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Article

Effects of Arbuscular Mycorrhizal Fungi on the Physiological Responses and Root Organic Acid Secretion of Tomato (Solanum lycopersicum) Under Cadmium Stress

by
Dejian Zhang
1,2,
Xinyu Liu
1,2,
Yuyang Zhang
3,
Jie Ye
3 and
Qingping Yi
1,2,*
1
Hubei Key Laboratory of Spices & Horticultural Plant Germplasm Innovation & Utilization, College of Horticulture and Gardening, Yangtze University, Jingzhou 434020, China
2
Hubei Engineering Research Center for Specialty Flowers Biological Breeding, Jingchu University of Technology, Jingmen 448000, China
3
National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China
*
Author to whom correspondence should be addressed.
Horticulturae 2025, 11(10), 1204; https://doi.org/10.3390/horticulturae11101204
Submission received: 10 September 2025 / Revised: 30 September 2025 / Accepted: 3 October 2025 / Published: 6 October 2025
(This article belongs to the Special Issue Horticultural Crops against Abiotic Stresses: Adaptation Skills and Agronomic Strategies)
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Abstract

Arbuscular Mycorrhizal Fungi (AMF) can form symbiotic relationships with most plants. They can alleviate the toxic effects of heavy metals on plants. This study analyzed the effects of AMF (Diversispora versiformis, D.v.) on the physiological responses and root organic acid secretion of tomato (Solanum lycopersicum L.) under cadmium (Cd) stress, in order to elucidate how AMF enhance Cd tolerance. The results indicated that when the AMF inoculation rate of tomato seedlings ranged from 26.75% to 38.23%, the AMF treatment significantly promoted tomato growth. Cd significantly reduced the agronomic traits of tomato. However, AMF inoculation dramatically lowered the Cd level from 19.32 mg/kg to 11.54 mg/kg in tomato roots, and effectively reduced the negative effect of Cd toxicity on seedling growth. Cd stress also significantly reduced the chlorophyll fluorescence parameters, chlorophyll contents, and photosynthetic intensity parameters in seedling leaves, while the AMF treatment significantly increased these indicators. Under Cd stress, the AMF treatment significantly increased the activities of SOD, POD, and CAT, and reduced the levels of reactive oxygen species and the contents of osmotic regulatory substances in roots. Under Cd stress conditions, the AMF treatment also significantly increased the auxin level (57.24%) and reduced the abscisic acid level (18.19%), but had no significant effect on trans-zeatin riboside and gibberellin contents in roots. Cd stress markedly reduced the content of malic acid and succinic acid by 17.28% and 25.44%, respectively; however, after the AMF inoculation, these indicators only decreased by 2.47% and 2.63%, respectively. Under Cd stress, AMF could increase tomato roots’ antioxidant capacity to reduce ROS level, thereby alleviating the toxicity induced by ROS and maintaining reactive oxygen metabolism, enhancing the plant’s stress resistance. In summary, the AMF treatment enhances the osmotic regulation capacity and maintains the stability of cell membranes by reducing the levels of osmotic regulatory substances in roots. It also enhances the Cd tolerance of tomato plants by regulating the contents of root hormones and aerobic respiration metabolites, among other pathways. Therefore, inoculating plants with AMF is a prospective strategy for enhancing their adaptive capacity to Cd-polluted soils.

1. Introduction

In recent years, heavy metal elements have accumulated in soil, water, and the atmosphere, seriously affecting the cultivation and safe production of crops. Cadmium (Cd), as one of the main heavy metal elements contributing to soil pollution, has the characteristics of wide range, wide distribution, non-degradability, strong toxicity, extremely strong mobility, and easy absorption and accumulation by plants, and it can also disrupt plant metabolism and damage plant growth [1]. When Cd absorbed by plants has accumulated beyond the safety threshold of the plants themselves, it will cause varying degrees of toxic effects to plants at the morphological, physiological, and molecular levels [2]. The Cd toxicity response in plants is mainly manifested as inhibited growth, damaged root systems, curled and yellowed leaves, and even leaf drop [2]. Excessive accumulation of Cd in plants induces the production of a large number of reactive oxygen species, causing lipid peroxidation of cell membranes, degradation of chloroplasts, and severe damage to the photosynthetic reaction center of plants, and seriously inhibits the growth and development of plants [3]. Therefore, plants must quickly take a series of protective measures—mainly by enhancing the activity of the antioxidant enzyme system and promoting the production of osmotic adjustment substances—to ensure the rapid removal of accumulated reactive oxygen species in cells. Studies have shown that Cd markedly increases ROS levels in tomato. In response, tomato plants present enhance antioxidant enzyme activities to alleviate Cd phytotoxicity [4].
Plant hormones (such as auxin, gibberellin, cytokinin, abscisic acid, and ethylene) are trace organic substances synthesized within plants, which regulate growth and development as well as adaption to environmental changes. They can influence plant life activities through either synergistic or antagonistic effects [5,6,7,8,9]. Studies have shown that plant hormones assist in integrating endogenous and exogenous signals, helping plants cope with abiotic stresses, such as Cd stress [10,11,12]. Gibberellins, abscisic acid, auxin, jasmonic acid, cytokinins, ethylene, salicylic acid, brassinosteroids, and polyamines have garnered attention from botanical researchers as sustainable phytohormones that can induce tolerance in Cd-stressed plants [13]. 4-Benzoylphenylboronic acid (PPBa) is a specific and effective inhibitor of flavin monooxygenase (YUCCA) enzymes, which inhibit the synthesis of IAA [14]. The YUCCA family plays a vital role in the synthesis pathway of IPA. If the activity of these enzymes is inhibited, it will affect the secretion of IAA, thereby regulating the accumulation of Cd [15]. Cd affects the normal growth of plants by inhibiting photosynthesis, influencing antioxidant enzyme activities, and regulating the synthesis and transportation of phytohormone [13]. At the molecular level, Cd stress also induces the expression of a series of genes, such as genes encoding for plant chelators, heavy metal ATPases, YSL transport proteins, ABC transport proteins, antioxidant system activity and oxidative stress response, and chlorophyll synthesis or degradation [13].
As symbiotic fungi, arbuscular mycorrhizal fungi (AMF) are widely present in soils and can form symbiotic relationships with most terrestrial plants [16]. Under heavy metal stress, AMF infect plant roots to form mycorrhizal symbioses. In particular, the AMF exogenous hyphal network enhances the plant’s absorption of mineral nutrients and alleviates the negative effects of heavy metals on plant growth [17,18]. Shaher et al. [19] demonstrated that AMF alleviated the toxic effects of heavy metals (Cd and Pb) by promoting nutrient absorption and secondary metabolite accumulation in Calendula officinalis. AMF (Rhizophagus irregularis) inoculation lowered Cd influx in Perennial Ryegrass (Lolium perenne L.), enhanced the availability of nutrients in the rhizosphere, and mitigated Cd phytotoxicity [20]. AMF also cause changes in the root exudates of plants. For instance, low-molecular-weight organic acids can form “heavy metal–low-molecular-weight organic acid” complexes with soil heavy metals, which reduces the mobility and bioavailability of heavy metals and alleviates heavy metals’ phytotoxicity [21]. The influence process of low-molecular-weight organic acids on the availability of heavy metals is relatively complex. It is not only related to the types and properties of organic acids themselves, but also to factors such as soil conditions and planting patterns [22]. Under Cd stress, AMF affect the secretion amounts of different types of low-molecular-weight organic acids, causing changes to the forms of heavy metals [23]. The root systems of plants can alter the soil redox potential and pH by secreting low-molecular-weight organic acids (such as malic acid and citric acid) to reduce the solubility and mobility of heavy metal elements, thereby alleviating the growth conditions of plants under heavy metal stress [23]. Therefore, after AMF have established a symbiotic relationship with plants, they can improve the morphology of the roots. At the same time, they affect the roots’ secretion of low-molecular-weight organic acids, thereby facilitating the host plants’ absorption of nutrient elements, inhibiting heavy metals’ mobility, and regulating the transport process of heavy metals in the host plants through the mycorrhizal structure and the complex mycelial network. As a result, heavy metals’ phytotoxicity on the host plants is reduced and the growth of the host plants is promoted, as AFM help the plants resist non-biological adverse conditions such as heavy metal stress [17,18,24].
As an annual or perennial herbaceous plant of the Solanaceae family, tomato (Solanum lycopersicum) is rich in lycopene, vitamins, and polyphenolic compounds, and is one of the most widely cultivated fruits and vegetables worldwide. Non-biological stress mainly refers to adverse conditions caused by environmental factors, including not only temperature stress, light stress, drought stress, and salt stress, but also various heavy metal stresses, such as Pb and Cd stress [25,26,27,28]. To date, most studies on non-biological stress in tomatoes have focused on the effects of salt stress, drought stress, and high-temperature stress. However, some existing studies have shown that tomatoes are sensitive to Cd. Moreover, Cd pollution is becoming increasingly severe, which not only reduces the yield and quality of vegetables such as tomatoes, but also poses a threat to human health [4]. A significant body of research has focused on the response mechanisms of vegetables such as cucumber, lettuce, and pepper under Cd stress. However, few studies have focused on the mechanism of tomato’s tolerance to Cd stress in relation to microorganisms such as AMF. Therefore, it is of significance to study the growth and physiological and biochemical changes in tomato under Cd stress conditions in relation to AMF. This study used tomato (Ailsa Craig) as the study material and applied AMF (Diversispora versiformis) and CdSO4 to interactively treat tomato seedlings. The study explored the growth and physiological–biochemical responses of tomato plants to AMF and CdSO4, and further analyzed the mechanism by which AMF enhances tomato’s tolerance to Cd stress. This study provides a theoretical basis for using microorganisms to remediate heavy metal-contaminated soil and improve plant stress resistance.

2. Materials and Methods

2.1. Plants, Growth Conditions, and Experimental Design

Diversispora versiformis (D. versiformis) was donated by the Bank of Glomeromycota in China (BGC), stored at 4 °C, and was then used in this study as an AMF (mycorrhizal fungal inoculum containing approximately 28 spores/g). Tomato seeds (Ailsa Craig) were provided by Huazhong Agricultural University. On 26 February 2024, after being sterilized with 75% alcohol (10 min), the tomato seeds were germinated in autoclaved sand (0.11 MPa, 121 °C, 1.5 h) at 26 °C/18 °C (14 h/10 h, day and night) and 78–86% relative humidity. Three-leaf tomato seedlings were then transplanted into plastic pots (14.6 × 8.2 × 12.2 cm) on 2 April 2024. The pots were pre-filled with autoclaved soil–sand mixture (2:1, v/v), and their compositions were 18.88 mg/g soil organic matter, 28.26 mg/kg NH4+-N, 24.38 mg/kg NO3−-N, 46.62 mg/kg Olsen-P, and 56.48 mg/kg available K. Each pot contained three tomato seedlings.
The tomato seedlings were inoculated with D. versiformis at the time of transplanting, at about 180 g/pot (2 April 2024). The non-inoculated pots likewise received equal amounts of autoclaved D. versiformis. The tomato seedlings were placed in a plant light incubator (day/night temperature and time set as 26 °C/18 °C and 14 h/10 h, respectively, the photon flux density set as 644–886 μmol/m2/s, and the air relative humidity set as 78–86%). Two months following inoculation with D. versiformis, a Cd stress (CdSO4, Sigma-Aldrich Merck KGaA, Darmstadt, Germany) treatment was initiated (2 June 2024) and maintained for 30 days (3 times, 100 mL/time); afterwards, the seedlings were harvested (2 July 2024).
This experiment included 4 treatments: inoculation without D. versiformis at 0 μmol/L Cd, inoculation with D. versiformis at 0 μmol/L Cd, inoculation without D. versiformis at 50 μmol/L Cd, and inoculation with D. versiformis at 50 μmol/L Cd. Each treatment was replicated 5 times (each time included 1 pot), with a total of 60 seedlings planted in 20 pots.

2.2. Methods of Determination

The harvesting time of the tomato seedlings was 2 July 2024. The whole roots of the tomato seedlings were scanned using an Epson Scanner machine (Perfection V700, J221A, Bengaluru, India) and analyzed with WinRHIZO for root system architecture (Regent Instruments Inc., Quebec, QC, Canada).
Chlorophyll a, chlorophyll b, and total chlorophyll contents were measured according to the protocol developed by Zhang et al. [28]. The chlorophyll fluorescence parameters were examined using an M-series modulated chlorophyll fluorescence meter (IMAGING-PAM, Heinz Walz GmbH, Nuremberg, Germany). Unfolded leaves were chosen for detection of the maximum photochemical efficiency (Fv′/Fm′), actual photochemical efficiency (φPSII), photochemical quenching coefficient (qP), and non-photochemical quenching coefficient (NPQ) using a Handy PEA continuous excitation fluorometer (Hansha Scientific Instruments Co., Ltd., Taian, China) from 09:00 to 11:00. Additionally, the photosynthetic parameters (intercellular CO2 concentration, net photosynthetic rate, transpiration rate, and stomatal conductance) were measured using a Li-6400 portable photosynthetic system analyzer (Li-COR Inc., Lincoln, NE, USA) from 09:00 to 11:00.
Tomato seedling roots (1–2 cm) were stained with 0.05% trypan blue and then used for the detection of mycorrhizal colonization according to the protocol developed by Lu et al. [27]. The tomato seedling roots were promptly treated with liquid nitrogen after harvesting and then stored at −80 °C for physiological and biochemical indicator analysis. The root Cd concentrations were assayed based on the protocol developed by Zhuang et al. [12]. The malondialdehyde (MDA) concentration was measured using the thiobarbituric acid method, the proline (Pro) level was measured using the ninhydrin colorimetry method, and the soluble sugar and soluble protein contents was detected in accordance with Li et al. [29]. The hydrogen peroxide (H2O2) and superoxide anion (O2.−) contents were detected using a H2O2 assay kit and an O2.− assay kit (ml154234, ml456781, Beijing Boxingong Technology Co., Ltd., Shanghai, China). The content of superoxide anion was calculated by using the hydroxylamine oxidation method, employing hydroxylamine (NH2OH) and O2-specific reoxidation reaction, determining the absorbance at a 540 nm wavelength, and calculating the concentration of NO2− using the standard curve. CAT, SOD, and POD activities were detected using appropriate assay kits (ml201168, ml902210, mll614100) (Shanghai Enzyme-link Biotechnology Co., Ltd., Shanghai, China) in accordance with Li et al. [29]. The abscisic acid (ABA) ELISA kit, trans-zeaxin nucleoside (tZR) ELISA kit, IAA ELISA kit, and gibberellin (GA3) ELISA kit (ml245168, ml202879, ml2014145, ml2029142, Nanjing Jiancheng Bioengineering Research Institute Co., Ltd., Nanjing, China) were used to determine the contents of endogenous hormones in tomato seedling roots. The concentrations of succinic acid and malic acid were measured via high-performance liquid chromatography (HPLC) in accordance with Chen et al. [23]: first, 1.00 g of tomato root was accurately weighed and mixed in a blender, ground with 4 mL of extraction solution, and centrifuged for 10 min at 10,000 r/min; the residue was added to 2 mL of extraction solution and then extracted and combined with the supernatant; the mixture was dried in a water bath at 90 °C at a fixed volume of 10 mL, and then extracted with a disposable syringe after whirlpool mixing; it was then filtered using a 0.45 μm filter membrane and analyzed using a machine.

2.3. Statistical Analysis

Analysis of variance (ANOVA) and the Trouvelot method were employed to analyze the data in SAS (8.1v). Photoshop 7.2.4 and Microsoft Excel 2013 were used for drawing figures and data processing. Furthermore, significant differences between treatments were analyzed using Duncan’s multiple range test (p < 0.05).

3. Results

3.1. Effects of AMF on the Agronomic Traits of Tomato Under Cd Stress Conditions

AMF significantly promoted tomato seedling growth (Figure 1). Under non-Cd condition, the AMF treatment increased the plant height, leaf number, total plant weight, root fresh weight, and aboveground fresh weight by 47.45%, 46.54%, 38.15%, 42.62%, and 39.35%, respectively (Table 1). Under Cd stress conditions (50 μmol/L), the AMF treatment also significantly increased the growth vigor of tomato seedlings, with increases in the leaf number, plant height, total plant weight, root fresh weight, and aboveground fresh weight by 9.39%, 27.24%, 46.02%, 20.83%, and 49.49%, respectively (Table 1). Table 1 also indicates that Cd markedly inhibited seedling growth: under the condition of no AMF inoculation, Cd stress significantly reduced the plant height, leaf number, total plant weight, root fresh weight, and aboveground fresh weight by 28.94%, 9.62%, 34.17%, 21.31%, and 34.09%, respectively. However, after inoculation with AMF, these indicators were only reduced by 9.59%, 1.13%, 3.87%, 4.92%, and 1.48%, respectively (Table 1). Thus, it can be concluded that the AMF inoculation has a promoting effect on the growth of tomato seedlings, while Cd significantly inhibits the seedling growth. However, AMF can alleviate the Cd phytotoxicity on the growth of tomato seedlings to a certain extent.

3.2. Development of AMF in Tomato Root Systems and Changes in Cd Content

From Figure 2, it can be observed that the root systems of the tomato seedlings subjected to the AFM inoculation treatment had structures such as mycorrhizal fungal hyphae and vesicles, indicating that the root systems of these tomato plants were all infected by Diversispora versiformis to varying degrees. An analysis of the data on mycorrhizal infection rates showed that the infection rates in the root systems of the tomato seedlings not subjected to the inoculation treatment were all 0.00 (Table 2). As shown in Table 2, in the absence of Cd stress, the infection rate of this mycorrhizal fungus in the root systems of the tomato seedlings subjected to the inoculation treatment was 0.38, which was significantly higher than the infection rate of 0.27 under Cd stress conditions. By detecting the Cd content in the root systems of the tomato seedlings, it was found that no Cd was detected in the root systems of the tomato seedlings not subjected to Cd stress. Under the 50 μmol/L Cd stress conditions, the AMF treatment markedly lowered the Cd level in the root systems from 19.32 mg/kg to 11.54 mg/kg. This indicates that Cd stress inhibits the infection of AMF in the root systems of tomato seedlings to some extent, while AMF can effectively weaken the absorption effect of Cd by the root systems.

3.3. Effects of AMF on the Root Architecture of Tomato Under Cd Stress Conditions

The effects of AMF on the structural indicators of tomato seedling roots under Cd stress are shown in Figure 3. Under non-Cd stress conditions, the AMF treatment significantly increased the total root length and total root surface area by 41.06% and 45.30%, respectively, but had no significant effect on root volume (Table 3). Under Cd stress conditions (50 μmol/L), the AMF treatment also significantly increased the total root length of the seedlings by 24.98%, but it had no significant effect on the total root surface area and root volume (Table 3). Table 3 also indicates the effects of Cd stress on the root growth of the seedlings. Without AMF inoculation, Cd stress significantly reduced the total root length by 28.17%, but there was no conspicuous difference in the total root surface area and root volume. However, after inoculation with AMF, the total root length decreased by only 10.23%, and the total root surface area and root volume remained the same without significant changes (Table 3). Thus, the AMF inoculation has a certain promoting effect on the root growth of tomato seedlings. Cd significantly inhibits the total length of the root system of tomato seedlings, and inoculation with AMF can, to some extent, alleviate the Cd phytotoxicity on the root growth.

3.4. Effects of AMF on Chlorophyll Contents and Chlorophyll Fluorescence Parameters of Tomato Leaves Under Cd Stress Conditions

The AMF treatment increased the chlorophyll contents in tomato leaves to a certain extent. Under non-Cd stress conditions, although chlorophyll a, chlorophyll b, and total chlorophyll increased in tomato leaves after the AMF treatment, the increases did not reach a significant level. However, under Cd stress conditions (50 μmol/L), the AMF treatment significantly increased these indicators by 57.38%, 72.73%, and 64.33%, respectively (Table 4). Table 4 also indicates that Cd significantly reduced the chlorophyll contents in tomato leaves. Without AMF inoculation, Cd stress significantly reduced chlorophyll a, chlorophyll b, and total chlorophyll by 43.26%, 49.54%, and 46.73%, respectively. However, after the AMF inoculation, these indicators decreased by only 10.69%, 12.84%, and 12.46%, respectively (Table 4). Thus, AMF increased the chlorophyll contents in tomato leaves to a certain extent, while Cd stress significantly inhibited the synthesis of chlorophyll. However, AMF could effectively alleviate the effects of Cd phytotoxicity on the synthesis of chlorophyll in tomato seedlings.
The effects of AMF on chlorophyll fluorescence parameters in tomato seedling leaves under Cd stress condition are also shown in Table 4. The AMF inoculation increased φPSII, Fv′/Fm′, qP, and NPQ in tomato leaves to a certain extent. Under non-Cd stress conditions, although φPSII, Fv′/Fm′, and qP increased in tomato leaves after the AMF treatment, the increases did not reach a significant level. However, under Cd stress conditions (50 μmol/L), the AMF treatment significantly increased these parameters by 41.86%, 85.71%, and 150.00%, respectively (Table 4). Table 4 also indicates that Cd stress significantly reduced the chlorophyll fluorescence parameters. Without AMF inoculation, Cd stress significantly reduced φPSII, Fv′/Fm′, and qP by 34.85%, 50.59%, and 63.64%, respectively. However, after the AMF inoculation, these parameters decreased by only 7.58%, 8.75%, and 9.09%, respectively (Table 4). Thus, the AMF treatment increased the chlorophyll fluorescence parameters in tomato leaves to a certain extent, while Cd stress significantly reduced these parameters and thereby reduced the efficiency of light energy utilization. However, AMF could effectively alleviate the reduction in chlorophyll fluorescence parameters induced by Cd stress, thereby improving the efficiency of light energy utilization.

3.5. Effects of AMF on Photosynthesis in Tomato Leaves Under Cd Stress Conditions

The AMF treatment increased the photosynthetic parameters (Pn, Gs, Ci, and Tr) of tomato leaves to a certain extent. Under non-Cd stress conditions, although Pn, Gs, and Tr increased in tomato leaves after AMF treatment, the increases did not reach a significant level. However, under Cd stress conditions (50 μmol/L), the AMF treatment markedly improved Pn, Gs, Ci, and Tr by 34.01%, 30.73%, 26.84%, and 18.82%, respectively (Table 5). Table 5 also indicates that Cd stress significantly reduced the photosynthetic parameters of tomato leaves. Without AMF inoculation, Cd markedly lowered Pn, Gs, Ci, and Tr by 33.52%, 33.33%, 35.38%, and 28.97%, respectively. However, after the AMF inoculation, these indicators decreased by only 10.91%, 12.85%, 18.03%, and 15.59%, respectively (Table 5). Thus, the AMF treatment increased the photosynthetic intensity of tomato leaves to a certain extent, while Cd stress inhibited the photosynthetic intensity and efficiency of tomato seedlings. However, inoculation with AMF could effectively alleviate the Cd phytotoxicity on the photosynthetic intensity and efficiency of tomato seedlings, thereby increasing the photosynthetic products.

3.6. Effects of AMF on the ROS Level in Tomato Roots Under Cd Stress Conditions

The effects of the AMF treatment on the internal ROS (H2O2 and O2.−) content in the root systems of tomato seedlings under Cd stress are shown in Table 6. Under non-Cd stress conditions, the content of H2O2 and O2.− in the tomato root systems did not show significant changes after the AMF treatment. However, under Cd stress conditions (50 μmol/L), the AMF treatment significantly reduced the content of H2O2 and O2.− by 33.33% and 32.77%, respectively (Table 6). Table 6 also indicates that Cd stress significantly increased the ROS concentration in the tomato root systems. Without AMF inoculation, Cd stress caused the content of H2O2 and O2.− to increase by 1.22 times and 1.63 times, respectively. However, after the AMF inoculation, these indicators only increased by 48.09% and 77.07%, respectively (Table 6). Thus, the AMF treatment has no significant effect on the internal ROS content of tomato seedling root systems, while Cd stress causes tomato seedling root systems to accumulate higher concentrations of ROS. However, inoculation with AMF can effectively regulate the metabolism of ROS in tomato root systems, thereby reducing the accumulation of ROS and protecting the structure and function of the cell membrane.

3.7. Effects of AMF on Antioxidant Enzyme Activities in Tomato Roots Under Cd Stress Conditions

The changes in the activities of antioxidant enzymes in the root systems of tomato seedlings are shown in Table 7. Under non-Cd stress conditions, the SOD, POD, and CAT activities in the tomato root systems did not show significant changes after the AMF treatment. However, under Cd stress conditions (50 μmol/L), the AMF treatment significantly increased these activities by 14.51%, 12.16%, and 30.04%, respectively (Table 7). Table 7 also indicates that Cd stress significantly increased the antioxidant enzyme activities in the tomato root systems. Without AMF inoculation, Cd stress caused SOD, POD, and CAT activities to increase markedly by 1.49 times, 0.89 times, and 0.79 times, respectively. However, after inoculation with the AMF, these indicators increased by 1.85 times, 1.13 times, and 1.32 times, respectively (Table 7). Thus, the AMF inoculation makes no significant difference to the activities of antioxidant enzymes in the root systems of tomato seedlings, while Cd stress significantly enhances antioxidant enzyme activities. However, under Cd stress conditions, inoculation with AMF can further increase the antioxidant enzyme activities, thereby improving the plant’s ability to remove reactive oxygen species and free radicals, maintaining the redox balance within plant cells, protecting the structure and function of cells, and effectively enhancing the plant’s antioxidant defense capacity.

3.8. Effects of AMF on the Content of Osmotic Regulatory Substances in Tomato Roots Under Cd Stress Conditions

Under non-Cd stress conditions, the concentrations of osmotic regulatory substances in tomato roots showed no significant changes after the AFM treatment. However, under Cd stress conditions (50 μmol/L), the AMF treatment significantly reduced the concentrations of Pro, MDA, soluble protein, and soluble sugar by 38.92%, 31.19%, 27.62%, and 49.27%, respectively (Table 8). Table 8 also indicates that Cd stress significantly increased the content of osmotic regulatory substances in tomato roots. Without AMF inoculation, Cd stress caused the concentrations of Pro, MDA, soluble protein, and soluble sugar to increase by 2.79 times, 1.05 times, 0.92 times, and 3.15 times, respectively. However, after the AMF inoculation, these indicators only increased by 1.32 times, 0.41 times, 0.39 times, and 1.11 times, respectively (Table 8). Thus, the AMF treatment has no significant effect on the content of osmotic regulatory substances in the roots of tomato seedlings, while Cd stress causes tomato seedling roots to accumulate higher concentrations of osmotic regulatory substances. However, inoculation with AMF can effectively alleviate the abnormal accumulation of osmotic regulatory substances induced by Cd stress, thereby regulating the water metabolism inside and outside the cells.

3.9. Effects of AMF on the Content of Endogenous Hormones in Tomato Roots Under Cd Stress Conditions

The effects of the AMF treatment on the concentrations of endogenous hormones in tomato roots under Cd stress conditions are shown in Table 9. Under non-Cd stress conditions, the IAA content significantly increased in tomato roots by 26.85% after the AMF treatment, while the ABA content significantly decreased by 12.74%. The levels of GA3 and tZR showed no significant changes (Table 9). Under Cd stress conditions (50 μmol/L), the AMF treatment significantly increased the IAA content by 57.24% and decreased the ABA content by 18.19%, while the contents of tZR and GA3 remained unchanged (Table 9). Without AMF inoculation, Cd stress significantly reduced the IAA and tZR contents by 38.92% and 20.77%, respectively, while increasing the ABA content by 22.43%, but the GA3 content remained unchanged (Table 9). However, after the AMF inoculation, the IAA and tZR contents decreased by only 3.96% and 14.26%, respectively, while the ABA and GA3 contents showed no significant changes (Table 9). Thus, AMF can positively regulate endogenous auxin synthesis in tomato and negatively regulate the biosynthesis of abscisic acid to promote plant growth, while Cd stress negatively regulates endogenous auxin and cytokinin in tomato and positively regulates the biosynthesis of abscisic acid to inhibit plant growth. It is noteworthy that AMF can effectively alleviate the Cd phytotoxicity on the synthesis of endogenous auxin and cytokinin in tomato and weaken the promoting effect on the synthesis of abscisic acid.

3.10. Effects of AMF on the Content of Succinic Acid and Malic Acid in Tomato Roots Under Cd Stress Conditions

The effects of the AMF treatment on the concentrations of succinic acid and malic acid in tomato roots under Cd stress conditions are displayed in Table 10. Under non-Cd stress conditions, the AMF treatment significantly increased the succinic acid and malic acid levels in tomato roots by 21.93% and 22.22%, respectively. Under Cd stress conditions (50 μmol/L), the AMF treatment also increased their concentrations by 17.91% and 30.59%, respectively (Table 10). Table 10 also indicates that Cd stress significantly reduced the succinic acid and malic acid levels in tomato roots. Without AMF inoculation, Cd stress significantly decreased the content of malic acid and succinic acid by 17.28% and 25.44%, respectively. However, after the AMF inoculation, these indicators decreased by only 2.47% and 2.63%, respectively (Table 10). Therefore, it can be concluded that AMF can positively regulate the biosynthesis of malic acid and succinic acid in tomato roots, while Cd stress shows a negative regulatory effect. It is noteworthy that inoculation with AMF can significantly alleviate the negative regulatory effect of Cd phytotoxicity on the biosynthesis of malic acid and succinic acid in tomato roots, thereby affecting the metabolism of endogenous acids; establishing a dynamic balance between energy supply, respiratory metabolism, redox homeostasis, and osmotic protection; and thus mitigating the Cd phytotoxicity on tomato growth.

4. Discussion

The phytotoxicity of Cd refers to the damaging effects it has on photosynthesis, growth, secondary metabolism, oxidative stress responses, and other plant processes [18]. The morphological indicators of plants include total plant weight, leaf number, plant height, fresh weight of root system, fresh weight of aboveground part, total root length, and total root surface area, which can be used to reflect the response of plants to Cd toxicity [30,31,32,33]. Yang et al. [20] used Lolium perenne L. as the material to study the impact of 100 mg/kg Cd stress on its growth and found that Ca significantly inhibited various growth indicators such as leaf fresh weight and root fresh weight. In another study, 400 mg·kg−1 Cd severely reduced the growth indicators of Rosa rugosa and also caused chlorosis and leaf desiccation [34]. In this study, the growth of the aboveground parts and roots of tomato plants treated with 50 μmol/L Cd was significantly inhibited. At the same time, phenomena such as leaf wilting, edge curling, darkening of color, chlorosis, slow addition of new leaves, and shedding of old leaves occurred. These findings suggest that Cd competes with mineral nutrients for the same transport pathways, thereby altering the absorption and distribution of mineral nutrients in plants, resulting in nutrient deficiency in the plants and inhibition of plant growth [35].
AMF are important functional microorganisms widely present in soils. After AMF infect plants and form a mycorrhizal symbiotic structure, they can improve the host plants’ nutrient and water absorption, thereby promoting the growth of the host plants and enhancing their stress resistance [26,36]. In this study, the AMF treatment significantly enhanced tomato growth. Especially under Cd stress conditions, the AMF treatment had a better recovery effect on the growth potential of tomato seedlings. This is similar to what was reported by Yang et al. [20] in their study on the effects of AMF on Perennial Ryegrass (Lolium perenne L.) under Cd stress, wherein inoculation with AMF reduced Cd influx in plants, enhanced nutrient availability, and thus mitigated Cd phytotoxicity. The findings of this study are also consistent with the research results reported by Zhuang et al. [12], who found that inoculation with AMF (Rhizophagus intraradices) can effectively alleviate the negative effects of Cd stress (300 μM) on the growth characteristics and nutrient element content of Malus hupehensis Rehd. Furthermore, the results of this study also indicated that after the AMF inoculation, the Cd content in the root systems of tomato seedlings under Cd stress conditions decreased significantly from 19.32 mg/kg to 11.54 mg/kg. This is consistent with the results of previous studies. For example, AMF dramatically reduced the Cd level in the roots and shoots of maize (Zea mays L.), which weakened the phytotoxicity of excessive Cd [37]. In another study, AMF significantly increased maize height and biomass and decreased the available Cd content in both the soil and maize [38]. Mycorrhization (Rhizophagus intraradices) could prevent Cd-induced growth inhibition and reduce Cd accumulation in the roots of Glycine max (L.) Merr [39]. AMF (D. eburnea) markedly altered soil Cd speciation by increasing the proportion of exchangeable Cd and decreasing residual Cd, resulting in changes to the Cd content in the roots of L. perenne and A. fruticosa [40]. In addition, AMF inoculation reduced the Cd level in P. yunnanensis [41].
The toxic effects of heavy metals also manifest in the destruction of the chloroplast structure in plant leaves. Chloroplasts are crucial sites for photosynthesis in plants, and chlorophyll, as an important photosynthetic pigment, plays a decisive role in the accumulation of plant biomass [42,43,44,45]. Li et al. [17] subjected Medicago truncatula to Cd stress (20 mg/g) and found that the chlorophyll content in the leaves significantly decreased. The chlorophyll a, chlorophyll b, and total chlorophyll levels in ‘Baizizhi’ and ‘Zizhi’ decreased with increasing Cd contents [34]. The chlorophyll pigments were significantly reduced in 100 mg/kg Cd-contaminated Brassica chinensis L. seedlings when compared to seedlings not subjected to Cd treatment [42]. The damage caused by Cd to chloroplasts and thylakoid membranes occurs concurrently with the activities of enzymes involved in chlorophyll synthesis, which activates enzymes related to chlorophyll degradation and ROS production, leading to a decrease in chlorophyll synthesis and content [46]. In this study, Cd dramatically lowered the chlorophyll b, chlorophyll a, and total chlorophyll concentrations in tomato seedling leaves, indicating that Cd stress could inhibit the synthesis of chlorophyll in tomato seedlings. It is notable that the AMF treatment significantly increased the chlorophyll a, chlorophyll b, and total chlorophyll levels in tomato seedlings, especially under Cd stress conditions where the AMF treatment had a better recovery effect. These results are similar to the results reported by Wang et al. [47], who found that after AMF inoculation, the agronomic traits of tomato significantly improved in moderately Cd-contaminated soil, specifically manifested as increased plant height, stem diameter, and chlorophyll content. Therefore, Cd stress significantly inhibited the synthesis of chlorophyll in tomato, but AMF could effectively alleviate this Cd phytotoxic effect.
When plants are subjected to heavy metal stress during their growth process, the inner membrane of the chloroplasts will be damaged, which affects photosynthesis and the production of assimilates in the plants [12,48]. In PSII, when plants are subjected to abiotic stress, the Fv′/Fm′ ratio decreases, indicating that the photosystem II has been damaged [49]. Under Cd stress (20 mg/Kg), the chlorophyll fluorescence parameters (φPSII and qP) of Medicago truncatula Gaertn decreased significantly, indicating that the Cd2+ stress damaged the photosynthetic organ [17]. Shaari et al. [42] found that Brassica chinensis L. seedlings subjected to 100 mg/kg Cd presented the lowest Fv′/Fm′ ratio (0.73), indicating that these seedlings were stressed as compared to the control. This study found that Cd stress significantly reduced φPSII, Fv′/Fm′, and qP in the leaves of tomato seedlings. However, after inoculation with the AMF, these indicators returned to normal levels. This finding is consistent with the results of other studies. In response to Cd stress (300 μM), Fv′/Fm′ was significantly increased in mycorrhizal (R. intraradices) compared to non-mycorrhizal M. hupehensis Rehd seedlings [12]. Under Cd stress conditions (20 mg/kg), after inoculation with arbuscular mycorrhizal fungi, the chlorophyll fluorescence parameters (φPSII and NPQ) of alfalfa (Medicago truncatula) were significantly improved, effectively alleviating the damage to the PSII reaction center caused by Cd stress [17]. This indicates that AMF can alleviate and even restore the damage to PSII caused by Cd stress. Under Cd stress conditions, AMF (Funneliformis mosseae) significantly increased the Fv′/Fm′, φPSII, and qP in Oryza sativa L. [48]. The above results indicate that Cd stress weakens the efficiency of light energy utilization by reducing chlorophyll fluorescence parameters. However, inoculation with AMF can effectively alleviate the reduction effect of Cd stress on these parameters, thereby mitigating the adverse effects of Cd on the PSII reaction center and enhancing the light energy utilization efficiency.
Photosynthesis is the process by which plants synthesize compounds rich in energy. It is the ultimate carbon synthesis pathway in various biochemical and physiological processes of plants, and it forms the basis of plant life activities [50]. Photosynthesis is highly sensitive to many adverse environmental conditions, including water stress, high temperature, salt damage, and heavy metal stress [18,51]. All these stresses reduce the photosynthetic efficiency of plants and thereby affect plant growth and development. Photosynthetic intensity parameters can precisely reflect the photosynthetic intensity in plants. As the degree of Cd stress increases, the Pn, Tr, and Gs of Rosa rugosa leaves showed gradually decreasing trends [34]. This is in agreement with this study, where Cd acts as an effective inhibitor of photosynthesis, suppressing plant photosynthesis through stomatal closure, and leading to damage to the photosynthetic apparatus and the destruction of the light-harvesting complexes and photosystems I and II [52]. There have been some reports on the effects of AMF inoculation in alleviating the negative impact of Cd stress on plant photosynthesis. AMF could mitigate Cd-induced photosynthesis and growth phytotoxicity and nutrient ion disorders in Malus hupehensis Rehd [12]. AMF mitigated the Cd phytotoxicity on photosynthesis efficiency in Cicer arietinum [53]. These results are consistent with those of this study, which found that under the condition of no AMF inoculation, Cd dramatically lowered the values of Pn, Gs, Ci, and Tr. However, after the AMF inoculation, these indicators returned to levels close to those without Cd stress. Therefore, Cd has an inhibitory effect on the photosynthetic intensity and efficiency of plants. However, AMF can effectively alleviate the negative effects of Cd on photosynthesis, thereby increasing photosynthetic products and alleviating the damage caused by Cd to plants.
During normal physical metabolism, plants produce reactive oxygen species (ROS). However, the generation and clearance of ROS are in a dynamic equilibrium. Once plants are subjected to adverse stress, this dynamic equilibrium is disrupted, leading to the accumulation of ROS, which causes membrane lipid peroxidation, leading to damage to the cell membrane structure as well as to lipids, proteins, and DNA [54,55]. During the development of plants, there is a set of protective enzyme systems within plant cells that prevent ROS from causing damage, such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR) [54]. The research by Zhang et al. [56] indicates that Cd stress increases the activity of lipoxygenase and NADPH oxidase, causing the significant accumulation of ROS (such as hydrogen peroxide and superoxide anion radicals), which subsequently leads to membrane lipid peroxidation in plants, resulting in the disruption of the cell membrane system, cell damage, and electrolyte leakage. Treatment with Cd caused significant increase in H2O2 content and triggered membrane lipid peroxidation in Perennial Ryegrass (Lolium perenne L.) [20]. The results of this study also indicated that Cd stress triggered an outbreak of ROS in tomato roots, causing damage to the cell membrane and the outflow of cytoplasm, and subsequently leading to membrane lipid peroxidation. This study also found that the AMF treatment significantly increased antioxidant enzyme activities (POD, SOD, CAT, etc.) to reduce ROS levels (hydrogen peroxide, superoxide anion radicals, etc.), thereby alleviating the damage caused by Cd stress to tomato seedlings. In another study, AMF alleviated Cd phytotoxicity mainly by promoting the immobilization and sequestration of Cd, reducing ROS production, and accelerating their scavenging in wheat (Triticum aestivum L.) [57]. AMF improved ROS scavenging efficiency (by enhancing the activity of POD and CAT) and alleviated oxidative stress in Perennial Ryegrass (Lolium perenne L.), thereby mitigating Cd poisoning [20]. These studies are in agreement with our study, showing that Cd induces the production of excessive ROS in plants. However, inoculation with AMF could enhance the activity of antioxidant enzymes in plants under Cd stress conditions, improve the plants’ antioxidant defense ability to reduce the content of ROS, maintain the redox balance within plant cells, protect the cell membrane’s function and structure, strengthen the antioxidant capacity, and mitigate Cd phytotoxicity to the cell membrane. AMF penetration and colonization involve a series of cytological and biochemical sequence of events and intracellular changes, including anti-oxidative damaging effect and ROS promotion [58]. In the early stages of the AMF–plant interaction, the mechanism of suppression or induction associated with plant defense holds the key to the plant–fungus compatibility in the context of this mutually beneficial symbiotic relationship [39]. The physiological processes include changes in the activation of plasma membrane-bound enzymes, kinases, phosphatases, and phospholipases; the permeability of the plasma membrane; and the production of signal molecules, including ROS. Regarding Cd stress, this study, in conjunction with previous studies, demonstrated that AMF are also involved in defense processes and mechanisms, potentially with effects on the induction of abiotic stress tolerance.
Under heavy metal stress conditions, plants will produce a large amount of osmotic regulatory substances. These substances not only maintain the cell turgor pressure and prevent excessive water loss from the protoplasm, but also stabilize the structure of organelles, in order to regulate various physiological functions and alleviate the damage caused by heavy metal stress to plants [59]. Proline (Pro), malondialdehyde (MDA), soluble proteins, and soluble sugars, among others, are all osmotic regulatory substances in plants [59]. The content of MDA significantly increased by 2.5-fold under Cd2+ stress in M. truncatula, indicating that Cd2+ caused oxidative damage to the cell membrane [17]. It is consistent with the conclusion of this study, which found that Cd stress increased the contents of osmotic regulatory substances (Pro, MDA, soluble protein, and soluble sugar) in the root systems of tomato seedlings. Such an increase is an adaptive response of tomato under heavy metal Cd stress, as it reduces lipid peroxidation in the cell membrane, alleviates membrane damage, and provides protection for the plants. This study also found that AMF could significantly reduce the accumulation of osmotic regulatory substances in the root systems of tomato, thereby alleviating the damage caused by Cd stress to tomato seedlings. This is in agreement with previous research results and further confirms the beneficial role of inoculating AMF in plants subjected to Cd stress to reduce lipid peroxidation [17,39]. Therefore, AMF can effectively alleviate the abnormal accumulation of osmotic regulatory substances induced by Cd, reduce the damage caused by membrane lipid peroxidation, and enhance the Cd tolerance of plants.
AMF also change the levels of phytohormones such as strigolactone (SL), IAA, tZR, GA3, and ABA, which confer resistance to abiotic stresses, including drought, salt, and heavy metal stresses, in host plants by coordinating multiple signal transduction pathways [57]. Strigolactone (SL) induces spore germination and promotes hyphal growth in AMF [60]. Application of the strigolactone GR24 improved Cd tolerance by regulating Cd uptake and antioxidant metabolism in Hordeum vulgare L. [61]. The high SL level in AMF-treated seedlings could lower Cd toxic action by regulating Cd accumulation and scavenging ROS in M. hupehensis [12]. AMF could also increase the seedling biomass of M. hupehensis under Cd stress conditions, possibly by increasing the IAA level in both the leaves and roots [12]. The increased IAA level in mycorrhizal tomato under Cd stress conditions strengthened the mutualism between AMF and the host plants. AMF could inhibit the expression of Cd transport and absorption genes, increase Cd content in cell walls, promote antioxidant enzyme biosynthesis, and alleviate Cd-mediated growth inhibition [18]. Relatively high root IAA levels were associated with higher plant Cd tolerance in mycorrhizal tomato under Cd stress conditions.
The normal functioning of respiratory metabolism plays a crucial role in the growth and development of plants. When plants are exposed to heavy metal stress, an appropriate amount of intermediate metabolic products serves as the foundation for their adaptation to heavy metal-contaminated soil [62]. As intermediate products of plant respiratory metabolism, succinic acid and malic acid are closely related to plant metabolic process. In this study, Cd stress significantly reduced the contents of malic acid and succinic acid in the roots, which is consistent with the research results reported in sunflower [63]. The concentration of respiratory metabolites in the root system is remarkably correlated with the root activity in the rhizosphere soil. Malic acid and succinic acid, as respiratory metabolites of the root system, could strengthen root activity and accelerate plant growth [62]. In this study, Cd stress might have inhibited tomato growth by reducing the levels of malic acid and succinic acid in the roots, thereby weakening the root respiration metabolism. AMF not only significantly promote plant growth and nutrient absorption, but also promote the secretion of low-molecular-weight organic acids (such as malic acid and succinic acid) by the roots. Low-molecular-weight organic acids have significant impacts on the physical and chemical properties of the soil and the toxicity of heavy metals to plants. They play a positive role in the activation and absorption of insoluble nutrients in the rhizosphere, converting insoluble substances into usable active components through acidification and other pathways, thereby promoting plant growth [64]. In this study, the AMF inoculation treatment significantly promoted the secretion of succinic acid and malic acid in the roots of tomato seedlings. Under Cd stress, low-molecular-weight organic acids can alter the speciation and bioavailability of heavy metals, thereby affecting the absorption and accumulation of Cd in plants [65]. The biological toxicity of Cd in soil mainly depends on its form. Cd exists in various forms in the soil, including in exchangeable form, iron–manganese oxide form, and organic-bound form. Some studies have shown that the inoculation of AMF reduces the content of exchangeable Cd, possibly because the change in the number of soil microorganisms improves the growth of plant roots and their absorption of nutrients, thereby altering the form of Cd [66]. Low-molecular-weight organic acids secreted by the root system are also one of the factors that affect the form of Cd. Among them, citric acid and malic acid can increase the content of exchangeable heavy metals in soil, thereby achieving the purpose of activating heavy metals [66]. Lactic acid and malic acid can also cause changes to the form of Cd by altering the pH value. The content of iron–manganese complexed Cd in soil treated with AMF increased significantly after inoculation [67]. A possible reason is that under the space limitation of the root bags, organic acids are concentrated, making it easier to alter the pH value and redox potential of the soil, thereby promoting the formation of iron–manganese complexed Cd [67]. The content of organic Cd is significantly reduced. A possible reason for this is that AMF, in order to provide more nutrients to the host plant, promote the decomposition of organic matter into small molecules that are easily absorbed by the host plant, thereby reducing the combination of organic matter and Cd, and resulting in a decrease in the content of organic-bound Cd [67]. This study found that AMF could, to some extent, alleviate the negative effects of Cd on the secretion of citric acid and malic acid by tomato roots and enhance the plant’s tolerance to heavy metals, thereby alleviating the inhibitory effect of Cd stress on plant growth. In this study, the AMF treatment significantly reduced the Cd content in tomato plants, indicating that the AMF treatment enhanced the tolerance of tomato plants to Cd by increasing the contents of malic acid and citric acid in the roots, thereby promoting root growth. The main reasons are as follows: First, the mycelia of AMF contain binding sites for heavy metals, allowing heavy metals to be adsorbed, bound, and fixed, thereby reducing the stress induced by heavy metals on the host plants. Second, the AMF inoculation significantly increased the biomass of tomato plants to be much higher than that of the control, which indirectly led to a decrease in the Cd content in the plants as the larger biomass had a dilution effect. Yu et al. [68] also indicated that the mycelium has a strong ability to adsorb Cd, which supports the significance of the AMF ecological function in this study. This research fully utilized the role of the AMF root exudate mycelium and examined the concentrations of low-molecular-weight organic acids secreted by the root system. The AMF inoculation promoted the complexation and chelation reactions between organic acids and Cd and reduced the toxicity of Cd to tomato plants, thereby enhancing the tolerance of tomato plants to Cd and promoting their growth.

5. Conclusions

While Cd can disrupt plant physiological processes, adversely affecting plant growth, oxidative stress responses, photosynthesis, and respiratory metabolism, among other processes, AMF may reduce Cd uptake in tomato seedlings. Furthermore, AMF could alleviate Cd phytotoxicity in tomato seedlings through multiple mechanisms, such as reducing Cd transport, accelerating plant growth, modulating organic acid exudation, and strengthening photosynthesis and antioxidant capacity. This study demonstrated that inoculation with AMF is an effective strategy for remediating Cd-polluted soil. However, the efficacy of AMF in reducing Cd phytotoxicity depends on several factors, such as environmental conditions, experimental duration, soil properties, and AMF taxa. Further knowledge of the intricate plant–AMF–Cd interactions is crucial for optimizing AMF-assisted phytoremediation strategies and developing Cd-tolerant and high-yielding crop varieties for cultivation in polluted soil.

Author Contributions

Conceptualization, Q.Y.; Data curation, D.Z., X.L. and J.Y.; Formal analysis, Y.Z.; Investigation, D.Z.; Project administration Q.Y.; Supervision, Q.Y.; Writing, D.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the open funds of the Open Fund of Hubei Key Laboratory of Spices & Horticultural Plant Germplasm Innovation & Utilization (No. 10) and the National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops (No. Horti-KF-2023-16).

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Horticulturae 11 01204 g001
Figure 1. Growth performance of Solanum lycopersicum after inoculation with AMF under Cd conditions. Note: (A)—0 μmol/L Cd+AMF, (B)—0 μmol/L Cd−AMF, (C)—50 μmol/L Cd+AMF, (D)—50 μmol/L Cd−AMF.
Figure 1. Growth performance of Solanum lycopersicum after inoculation with AMF under Cd conditions. Note: (A)—0 μmol/L Cd+AMF, (B)—0 μmol/L Cd−AMF, (C)—50 μmol/L Cd+AMF, (D)—50 μmol/L Cd−AMF.
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Figure 2. Root colonization of D. versiformis of Solanum lycopersicum inoculated with D. versiformis at 0 μmol/L Cd and 50 μmol/L Cd. Note: (A)—0 μmol/L Cd, (B)—50 μmol/L Cd.
Figure 2. Root colonization of D. versiformis of Solanum lycopersicum inoculated with D. versiformis at 0 μmol/L Cd and 50 μmol/L Cd. Note: (A)—0 μmol/L Cd, (B)—50 μmol/L Cd.
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Figure 3. Root system architecture of Solanum lycopersicum after inoculation with AMF under Cd conditions. Note: (A)—0 μmol/L Cd+AMF, (B)—0 μmol/L Cd−AMF, (C)—50 μmol/L Cd+AMF, (D)—50 μmol/L Cd−AMF.
Figure 3. Root system architecture of Solanum lycopersicum after inoculation with AMF under Cd conditions. Note: (A)—0 μmol/L Cd+AMF, (B)—0 μmol/L Cd−AMF, (C)—50 μmol/L Cd+AMF, (D)—50 μmol/L Cd−AMF.
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Table 1. Effects of AMF on plant growth of Solanum lycopersicum seedlings under Cd conditions.
Table 1. Effects of AMF on plant growth of Solanum lycopersicum seedlings under Cd conditions.
TreatmentsPlant Height (cm)Leaf Number (#)Totol Weight (g)Root Weight (g)Shoot Weight (g)
0 μmol/L Cd−AMF17.62 ± 1.06 b23.81 ± 1.18 b8.02 ± 0.49 b0.61 ± 0.05 b7.42 ± 0.44 b
+AMF25.98 ± 1.84 a34.89 ± 1.47 a11.08 ± 0.81 a0.87 ± 0.04 a10.34 ± 0.59 a
50 μmol/L Cd−AMF12.52 ± 1.06 c21.52 ± 1.51 c5.28 ± 0.29 c0.48 ± 0.03 c4.89 ± 0.37 c
+AMF15.93 ± 1.32 b23.54 ± 2.01 b7.71 ± 0.25 b0.58 ± 0.04 b7.31 ± 0.42 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 2. Root fungal colonization rate and root Cd content of Solanum lycopersicum seedlings.
Table 2. Root fungal colonization rate and root Cd content of Solanum lycopersicum seedlings.
TreatmentsRoot Fungal Colonization RateRoot Cd Content (mg/Kg)
0 μmol/L Cd−AMF0.00 ± 0.00 c0.00 ± 0.00 b
+AMF0.38 ± 0.03 a0.00 ± 0.00 b
50 μmol/L Cd−AMF0.00 ± 0.00 c19.32 ± 1.02 a
+AMF0.27 ± 0.02 b11.54 ± 1.04 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 3. Effects of AMF on root system architecture of Solanum lycopersicum under Cd conditions.
Table 3. Effects of AMF on root system architecture of Solanum lycopersicum under Cd conditions.
TreatmentsTotal Root Length (cm/plant)Total Root Surface Area (cm2/plant)Root Volume (cm3/plant)
0 μmol/L Cd−AMF72.73 ± 11.16 b6.49 ± 0.52 b0.39 ± 0.03 ab
+AMF102.59 ± 10.11 a9.43 ± 0.84 a0.46 ± 0.04 a
50 μmol/L Cd−AMF52.24 ± 14.05 c5.65 ± 0.49 b0.33 ± 0.03 b
+AMF65.29 ± 12.06 b6.08 ± 0.51 b0.37 ± 0.02 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 4. Effects of AMF on the chlorophyll contents and the parameters of chlorophyll fluorescence in leaves of Solanum lycopersicum under Cd conditions.
Table 4. Effects of AMF on the chlorophyll contents and the parameters of chlorophyll fluorescence in leaves of Solanum lycopersicum under Cd conditions.
TreatmentsChlorophyl a (mg/g)Chlorophyl b (mg/g)Total Chlorophyll (mg/g)φPSII Fv′/Fm′qP NPQ
0 μmol/L Cd−AMF2.15 ± 0.18 ab1.09 ± 0.08 ab3.21 ± 0.12 ab0.66 ± 0.04 ab0.85 ± 0.05 ab0.33 ± 0.02 ab0.81 ± 0.04 a
+AMF2.21 ± 0.17 a1.27 ± 0.11 a3.49 ± 0.21 a0.71 ± 0.05 a0.96 ± 0.07 a0.39 ± 0.02 a0.82 ± 0.05 a
50 μmol/L Cd−AMF1.22 ± 0.11 c0.55 ± 0.02 c1.71 ± 0.12 c0.43 ± 0.02 c0.42 ± 0.03 c0.12 ± 0.01 c0.89 ± 0.04 a
+AMF1.92 ± 0.13 b0.95 ± 0.04 b2.81 ± 0.18 b0.61 ± 0.03 b0.78 ± 0.04 b0.30 ± 0.02 b0.81 ± 0.06 a
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 5. Effects of AMF on the photosynthetic parameters in leaves of Solanum lycopersicum under Cd conditions.
Table 5. Effects of AMF on the photosynthetic parameters in leaves of Solanum lycopersicum under Cd conditions.
TreatmentsPn (μmol/m2·s)Gs (μmol/m2·s)Ci (μmol/mol)Tr (μmol/m2·s)
0 μmol/L Cd−AMF8.89 ± 0.79 ab2.88 ± 0.22 ab256.28 ± 24.12 b3.59 ± 0.22 ab
+AMF9.81 ± 0.63 a3.22 ± 0.23 a345.43 ± 29.19 a4.15 ± 0.26 a
50 μmol/L Cd−AMF5.91 ± 0.35 c1.92 ± 0.17 c165.62 ± 11.21 d2.55 ± 0.23 c
+AMF7.92 ± 0.49 b2.51 ± 0.21 b210.07 ± 19.29 c3.03 ± 0.29 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 6. Effects of AMF on the ROS levels in root of Solanum lycopersicum under Cd conditions.
Table 6. Effects of AMF on the ROS levels in root of Solanum lycopersicum under Cd conditions.
TreatmentsH2O2 (μmol/g)O2.− (μmol/g)
0 μmol/L Cd−AMF105.14 ± 9.26 c82.22 ± 2.15 c
+AMF111.25 ± 9.59 c85.39 ± 0.16 c
50 μmol/L Cd−AMF233.54 ± 10.01 a216.55 ± 0.10 a
+AMF155.71 ± 13.47 b145.59 ± 0.14 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 7. Effects of AMF on the antioxidant enzyme activity in root of Solanum lycopersicum under Cd conditions.
Table 7. Effects of AMF on the antioxidant enzyme activity in root of Solanum lycopersicum under Cd conditions.
TreatmentsSOD (U/min g)POD (U/min g)CAT (U/min g)
0 μmol/L Cd−AMF222.58 ± 20.15 c1980.21 ± 152.12 c105.91 ± 9.72 c
+AMF212.28 ± 11.18 c2004.92 ± 165.31 c108.32 ± 8.42 c
50 μmol/L Cd−AMF554.36 ± 44.38 b3755.42 ± 256.12 b189.23 ± 13.46 b
+AMF634.78 ± 50.46 a4212.22 ± 332.18 a246.08 ± 18.14 a
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 8. Effects of AMF on the osmotic regulating substances in root of Solanum lycopersicum under Cd conditions.
Table 8. Effects of AMF on the osmotic regulating substances in root of Solanum lycopersicum under Cd conditions.
TreatmentsPro (ug/g)MDA (μmol/g)Soluble Protein (mg/g)Soluble Sugar (μmol/g)
0 μmol/L Cd−AMF32.13 ± 2.26 c2.21 ± 0.13 c13.31 ± 1.02 c10.25 ± 0.92 c
+AMF30.65 ± 2.89 c2.13 ± 0.16 c13.88 ± 1.07 c11.08 ± 1.06 c
50 μmol/L Cd−AMF122.01 ± 10.36 a4.52 ± 0.29 a25.62 ± 2.09 a42.56 ± 3.09 a
+AMF74.52 ± 5.44 b3.11 ± 0.26 b18.55 ± 1.14 b21.59 ± 2.02 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 9. Effects of AMF on the contents of root phytohormone of Solanum lycopersicum under Cd conditions.
Table 9. Effects of AMF on the contents of root phytohormone of Solanum lycopersicum under Cd conditions.
TreatmentsIAA (ng/g FW)tZR (ng/g FW)GA3 (ng/g FW)ABA (ng/g FW)
0 μmol/L Cd−AMF15.16 ± 1.22 b510.31 ± 40.45 a353.41 ± 30.42 a156.80 ± 12.65 b
+AMF19.23 ± 1.49 a549.82 ± 50.19 a346.58 ± 30.13 a136.83 ± 10.26 c
50 μmol/L Cd−AMF9.26 ± 0.85 c404.31 ± 30.42 b338.62 ± 20.78 a191.97 ± 16.21 a
+AMF14.56 ± 1.15 b437.55 ± 32.13 b341.67 ± 31.69 a157.05 ± 12.06 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
Table 10. Effects of AMF on succinic acid and malic acid concentrations in Solanum lycopersicum root under Cd conditions.
Table 10. Effects of AMF on succinic acid and malic acid concentrations in Solanum lycopersicum root under Cd conditions.
TreatmentsMalic Acid (μmol·g−1 FM)Succinic Acid (μmol·g−1 FM)
0 μmol/L Cd−AMF0.81 ± 0.07 b1.14 ± 0.08 b
+AMF0.99 ± 0.06 a1.39 ± 0.12 a
50 μmol/L Cd−AMF0.67 ± 0.05 c0.85 ± 0.07 c
+AMF0.79 ± 0.06 b1.11 ± 0.09 b
Note: Different letters after the data in the column indicate significant differences between treatments at the 0.05 level, n = 5.
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Zhang, D.; Liu, X.; Zhang, Y.; Ye, J.; Yi, Q. Effects of Arbuscular Mycorrhizal Fungi on the Physiological Responses and Root Organic Acid Secretion of Tomato (Solanum lycopersicum) Under Cadmium Stress. Horticulturae 2025, 11, 1204. https://doi.org/10.3390/horticulturae11101204

AMA Style

Zhang D, Liu X, Zhang Y, Ye J, Yi Q. Effects of Arbuscular Mycorrhizal Fungi on the Physiological Responses and Root Organic Acid Secretion of Tomato (Solanum lycopersicum) Under Cadmium Stress. Horticulturae. 2025; 11(10):1204. https://doi.org/10.3390/horticulturae11101204

Chicago/Turabian Style

Zhang, Dejian, Xinyu Liu, Yuyang Zhang, Jie Ye, and Qingping Yi. 2025. "Effects of Arbuscular Mycorrhizal Fungi on the Physiological Responses and Root Organic Acid Secretion of Tomato (Solanum lycopersicum) Under Cadmium Stress" Horticulturae 11, no. 10: 1204. https://doi.org/10.3390/horticulturae11101204

APA Style

Zhang, D., Liu, X., Zhang, Y., Ye, J., & Yi, Q. (2025). Effects of Arbuscular Mycorrhizal Fungi on the Physiological Responses and Root Organic Acid Secretion of Tomato (Solanum lycopersicum) Under Cadmium Stress. Horticulturae, 11(10), 1204. https://doi.org/10.3390/horticulturae11101204

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