany, S.M., nhs, M. et al. Exploring the benefits of AMF colonization for improving wheat growth, physiology and metabolism, and antimicrobial activity under biotic stress from aphid infection. BMC Plant Biol 25, 198 (2025). https://doi.org/10.1186/s12870-025-06196-4

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Keywords

BMC Plant Biology

ISSN: 1471-2229

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