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. 2024 Nov 25;24:1119. doi: 10.1186/s12870-024-05824-9

Effect of arbuscular mycorrhizal fungi on physiological, bio-chemical and yield characters of wheat plants (Triticum aestivum L.) under drought stress conditions

Khaled Abdelaal 1,✉, Abdulaziz Alaskar 2,✉, Yaser Hafez 3
PMCID: PMC11587776  PMID: 39581979

Abstract

This experiment was conducted to study the effect of inoculation with arbuscular mycorrhizal fungi (AMF) as an ecofriendly strategy on physiological, biochemical and yield characters of wheat plants. Our results showed a significant decrease in chlorophyll a and b as well as the maximum quantum efficiency of PSII (Fv/Fm) in wheat plants under drought conditions compared to control in the two seasons. Drought stress significantly reduced relative water content (RWC%) in the stressed plants compared with the control. Additionally, 1000 grain weight (g) and biological yield (t h− 1) were reduced significantly under drought stress. Furthermore, hydrogen peroxide (H2O2), Superoxide (O2−), electrolyte leakage (EL%), lipid peroxidation (MDA) and total phenolic compounds were increased significantly in the stressed plants under drought conditions. However, wheat plants treated with AMF displayed a significant increase in chlorophyll concentrations and the maximum quantum efficiency of PSII as well as RWC% in the stressed wheat plants when compared with the stressed untreated plants. Our findings also indicated that application of AMF led to regulate the antioxidant enzymes activity, proline content and decrease hydrogen peroxide (H2O2), Superoxide (O2−), electrolyte leakage (EL%) and lipid peroxidation (MDA) levels in the drought stressed wheat plants. Eventually, application of AMF as ecofriendly approach can improve wheat growth and grain yield of wheat plants by mitigating the adverse effects of drought stress. These results provide evidence for the important role of AMF in agricultural production and maximizing wheat grain yield.

Keywords: Wheat, Drought, AMF, Chlorophyll, Antioxidant enzymes, ROS, MDA

Introduction

Climate changes have a significant impact on agricultural soil and crop production all over the world. According to climate changes, the economic crops are exposed to various stresses, such as biotic stress [1–4] and abiotic stress [5, 6] like salinity [7–10] and drought [11–13]. Drought is one of the most effective stresses on plants [14–16], it is considered a main threat worldwide and extremely affect the plant growth and yield [17, 18]. The morphological traits like plant length and leaves number were significantly decreased [19, 20]. Also, chlorophyl content and RWC were markedly reduced under water deficit conditions [21, 22]. Enzymatic and nonenzymatic antioxidant system such as catalase, superoxide dismutase and peroxidaseas well as proline were significantly augmented in the drought stressed plants such as faba bean [23], and wheat [24]. Additionally, one of the response mechanisms to drought conditions is the overproduction of reactive oxygen species like superoxide and hydrogen peroxide [25, 26]. Furthermore, lipid peroxidation was significantly increased and recorded as malondialdehyde (MDA) under drought stress [27]. Cell membrane stability index (CMSI) was increased significantly under stress conditions, in this regard, Ghanem and Al-Farouk [17] reported that cell membrane stability index was increased significantly in the drought stressed wheat plants. Wheat is one of the most important plants worldwide, it’s production usually suffer from many environmental factors such as plant pathogens [28–30], salinity [31] and drought [32]. The yield production can be improved using ecofriendly strategies such as plant growth promoting bacteria [33, 34] and arbuscular mycorrhizal fungi (AMF) under stress conditions. AMF are ecofriendly approaches in agricultural sustainability under abnormal conditions, they can improve the growth and productivity of many plants because of their role as bio stimulants [35].

AMF can help plants to grow strongly under stress conditions via mediating many physiological processes between AMF and the host plant to improve photosynthetic rate and other traits [36], as well as increase water uptake. Masrahi et al. [36] found that application of AMF led to improve yield, and nutrients elements of the salt stressed barley plants. AMF may improve agroecosystem performance and sustainability; they can increase the yield production by allocating extra nutrients to plant tissues associated with stress alleviation [37]. AMF, especially under stressful environmental conditions, can efficiently enhance growth and productivity of several plants [38–41]. AMF may induce many changes in host plants to cope with the environmental stress factors such as heavy metals [42]. AMF can directly or indirectly effect on the plants under stress via increasing nutrient availability and transport through extracellular fungal hyphae, improving soil fertility and consequently improving plant stress tolerance [40]. AMF not only help plants absorb P from the soil, but also transport great amounts of N to the host plant. The enhancement role of AMF was recorded also on the growth and yield production of rice plants [43]. Recently, many studies are being conducted to use natural alternatives to improve crop productivity under different stress conditions. Thus, the objective of this study was to assess the role of arbuscular mycorrhizal fungi as a promising approach in improving wheat growth and yield under drought conditions. To test our hypotheses, we examined the morpho-physiological and biochemical parameters to better understand the potential mechanisms regulating plant adaptation to drought stress under AMF application.

Materials and methods

Experimental design

The pots experiments were accomplished during two seasons (2022/2023 and 2023/2024) to evaluate the impact of arbuscular mycorrhizal fungi (AMF) in mitigating the effects of drought stress on wheat plants. The morphological features and physio-biochemical characters were studied on wheat (Triticum aestivum L.) plants (Sids 12 cultivar) under drought stress (70% field capacity). Wheat grains were obtained from Agricultural research center, Egypt. The physio-biochemical characteristics were studied and determined at EPECRS Excellence Center, Agricultural Botany Dept., Kafrelsheikh University. The experiment was organized in a completely randomized design with four treatments. The sowing date was at 11 November and 12 November during the two seasons, respectively. Each pot was field with 8 kg soil and contains 10 grains. The samples of soil were taken to study their properties. Soil texture was clay, Ca++ 6.57 mmol L− 1, Mg++ 3.64 mmol L− 1, K++ 0.43 mmol L− 1, Na++ 22.28 mmol L− 1, SO4− 14.98 mmol L− 1, HCO3− 2.32 mmol L− 1 and available N, P, and K was 28.2, 5.62 and 245 mg kg− 1 respectively. The fertilization rate of NPK was added, Nitrogen was used as urea at 140 kg ha− 1 Phosphorous was used at 240 kg ha− 1, however potassium was used at 125 kg ha− 1. AMF spores (Glomus sp. and Gigaspora sp.) [44] were extracted from the soil of the experimental farm, Kafrelsheikh University, Egypt and were identified according to Schenck and Perez [45] then were distributed with carriers into the soil at 5 cm depth before sowing at 30 kg ha− 1. All pots were irrigated well for three weeks, then the pots were exposed to drought (70% field capacity). The treatments were as the following:

  1. Control: plant irrigated well (90% field capacity).

  2. Control + AMF.

  3. Drought (70% field capacity).

  4. Drought + AMF.

The plants were chosen at 55 days from sowing in both seasons to study the physiological and biochemical characteristics as the following:

Physiological characters

Determination of chlorophyll a, b and relative water content (RWC%)

Flag leaf samples (0.5 g) were selected to chlorophyll extraction, the samples were extracted with 5mL N-N Dimethyl formamide. After keeping the samples in the refrigerator for 24 h, chlorophyll a and b were assayed at 647 and 664 nm spectrophotometrically [46].

For RWC% determination, some discuses of leaves were placed in distilled water, after 24 h the turgid weight was documented. The samples were dried (60 °C) for 72 h, then the dry weight was recorded. RWC% = (FW − DW)/(TW − DW) × 100 where FW: fresh weight, DW: dry weight, and TW: turgid weight [47].

Maximum quantum efficiency of PSII (Fv/Fm)

The chlorophyll fluorometer was used to measure Fv/Fm [48]. The maximum chlorophyll fluorescence (Fm) and the minimum (Fo) as well as variable fluorescence (Fv) were determined to calculate the maximum quantum efficiency of PSII (Fv/Fm) as follow: Fv/Fm = (Fm − Fo)/Fm.

Total soluble sugars determination

Total soluble sugar content was determined in fresh flag leaves as described by Trevelyan and Harrison [49].

Biochemical characters

Determination of electrolyte leakage (EL%) and lipid peroxidation (MDA)

Twenty discs of flag leaves were shaken water for 20 h with 25 cm3 deionized, the primary electrical conductivity was recorded. The samples were heated at 80 ◦C for 1 h, and shaken again for 20 h at 21◦C. The final conductivity was recorded. EL% = primary conductivity/final conductivity × 100 [50]. Lipid peroxidation was assayed as malondialdehyde (MDA) using spectrophotometer as µmol g− 1 FW. MDA = (6.45 × (A532 − A600) − (0.56 × A450)) ×V − W where V = volume (cm3); W = weight (g) [51].

Determination of hydrogen peroxide (H2O2) and superoxide (O2−)

H2O2 was measured in fresh flag leaves, 500 mg was macerated with 0.1% trichloroaceticacid (TCA) and homogenized at 4 °C with 3 mL K-phosphate buffer. The samples were centrifuged at 10,000 ×g for 10 min, then 3mL of supernatant was mixed with 1 mL of 0.1% TiCl4 in 20% H2SO4 (v/v), the mixture was centrifuged at 10,000 ×g for 12 min. H2O2 was measured spectrophotometrically and expressed as nmol g− 1 fresh weight [52]. O2− was measured in fresh flag leaves spectrophotometrically at 480 nm in the reaction mixture according to Yesbergenova et al. [53].

Proline and total phenolic compounds

A total of 500 mg fresh flag leaves were homogenized in 3% sulphosalicylic acid and centrifuged for 20 min at 3000 ×g according to Bats et al. [54]. The absorbance was recorded spectrophotometrically at 520 nm for proline measurements. Furthermore, total phenolic compounds were determined using the method of Singleton and Rossi [55], the absorbance was noted spectrophotometrically at 750 nm (µg mL− 1 gallic acid equivalent).

Determination of antioxidant enzymes [catalase (CAT), peroxidase (POD) and superoxide dismutase (SOD)

The samples of fresh flag leaves were ground in liquid nitrogen for protein extract as described by Bradford [56]. The activity of CAT, POD and SOD were assayed in supernatant according to Aebi [57], Hammerschmidt et al. [58] and Giannopolitis and Ries [59], respectively.

Determination of yield characters

At harvest stage 1000 grain weight (g) and grain yield (t h− 1) as well as biological yield (t h− 1) were determined.

Statistical analysis

Statistical analysis was performed using ANOVA according to Gomez and Gomez [60], when the difference was significant (P ≤ 0.05), the means between treatments were compared by according to Student’s t-test.

Results

Effect of drought and AMF on chlorophyll a, b and maximum quantum efficiency of PSII (Fv/Fm) in wheat plants

Drought stress significantly decreased (p ≤ 0.05) chlorophyll a, b and maximum quantum efficiency of PSII (Fv/Fm) in wheat seedlings compared to control plants in both seasons (Fig. 1). The obtained results exhibited that application of AMF significantly increased chlorophyll a, b and maximum quantum efficiency of PSII under drought conditions compared with the stressed untreated wheat plants. Concerning chl a and chl b, application of AMF led to improve wheat seedlings growth and give the best results of chl a and chl b in the stressed plants compared with other treatments in both seasons. Additionally, the maximum values of maximum quantum efficiency of PSII were recorded in the control treated wheat plants with AMF compared to the other treatments and without a significant deference when compared with control in the two seasons.

Fig. 1.

Fig. 1

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Effect of drought and AMF on Ch a (A), Ch b (B) and Fv/Fm in wheat plants during 2022/2023 and 2023/2024 seasons. Bars followed by different letters are significantly different according to Student’s t-test

Effect of drought and AMF on RWC% and proline content in wheat plants

Drought stress significantly decreased RWC% in the stressed wheat plants compared with the control in both seasons (Fig. 2). However, wheat plants treated with AMF exhibited a significant increase in RWC% comparing with the stressed untreated wheat plants in the two seasons. Our findings also showed that proline content was increased significantly in the drought stressed wheat plants compared with the control as a response to drought stress. Also, proline content was increased in the control treated plants (control + AMF) when compared with control untreated plants. Nevertheless, the inoculation with AMF led to regulate the concentration of proline in the stressed plants compared with the stressed uninoculated plants in both seasons (Fig. 2).

Fig. 2.

Fig. 2

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Effect of drought and AMF on RWC% (A) and proline (B) in wheat plants during 2022/2023 and 2023/2024 seasons. Bars followed by different letters are significantly different according to Student’s t-test

Effect of drought and AMF on Electrolyte leakage (EL%) and lipid peroxidation (MDA) in wheat plants

Drought stress significantly augmented EL% and MDA content in the drought stressed wheat plants compared to those of well water plants (control) in the two seasons. Nevertheless, inoculation with AMF significantly decreased the levels of EL% and MDA in the stressed plants compared with the stressed untreated plants. The best treatment which showed the lowest levels of EL% and MDA were control + AMF followed by control, then the stressed treated plants (drought + AMF) in both seasons (Fig. 3).

Fig. 3.

Fig. 3

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Effect of drought and AMF on EL% (A) and MDA (B) in wheat plants during 2022/2023 and 2023/2024 seasons. Bars followed by different letters are significantly different according to Student’s t-test

Effect of drought and AMF on reactive oxygen species (ROS) superoxide and hydrogen peroxide in wheat plants

In the present study, drought stress led to negative changes in cellular organelles associated with a significant increase in reactive oxygen species (ROS) especially, O2− and H2O2 in the stressed wheat plants (drought) in the two seasons compared to the control (Fig. 4). The levels of O2− and H2O2 was reduced meaningfully in the stressed wheat plants which inoculated with AMF (drought + AMF) comparing with the stressed untreated plants (drought) in both seasons. The best results of superoxide were recorded with the control and control + AMF treatments without any significant differences in both seasons. However, the best results of hydrogen peroxide were observed in the control + AMF treatment followed by the control treatment in both seasons.

Fig. 4.

Fig. 4

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Effect of drought and AMF on superoxide (A) and hydrogen peroxide (B) in wheat plants during 2022/2023 and 2023/2024 seasons. Bars followed by different letters are significantly different according to Student’s t-test

Effect of drought and AMF on total phenolic compounds and total soluble sugars in wheat plants

Total phenolic compounds and total soluble sugars are very important indicators under drought conditions. Our results presented in Fig. 5 showed that drought stress caused a significant increase in total phenolic compounds and total soluble sugars content in the stressed wheat plants (drought) compared with the control in the both seasons. However, a significant reduction in total phenolic compounds was recorded in the stressed plants which inoculated with AMF (drought + AMF). Furthermore, inoculation of wheat plants with AMF led to increase total soluble sugars content in the stressed plants (drought + AMF) compared with the stressed plants in the two seasons.

Fig. 5.

Fig. 5

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Effect of drought and AMF on total phenolic compounds (A) and total soluble sugars (B) in wheat plants during 2022/2023 and 2023/2024 seasons. Bars followed by different letters are significantly different according to Student’s t-test

Effect of drought and AMF on CAT, POD and SOD activity in wheat plants

Antioxidant enzymes is very important component in the defense system in plant, CAT, POD and SOD were augmented significantly in the stressed wheat (drought) in both seasons compared to control treatment. On the other hand, the application of AMF led to adjust the CAT, POD and SOD activities in the stressed treated wheat plants (drought + AMF) under drought conditions in the two seasons. Additionally, the inoculation of wheat grains with AMF led to a significant increase in POD and SOD activity in the control inoculated plants (control + AMF) when compared with control treatment in the two seasons (Fig. 6).

Fig. 6.

Fig. 6

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Effect of drought and AMF on CAT (A), POD (B) and SOD (C) activity in wheat plants during 2022/202S3 and 2023/2024 seasons. Bars followed by different letters are significantly different according to Student’s t-test

Effect of drought and AMF on yield characters of wheat plants

As an important indicator for the negative effects on plants, drought stress was adversely affected yield characters of wheat plants such as 1000 grain weight, grain yield and biological yield. The stressed wheat plants showed a significant decrease in 1000 grain weight, grain yield and biological yield compared with control plants in the two seasons (Fig. 7). In this experiment, the inoculation with AMF significantly increased the 1000 grain weight, grain yield and biological yield in the stressed inoculated wheat plants (drought + AMF) compared with the stressed uninoculated plants (drought) in the two seasons. Moreover, inoculation of wheat grains with AMF led to an increase in 1000 grain weight, grain yield and biological yield in the control inoculated plants (control + AMF) compared with the control treatment with any significant differences in both seasons (Fig. 7).

Fig. 7.

Fig. 7

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Effect of drought and AMF on 1000 grain weight (A), grain yield (B) and biological yield (C) activity in wheat plants during 2022/2023 and 2023/2024 seasons. Bars followed by different letters are significantly different according to Student’s t-test

Discussion

The adverse effects of drought stress on wheat plants led to numerous changes such as increase of EL% and MDA, reduction in chl a, b and RWC, increase the enzymes activity. In the current study, drought stress significantly reduced chl a, b content and maximum quantum efficiency in the stressed plants in the two seasons (Fig. 1). This effect may be due to the harmful impact on stomatal conductance, decreased photosynthetic rate and carboxylase activity and CO2 assimilation resulting in decrease Fv/Fm under drought [61, 62]. Application of AMF was very beneficial and led to a significant increase in chl a, b content and Fv/Fm under drought stress in the stressed plants (Fig. 1). This increase could be due to the positive role of AMF in increasing the nutrients uptake like phosphorus, potassium and magnesium which participate as central atom in chlorophyll resulting in the increase in chl a, b and maximum quantum efficiency. The useful effect of AMF was recorded in many plants [63, 64]. Our findings also showed that RWC% decreased significantly in the stressed wheat plants compared with the control (Fig. 2). The decrease in RWC% might be attributed to the harmful effect of drought on water uptake and mobility as well as the reduction in water availability under drought stress [61, 65]. Furthermore, inoculation of wheat grains with AMF improves RWC in the stressed wheat plants (drought + AMF) compared with the stressed untreated plants (drought). The improvement in RWC could be due to the role of AMF in increasing water absorption in the stressed wheat plants under drought conditions, this positive effect of AMF was studied in maize plants [66] and wheat plants [67]. Under drought stress, proline content was increased meaningfully in the stressed wheat plants compared with control because of proline is very important osmoprotectant which, accumulate under stress to protect the plant cells from oxidative damage. In addition, application of AMF led to increase proline content in the control plants which inoculated with AMF (control + AMF). The negative impact of drought stress on EL% and MDA was observed in the stressed wheat plants. EL% and MDA levels were augmented significantly in the stressed plants (Fig. 3). The significant increase in EL% and MDA is associated with the oxidative stress in plant organelles under stress conditions, the increase in EL% and MDA levels was recorded under several stresses [61, 68] in many plants. This increase may be due to the adverse effect on cell membrane and selectivity resulting in increased leakage of electrolytes in the stressed plants. In the current research, a significant increase in O2− and H2O2 under drought stress in wheat plants (drought) were recorded (Fig. 4). This increase could be attributed to the oxidative stress which occurred under drought resulting in the accumulation of O2− and H2O2. The over production of O2− and H2O2 is one of the most common signs under several stress factors [69, 70]. However, application of AMF led to decrease the levels of O2− and H2O2 in the stressed wheat plants comparing with the stressed untreated plants (drought). This reduction in the levels of O2− and H2O2 in the stressed wheat plants may be due to that, the inoculated plants with AMF display defense mechanisms to keep their organelles from oxidative damages with induced the antioxidant compounds. Application of arbuscular mycorrhizal fungus led to mitigate the harmful effects of water deficit stress on Dracocephalum moldavica [71].

Total phenolic compounds and total soluble sugars were increased significantly in the stressed wheat plants under drought conditions compared with the control plants (Fig. 5). The inoculation with AMF regulates the levels of total phenolic compounds and increase total soluble sugars in the stressed wheat plants. The useful role of AMF could be attributed to the role of AMF in producing glomalin-related soil protein, which acts as a promoter of water-stable aggregates, and improving the water status in plants as well as regulating the levels of total phenolic compounds and total soluble sugars [72]. One of the main components that is directly related to plant stress tolerance is antioxidant enzymes. We observed an increase in the antioxidant enzymes CAT, POD and SOD activities in the stressed wheat plants compared to control (Fig. 6). These increases may be due to the role of antioxidant enzymes in overcoming the adverse effects of several stresses on the stressed plants [73–75]. Our results established the effectiveness of AMF to protect the stressed wheat plants from the detrimental impact of drought, and indicated that it may play a significant role in regulating the production of antioxidant enzymes which have a protective action under stress conditions such as drought. Earlier studies also stated that AMF has an important effect in increasing CAT, SOD, and GR activity to improve the plant tolerance and increase biomass growth under drought conditions [76]. Additionally, the useful effect of AMF in enhancing drought tolerance was observed in many plants such as mize [77] by preventing malondialdehyde production and oxidative damage via improving the antioxidant enzymes activities.

In this study the adverse impact of drought on wheat yield was recorded, this effect could be due to its role in decreasing the water and elements uptake resulted in growth inhibition, decrease photosynthetic and assimilation, consequently decrease the yield characters of wheat such as 1000 grain weight, grain yield and biological yield (Fig. 7). However, the inoculated wheat plants with AMF showed a significant increase in yield characters under drought conditions. This increase may be attributed to the promoting role of AMF in improving the nutrients, water uptake and water use efficiency as well as some important phytohormones such as cytokines and gibberellic acids [78] which led to increase yield characters like grain yield and biological yield of the stressed wheat plants. Several studies have confirmed that, the inoculation with AMF led to increase growth rate and yield characters under stress by regulating hormonal balances, uptake essential nutrients, and creating growth regulators [79, 80].

Conclusions

Drought stress caused a significant decrease in the growth, physiological and biochemical as well as yield characteristics of the stressed wheat plants. Chlorophyll a, b concentration and Fv/Fm as well as relative water content significantly reduced in the stressed wheat plants compared to control. Moreover, 1000 grain weight (g), grain yield (t h− 1) and biological yield (t h− 1) were reduced significantly under drought conditions. Furthermore, superoxide, hydrogen peroxide, electrolyte leakage, lipid peroxidation and total phenolic compounds were increased significantly as indicators to oxidative stress in the stressed wheat plants under drought stress. On the other hand, inoculation with AMF has a positive effect on the most studied characters such as chlorophyll concentration and the maximum quantum efficiency of PSII as well as RWC% in the stressed wheat plants when compared with the stressed untreated plants. Also, AMF led to decrease the levels of hydrogen peroxide, superoxide, electrolyte leakage and lipid peroxidation however, the activity of antioxidant enzymes was upregulated and adjusted in the drought stressed wheat plants. Overall, inoculation with AMF can improve growth and grain yield characters of wheat plants by justifying the negative effects of drought stress. We recommend more future studies mainly physiological and molecular studies to evaluate and explain the effect of AMF on different wheat cultivars under stress conditions.

Acknowledgements

The authors would like to extend their appreciation to the Researchers Supporting Project Number (number RSP2024R505), King Saud University, Riyadh, Saudi Arabia.

Abbreviations

AMF

Arbuscular Mycorrhizal Fungi

Fv/Fm

The maximum quantum efficiency of PSII

RWC%

Relative Water Content

ROS

Reactive Oxygen Species

H2O2

Hydrogen peroxide

O2−

Superoxide

EL%

Electrolyte Leakage

MDA

Lipid Peroxidation

Chl

Chlorophyll

CMSI

Cell Membrane Stability Index

CAT

Catalase

POD

Peroxidase

SOD

Superoxide Dismutase

Author contributions

Conceptualization, Kh.A.; A.A. and Y.H.; methodology, Kh.A.; software, Kh.A.; A.A. and Y.H.; formal analysis, A.A. and Y.H.; resources, Kh.A.; A.A. and Y.H.; data curation, Kh.A.; A.A. and Y.H; writing—original draft preparation, Kh.A.; A.A. and Y.H.; writing—review and editing, A.A. and Y.H.; funding acquisition, Kh.A.; A.A. and Y.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Researchers Supporting Project (number RSP2024R505), King Saud University, Riyadh, Saudi Arabia.

Data availability

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

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s note

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

Contributor Information

Khaled Abdelaal, Email: khaled.elhaies@gmail.com.

Abdulaziz Alaskar, Email: aalaskara@ksu.edu.sa.

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Data Availability Statement

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

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