Next Article in Journal
A Dual-Source Energy Balance Model Coupled with Jarvis Canopy Resistance for Estimating Surface Evapotranspiration in Arid and Semi-Arid Regions
Previous Article in Journal
Foliar Spraying with Endophytic Trichoderma Biostimulant Increases Drought Resilience of Maize and Sunflower
Previous Article in Special Issue
Exploring the Roles of Arbuscular Mycorrhizal Fungi in Plant–Iron Homeostasis
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 14
Issue 12
10.3390/agriculture14122361
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Physio-Biochemical Mechanisms of Arbuscular Mycorrhizal Fungi Enhancing Plant Resistance to Abiotic Stress

by
Dandi Sun
1,
Xiaoqian Shang
1,
Hanwen Cao
1,
Soon-Jae Lee
2,
Li Wang
1,
Yantai Gan
1,3,† and
Shoujiang Feng
1,*
1
State & Local Joint Engineering Research Center for Ecological Treatment Technology of Urban Water Pollution, Zhejiang Provincial Key Lab for Water Environment and Marine Biological Resources Protection, College of Life and Environmental Science, Wenzhou University, Wenzhou 325035, China
2
Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland
3
Agriculture and Agri-Food Canada, Swift Current Research and Development Centre, Swift Current, SK S9H 3X2, Canada
*
Author to whom correspondence should be addressed.
†
Present address: Agroecosystems, The UBC-Soil Group, Tallus Heights, Kelowna, BC V4T 3M2, Canada.
Agriculture 2024, 14(12), 2361; https://doi.org/10.3390/agriculture14122361
Submission received: 27 October 2024 / Revised: 6 December 2024 / Accepted: 17 December 2024 / Published: 22 December 2024
(This article belongs to the Special Issue Mycorrhizal Symbiosis in Agricultural Production)
Browse Figures
Versions Notes

Abstract

:
Agricultural innovations in the past decades have addressed the mounting challenges of food, feed, and biofuel security. However, the overreliance on synthetic fertilizers and pesticides in agriculture has exacerbated biodiversity loss, environmental degradation, and soil health deterioration. Leveraging beneficial soil microorganisms, particularly arbuscular mycorrhizal (AM) fungi, offers an emerging solution to reduce dependence on synthetic agrochemicals in crop production. Understanding the mechanisms can help maximize AM fungi’s benefits in response to abiotic stresses. In this review, we explore the main mechanisms of AM fungi in promoting soil nutrient mobilization and uptake, increasing water absorption, stimulating antioxidative enzyme activities, altering morphophysiological structure, and performing hormonal crosstalk when mycorrhizal plants face an abiotic stressor. Also, we highlight the necessity of innovating practical ways to cope with variations in AM fungal species, diversity in host species, soil, and environmental conditions, as well as difficulties in mass multiplication for commercialization. Understanding the mechanisms and limitations may help explore the biofertilizer potential of AM fungal symbiosis, benefiting crop production while addressing the environment and soil health issues.

1. Introduction

Agriculture worldwide faces a significant challenge of meeting the ever-growing demands for food, feed, and fiber while adapting to global climate change [1,2]. Intensive farming systems through high production inputs have increased global food security and saved millions of lives in developing countries since the ‘Green Revolution’ [3]. However, the benefits of maximizing food production via high inputs occur at the cost of natural environments [4,5]. Excessive use of synthetic fertilizers and pesticides in intensive farming systems has adverse eco-environmental consequences [6,7], including water pollution [8,9], soil acidification [10,11], and loss of biodiversity [12]. In some irrigated areas, overuse of agrochemicals disrupts plant–soil–microbiome interactions [13,14], impeding the potential benefits of soil microbial communities [15,16]. Additionally, synthetic nitrogen-induced emissions contribute to elevated atmospheric CO2 levels [17,18] and exacerbate global climate change [19,20].
A sustainable alternative to traditional agrochemical-driven intensified farming systems is to harness the functional capabilities of soil microbial communities, such as arbuscular mycorrhizal (AM) fungal symbiosis. This plant–microbe mutualistic association occurs in nearly 80% of land plant species [21], including cultivated plants [22]. AM fungal spores colonizing plant roots through root cells, germinating spores form hyphal branches, and intraradical hyphae and establish mycelial nets (Figure 1). During symbiosis development, some cross-kingdom small RNAs (sRNA) transfer from host plants to mycorrhizal fungi through root hairs [23], underpinned by a bidirectional exchange of information [24]. Decades of research have helped our understanding of the evolutionary characteristics of AM fungi and the unique features of the microbiome-dominant hyphosphere [25]. AM fungal symbiosis can influence microbially driven carbon flux [26] and deliver multiple dimensions of ecosystem function [27]. More than two-thirds of terrestrial plants acquire nutrients through symbiosis with AM [25].
Symbiosis induces dramatic changes in plant carbon metabolism and nutrient remobilization in the rhizosphere, as the fungus requires C sources from host plants for spore propagation and extraradical hyphal development [28,29]. Carbon is supplied to AM fungal networks through photosynthesis and translocation from plant leaves to colonized sites in roots (Figure 2). The mutually beneficial symbiosis induces upward nutrient flow and downward carbon flow in the plant–soil–rhizosphere continuum. The AM fungi require C sources from host plants for spore propagation and extraradical hyphal development. In contrast, AM fungi produce a network of extraradical mycelium, spreading from host roots into the surrounding soil and establishing belowground interconnections to supply plant-required nutrients like P, N, Zn, Cu, and Mg. These functioning features occur in the hyphosphere with hyphal exudates and the other enzymes involved in the nutrient flow process. While the plant–AM fungi symbiotic relationship is a nutrient trade-off, the mutually beneficial association can enhance plant ability to acquire essential minerals, which is crucial for enhancing soil health through the contribution of hyphosphere microbiomes to nutrient cycling, carbon sequestration, and soil aggregation.
It is estimated that approximately 13 Gt of CO2 equivalent fixed by terrestrial plants is allocated to underground AM fungi per year, which is equivalent to 36% of the current annual CO2 emissions from fossil fuels [30]. In return, AM fungi produce a network of extraradical mycelia, spreading from host roots into the surrounding soil and establishing belowground interconnections that facilitate the acquisition of nutrients. These functions are crucial for the plant uptake of nutrients, such as phosphorus (P) [31,32], nitrogen (N) [33], and metallic micronutrients [34], while decreasing the ratios of soil-available Cd to Zn and Fe [35]. In addition, AM fungi play an important role in reducing greenhouse gas (GHG) emissions while enhancing soil health through the contribution of hyphosphere microbiomes to soil aggregation [36], carbon sequestration [37], and nutrient cycling [36]. Using 15N isotope tracing techniques, researchers [38] have demonstrated the positive effects of AM fungi on N2O emissions in maize (Zea mays L.) owing to changes in root traits, reduced (nirK + nirS)/nosZ ratio, and altered denitrifier community composition. A recent meta-analysis synthesizing the results of 13 peer-reviewed articles and three graduate theses showed that AM fungi significantly increased microbial biomass N and plant biomass, leading to reduced soil N2O emissions [39]. A pod experiment with pasture species under different air temperature regimes showed that AM fungal inoculation reduced N2O emissions at normal and elevated temperatures [40], implying that AM fungal symbiosis could play a role in mitigating the warming climate.
In addition to enhancing plant nutrition and soil health while reducing N2O-induced GHG emissions, AM fungal symbioses can systemically induce structural and biochemical changes in colonized plants when facing abiotic stressors. AM fungi-induced changes in root traits and soil denitrifier community composition can reduce soil N2O production in the presence of AMF hyphae [41], leading to decreased GHG emissions [38]. Similarly, AM fungi-induced changes in biochemical traits can enhance host plant resistance to abiotic stress. Here, we summarize the significant abiotic stresses that AM fungus-dominated hyphosphere microbiomes can help to reduce potential damage (Table 1), including, but not limited to, prolonged drought [42,43], extreme cold [44], high temperatures [26,45], heavy metals [46,47], herbivorous nematodes [48], high salinity [49], and microplastic contamination in soil [50,51]. Consequently, AM fungal symbiosis helps to increase soil productivity. A recent meta-analysis of synthesizing 168 studies across the globe revealed that 77% of AM fungi-infested crops increased yield by an average of 21% [52]. Yield increases were observed in many staple food crops, such as barley, maize, rice, and wheat, tested under various cropping management (Table 2 and Table 3).
Despite their potential, many questions concerning the effects of AM fungal networks on real-world agriculture still need to be answered. What mechanisms govern the complex interactions among host plants, AM fungi, plant–AM fungi compatibility, and the potential synergetic effect remains unclear. Understanding the possible mechanisms will help harness the biological potential of AM fungal symbiosis to support agroecosystem functioning and alleviate agrochemical-induced adverse environmental impacts. Therefore, this study aimed to (i) analyze the mechanisms by which AM fungi help plants resist a range of abiotic stresses, (ii) highlight the disentangling of signaling pathways and regulatory mechanisms between the two partners when facing an abiotic stressor, and (iii) discuss the potential use of AM fungal symbiosis in the development of biofertilizers for real-world agriculture.

2. Physio-Biochemical Mechanisms of AM Fungi Enhancing Plant Resistance to Abiotic Stress

2.1. Mechanisms for AM Fungi Enhancing Nutrient Uptake

A significant challenge in crop production is optimizing the plant nutrient supply for maximal yield. Among the essential nutrients for plant growth and development is phosphorus (P), a vital component in converting the sun’s energy into food, fiber, and oil; metabolizing sugar and energy storage; promoting cell division and enlargement; and transferring genetic information. However, P fixation occurs when applied to soil, where it reacts with other minerals to form insoluble compounds that are not readily available to plants. Additionally, P fertilizers are limited by the finite availability of rock phosphate for manufacturing [99]. AM fungi can mobilize organic P [31] and enhance plant P uptake from the soil [100]. In tomato (Solanum lycopersicum L.), AM fungi modulates both P and Zn uptake; when Zn concentration is below a threshold, AM fungi enhance Zn uptake, while when Zn is above the critical concentration, AM fungi restrict Zn translocation to plant shoots [45]. The synergistic relationship between Zn and AM fungi increases lycopene, vitamin C, and vitamin A contents and enhances antioxidant activities compared to non-AM fungal tomatoes. Similarly, the symbiosis between the AM fungal species Rhizophagus irregularis CD1 and cotton (Gossypium hirsutum L.) enhances the expression of specific P transporter genes [101], leading to enhanced photosynthesis and cotton yield (by 29%) due to a concomitant increase in chlorophyll pigments [100].
Studies have shown that the AM network facilitates nutrient uptake through two pathways (Figure 2): (i) the colonization of multiple fungal species on the host plant, forming mycelia across different AM fungi [102], where hyphae extend from one host’s root system to another, with individual plants acting as the source of carbon responsible for the growth of hyphal networks [28,103]; and (ii) hyphal fusion, known as anastomosis [104], between the hyphae of different AM species through self-recognition, where fused hyphae colonize the roots of adjacent plants within the plant community, forming extended AM fungal networks [105]. Although these networks can form from a single AM species connecting individual plants, they become highly complex and fluctuate dynamically with increasing microbial species diversity. Multiple AM fungal species or different microbiomes can colonize plants simultaneously, and a single plant species can connect multiple AM fungal species to form distinct AM networks [106], which can nest within the broader network formed by multiple strains.
The interaction among the host plants, AM fungi, and the associated bacteria such as endobacteria living inside AM fungi can lead to a plant–AM fungi–bacterium continuum in the hyphosphere that facilitates top-down carbon flow and bottom-up mineral flow (especially phosphorus and nitrogen) via the continuum (Figure 3) [107]. Some AM fungal hyphae recruit distinct microbes into their hyphosphere [25], where the microbiome interactions stimulate nutrient mobilization and turnover. In contrast, the other AM fungal species can cooperate with N2-fixing bacteria, converting atmospheric N2 molecules into a form usable by the plant [108]. For example, in the model grass Brachypodium distachyon, the synergetic relationship of the AM Rhizophagus irregularis and soil microbial communities led to a doubling of the N that mycorrhizal plants acquire from organic matter and a tenfold increase in N acquisition compared to non-mycorrhizal plants grown in the absence of soil microbial communities. Although AM fungi lack efficient exoenzymes to access organic nutrients directly, multipartite synergies or microbial interplay may be involved in efficient organic N utilization by AM fungal hyphae [109].

2.2. Mechanisms for AM Fungi Enhancing Water Absorption Under Abiotic Stress

When plants face severe drought stress, plant–AM fungal symbiosis can enhance plants’ ability to absorb more water through the following mechanisms. First, AM fungal colonization stimulates the growth of root hairs, thereby increasing the root surface area for water absorption. Hyphal exploration in the rhizosphere extends the network into the soil profile, allowing plants to access water from a larger soil volume. Second, AM fungi can increase soil water absorption by altering the permeability and transport capabilities of the root membrane, thereby allowing more water absorption from the soil solution. Third, AM fungi contribute to forming the soil aggregates, providing spatially heterogeneous microenvironments for fine-scale organization of the soil microbiome and associated biogeochemistry, which facilitates plant water uptake. However, the assemblage of the core members of hyphosphere microbiomes is mediated by environmental factors such as soil physicochemical properties, which affect AM functioning [110].

2.3. AM Fungi Promote Osmotic Regulation Under Drought Stress

Drought is one of the most frequently occurring abiotic stressors in crop production. Numerous studies have documented that crop plants have evolved a dedicated mechanism to tolerate mild-to-moderate levels of drought stress by performing osmotic regulation, a critical adaptive mechanism in response to stress [111,112,113,114]. In adverse environmental conditions, such as drought, osmotic adjustment enables plants to maintain cell turgor and rigidity by preventing water loss, thus surviving stress [115]. The magnitude of the osmotic adjustment effect varies among cultivars, and some genotypes resist dehydration better than others due to different drought adaptation mechanisms, such as morphological, physiological, and biochemical traits [116]. For example, wheat genotypes with longer spikes or rolling leaves can delay or prevent cell death and help maintain productivity under water-stress conditions. The postulation of genes signals the pathways for plants to synthesize cellular solutes, such as sugars, prolines, and other amino acids like glycine betaine and β-alanine betaine, that modulate osmotic adjustment at the cellular level, whole plant, and ecosystem scale in the presence of AM fungal symbiosis.
At the cellular level, two fundamental plant functions—photosynthesis and transpiration—are crucial for osmotic adjustment. Plant stomata regulate these processes, satisfying the demand for CO2 via photosynthesis while controlling water loss, ensuring a productive soil‒root‒xylem‒atmospheric hydraulic system (Figure 3). The balance between water vapor loss from leaves to the atmosphere and the water supply from soil to leaves regulates the CO2 supply via stomata and biochemical demand for CO2, which revolves around maintaining a specific pressure level (Figure 3a). Stomatal conductance, a measure of gaseous diffusion capacity, primarily dictates the exchange of gasses into and out of leaves, and is determined by the stomatal density and pore aperture (Figure 3b). Physical pore dimensions and stomatal density determine the maximum stomatal conductance. Plants with rapid stomatal kinetics can maximize CO2 uptake while minimizing unnecessary water loss, resulting in higher water-use efficiency.
In the whole plant system, plants use strategies to mitigate the effect of drought stress. Some plants maintain their leaf water potential by rapidly closing their stomata to reduce gas exchange and photosynthesis. Others, however, close their stomata later, allowing the leaf water potential to drop while maintaining higher gas exchange and carbon assimilation. When water stress exceeds a critical threshold, the leaf water potential drops to a point where cavitation occurs, which leads to a rapid loss of hydraulic conductivity in the soil–root–xylem system, influencing whole-plant CO2 assimilation and transpiration [117] (Figure 3a).
At the ecosystem scale, the relationship between water and CO2 fluxes changed from linear to nonlinear under drought stress conditions due to the canopy structure and associated environmental conditions (Figure 3c). Canopy temperature, relative humidity, leaf area index, net ecosystem exchange, and soil water content drive osmotic adjustment. During osmotic regulation, the accumulation of solutes in vacuoles, a reversible physiological process, helps buffer cytosolic solutes and supports metabolism. AM fungal symbiosis helps plants regulate turgor pressure by increasing accumulative solutes through the elastic adjustment of cell membranes, which is critical in tolerance to dehydration. This finding emphasizes the importance of osmotic adjustment in supporting production under water stress in mycorrhizal plants.

2.4. AM Fungi Promote Stress-Related Gene Expression Under Abiotic Stress

Studies have shown that symbiotic interactions play a crucial role in enhancing the ability of plants to cope with abiotic stress by inducing the expression of a series of genes involved in stress response and signaling pathways. Genes encoding transcription factors, kinases, and other regulatory proteins can mediate the effects of hormones, such as auxins, cytokinins, and abscisic acid [118]. The production of stress-related proteins and other molecules enables plants to survive abiotic stress. For example, when plants are under nutrient deficiency stress, AM fungi induce the expression of genes encoding nutrient transporters, stimulating the defense-related signaling molecules involved in nutrient cycling [119]. Under salt stress, AM fungi induce the expression of salt-responsive plant genes, including those coding for osmoprotectants and other stress-responsive proteins, thereby enhancing plant salt tolerance [120].
Similarly, AM fungi can affect the expression of genes related to photosynthesis and carbon metabolism [121]. This includes gene coding for carbon fixation, storage, and allocation enzymes, crucial for plant growth and development and carbon allocation to the active sites. In the following sections, we will show that AM fungi can regulate root morphological changes, such as branching, root hair volumes, and root architecture, which involve the expression of genes coding for plant meristem and root activities.
Furthermore, under abiotic stress, AM fungi induce the expression of genes involved in synthesizing secondary metabolites, such as those encoding enzymes that produce defense compounds, such as phenolics and alkaloids. Likewise, AM fungi can activate or upregulate the expression of genes encoding antioxidant enzymes. This is achievable through the action of transcription factors in response to various stimuli, such as oxidative stress or hormonal signals. AM fungi can modulate the activity of existing enzymes, thereby increasing their catalytic activity, stability, and localization. However, the specific genes regulated by AM fungi can vary depending on the plant species, AM fungal strain, and environmental conditions. AM fungi-induced changes in gene expression are part of a complex signaling network that governs plant growth, development, and responses to environmental stresses. Advanced molecular techniques have been developed over the last few decades to understand the mechanisms governing stress tolerance at the genetic level. The discovery of microRNAs (miRNAs) that regulate gene expression and post-translational modifications of proteins to accommodate more complex functions for the same set of genes has proven critical in understanding abiotic stress tolerance. With CRISPR technology, scientists have a more significant and faster chance of incorporating abiotic stress tolerance into crop plant management. The new CRISPR-based tools and modifications may help researchers gain new insights into the biochemical mechanisms responsible for abiotic stress.

2.5. AM Fungi Enhancing Antioxidant Activity in Response to Abiotic Stress

Studies have shown that AM fungi can regulate the activities of various antioxidant enzymes to protect plant cells from oxidative damage caused by free radicals, such as reactive oxygen species (ROS) and reactive nitrogen species (RNS) (Figure 4) [122,123]. These free radicals act as signaling molecules, playing an important role in attacking plant cells; however, the magnitude of the damage depends on the equilibrium between the production and scavenging of these reactive species. Antioxidant enzymes are crucial for neutralizing reactive species and maintaining cellular redox balance. AM fungi operate through redox signaling with small molecules, such as hydrogen peroxide (H2O2) or nitric oxide (NO), acting as secondary messengers to regulate the activity of antioxidant enzymes. For example, H2O2 can activate specific protein kinases that phosphorylate antioxidant enzymes.
The antioxidant machinery may include both enzymatic and non-enzymatic components. The former includes main enzymes, such as superoxide dismutase (SOD), the universal enzyme of organisms that live in the presence of oxygen. Under abiotic stress, this enzyme catalyzes the conversion of superoxide into oxygen and hydrogen peroxide. Superoxide anions are the intended products of dedicated signaling enzymes and the byproducts of several metabolic processes, including mitochondrial respiration. Through its activity, SOD controls the levels of a variety of ROS and RNS, both limiting the potential toxicity of these molecules and controlling a broad aspect of cellular life. Aerobic organisms, such as crop plants, have multiple SOD proteins targeted to different cellular and subcellular locations, reflecting the multiple sources of their substrate superoxide [124].
Other antioxidant enzymes that AM fungi can stimulate include aspectate peroxidase (APX), which catalyzes the reduction of H2O2 using ascorbate (vitamin C) as an electron donor [125]. AM fungi can affect the expression of APX genes, enhancing the capacity of plants to utilize ascorbate for H2O2 detoxification [126]. Another important antioxidant enzyme AM fungi may stimulate is glutathione peroxidase (GPX), which reduces H2O2 to water. When facing an abiotic stressor, AM fungi regulate the expression of GPX genes, supporting the plant glutathione-dependent antioxidant system [127]. In the scientific literature, AM fungi regulate many other antioxidant enzymes in the presence of an abiotic stressor, including glutathione S-transferase (GST) [128], an enzyme that uses glutathione to conjugate electrophilic compounds, such as those generated by ROS; peroxiredoxin (PRX) [129], a family of enzymes that can reduce peroxides using thioredoxin or other reducing cofactors; thioredoxin peroxidase (TPX) [130], an enzyme that uses thioredoxin to reduce peroxides, supporting the plant’s thioredoxin-dependent antioxidant system; and CAT [131], one of the main scavengers of H2O2. Increased CAT activity in the presence of AM fungi led to subsequent H2O2 detoxification in response to thermotolerance. These antioxidant enzymes can form a network of signaling pathways, providing coordinated regulation of metabolites to enhance plant stress tolerance [132].
The specific antioxidant enzymes regulated by AM fungi can vary depending on the plant species, AM fungal strain, and environmental conditions. AM fungi-induced changes in antioxidant enzyme expression are part of a complex signaling network that governs plant growth, development, and responses to environmental stresses. In recent years, many oxidative stress biomarkers have developed with specific complications associated with AM fungal symbiosis, which helps to understand the biochemical mechanisms responsible for enhanced resistance to abiotic stresses. However, uncertainties and controversies exist due to the need for appropriate tools and methodologies to evaluate these processes.

2.6. AM Fungi Modulating Hormonal Crosstalk Under Abiotic Stress

Hormones play a crucial role in metabolic flux regulation, affecting processes like photosynthesis, respiration, and biosynthesis. For instance, hormones regulate the ABA levels, influencing stomatal closure to conserve water and balance stress response and cell growth. Under adverse environmental conditions like high-temperature stress, AM fungi can perform hormonal crosstalk by directly influencing the production and metabolism of plant hormones that regulate the levels of auxins, cytokinins, and many abscisic acids, such as ABA (Figure 3). In mycorrhizal plants, AM fungi can induce the accumulation of osmoprotectants in roots [122], which helps to maintain root cell turgor and protect against osmotic stress, supporting root function and growth when water is below an optimal level for plant absorption. By modulating the plant’s auxins profile, AM fungi induce changes in root architecture and carbon fixation and maintains a more open stomatal aperture to prevent water loss, helping the plant cope with the specific stressor. For example, Poncirus trifoliata seedlings inoculated with AM fungus Funneliformis mosseae and S. indica, singly or in combination for 20 weeks, significantly increased root biomass, root total length, diameter and surface area, and lateral roots, which were associated with the increased concentrations of indoleacetic acid, indole butyric acid, trans-zeatin, dihydro-zeatin, and isopentenyl adenine in leaves and roots [133].
An interaction of AM fungi and ABA can simultaneously affect plants’ tolerance to abiotic stressors. In a controlled environmental study, adding ABA enhanced AM colonization and promoted plant growth [134]. Under Zn stress, a combination of AM fungi and ABA addition increased the ABA content in plant parts by 48–172% in AM plants compared to non-mycorrhizal plants [134]. Using tomato (Lycopersicon esculentum) mutants to study the role of ABA on the establishment of AM fungal symbiosis, researchers found that exogenous ABA and silver thiosulfate (STS) stimulate the putative antagonistic crosstalk between ABA and ethylene, which plays a vital role in the development of the complete arbuscular and its functionality [135].
A well-documented example of AM fungi modulating hormonal crosstalk under abiotic stress is the enhancement of auxin levels in the root system [134]. Increased auxin levels can promote root branching and growth, which is beneficial for nutrient uptake and water absorption. The increased auxin levels can also affect the transport of auxins to other parts of the plant, influencing other tissues’ development. Another example of AM fungi modulating hormonal crosstalk under abiotic stress is the production of gibberellins [136] involved in seed germination, stem elongation, and flowering. The enhanced gibberellins levels can promote plant growth in limited resources.
Similarly, AM fungi can influence cytokinin levels [134], essential for cell division and differentiation. By altering cytokinin levels, AM fungi can affect the balance between root and shoot growth. Furthermore, AM fungi can induce the production of secondary metabolites, such as phenolics and alkaloids, which are essential for plant defense against abiotic stressors. The biosynthesis of these compounds requires metabolic flux adjustments. By influencing these factors, AM fungi help plants maintain metabolic flux adjustments and enhance their tolerance to various stresses. Studies have demonstrated that fungal signals and host receptor-mediated signals regulate AM symbiosis. The molecular players regulate cooperative fungal colonization and symbiosis functionality when the host faces an abiotic stressor.

2.7. Hyphosphere Regulates Fungal Functioning to Abiotic Stress

These above findings indicate that the hyphosphere microbiomes open a new avenue for developing biofertilizer formulas. In practice, developing AM fungi-friendly nutrient management strategies will have long-term positive effects on sustainable agriculture, simultaneously providing food security and increasing resource use efficiency while maintaining soil health and environmental integrity. These findings also demonstrate that the symbiotic relationship between AM fungi and plants is a critical factor influencing plant metabolic adaptation to changing environments. By modulating hormonal crosstalk and gene expression, enhancing nutrient uptake and water absorption, and stimulating antioxidant activities and osmotic regulation in response to abiotic stress, AM fungi help the plant to prioritize between growth and defense, and consequently reduces damage caused by specific abiotic stressors and maintains or even increases productivity. However, AM fungi operate through a complex network of interactions among these factors. The particular mechanisms can vary depending on the plant species, the type of environmental stress encountered, and the developmental stage of the host plant. Plant and AM fungi regulate the interaction at the cellular, molecular, and genetic levels, and it is highly dependent on environmental and biological variables.

3. Limitations

Introducing AM fungi into agricultural systems involves many interactions among AM fungi, other microbes, soil conditions, and anthropogenic activities. Understanding these interactions is crucial for optimizing the benefits of AM fungi in agricultural use. Harnessing microbial communities can enhance nutrient uptake, improve soil structure, and increase plant resilience to abiotic and biotic stresses. However, the harnessing of the benefits of AM via the artificial augmentation process is limited. At the same time, the natural presence of AM fungi is insufficient to supply nutrients for the growth of crop plants. There are challenges to the mass multiplication of AM fungi for agricultural commercialization. While a variety of techniques such as hydroponics, aeroponics, and nutrient flow are available for the mass production of AM fungi, it is costly at present for inoculum purity testing and quality control due to the obligate nature of AM fungi and the low-quality inocula that are accessible in the market. To exploit the positive effects of mycorrhizal symbiosis, the protection and proper management of native AM fungal populations is required. We must improve to minimize disruption to soil microorganism communities, such as frequent tillage, excessive synthetic agrochemical inputs, and intensive cropping. We urge a shift in agricultural practices, such as using reduced or zero tillage to accommodate AM fungi in a favorable microenvironment. In designing an effective crop rotation, selecting plant species that have a natural affinity for AM fungi and readily form mycorrhizae with them compatibly can maximize the benefits. Also, decades of breeding programs focusing on high crop yields using genes from narrowed genetic backgrounds may have compromised naturally beneficial symbiotic partners. Some traditional breeding approaches may need to utilize the multigenic nature of resistance to abiotic stressors. Host plant diversity, such as cereal–oilseed–legume–forage in crop rotation, is essential for optimizing AM fungal diversity and its functioning in cropping systems. Also, there are variations in the defense mechanisms induced by different AM species across diverse plants and environments. In practical applicability, we must ensure the quality and viability of AM fungi inoculants (products containing live AM fungi) for successful colonization and improve the effectiveness of the specific AM fungal strains in agricultural settings.

4. Conclusions

Sustaining food production under the impact of global climate change is a pressing challenge in the 21st century. Current agricultural practices that rely on synthetic fertilizers and pesticides have led to soil health and environmental issues, necessitating alternative approaches. The introduction of AM fungi into agricultural systems provides an emerging solution. This review highlights recent research progress and knowledge about the underlying mechanisms for AM symbiosis and its regulation. This will help facilitate agricultural biotechnological procedures to improve AM colonization and use efficiency in real-world agriculture. However, the multitude of interactions of host plants–AM fungi-associated microorganisms–soil environmental conditions are complex, and various anthropogenic activities can interface with the performance of the interactive symbiosis. The effectiveness of AM fungal symbiosis in agricultural use can be further complicated by variability in AM species and the diversity of host plant communities and soil microenvironments. Also, a lack of standardized AM inoculant applications may have influenced the efficacy of AM use at scale. Nonetheless, advances in molecular tools enable researchers to have a deeper understanding of transcriptional modules regulating the establishment of AM symbiosis. Technological innovations in plant genetics and molecular biology allow researchers to understand the specific interactions and crosstalk between transcription factors and transcription regulators in AM symbiosis. A rapid rise in interest in the scientific community for mycorrhizal symbiosis has encouraged societal exploration of AM fungi’s potential to transform traditional agriculture into a more resilient and preserving agricultural ecosystem.

Author Contributions

D.S., X.S. and H.C. conducted literature search, data collection, and prepared visual presentations; S.F., L.W. and Y.G. conceptualized the work and performed administration of the project; S.-J.L. reviewed different versions of the paper. All the authors wrote and edited different sections. Y.G. finalized the submitted version. All authors have read and agreed to the published version of the manuscript.

Funding

This project was supported by the National Natural Science Foundation of China (No. 32472826), Wenzhou University Research Start-Up Fund (No. QD2024084), and Wenzhou Talent Introduction Fund.

Conflicts of Interest

The authors declare that the research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Godfray, H.C.J.; Beddington, J.R.; Crute, I.R.; Haddad, L.; Lawrence, D.; Muir, J.F.; Pretty, J.; Robinson, S.; Thomas, S.M.; Toulmin, C. Food security: The challenge of feeding 9 billion people. Science 2010, 327, 812–818. [Google Scholar] [CrossRef]
  2. Wheeler, T.; Von Braun, J. Climate change impacts on global food security. Science 2013, 341, 508–513. [Google Scholar] [CrossRef] [PubMed]
  3. Pingali, P.L. Green Revolution: Impacts, limits, and the path ahead. Proc. Natl. Acad. Sci. USA 2012, 109, 12302–12308. [Google Scholar] [CrossRef] [PubMed]
  4. Weiskopf, S.R.; Isbell, F.; Arce-Plata, M.I.; Di Marco, M.; Harfoot, M.; Johnson, J.; Lerman, S.B.; Miller, B.W.; Morelli, T.L.; Mori, A.S.; et al. Biodiversity loss reduces global terrestrial carbon storage. Nat. Commun. 2024, 15, 4354. [Google Scholar] [CrossRef] [PubMed]
  5. van der Putten, W.H.; Bardgett, R.D.; Farfan, M.; Montanarella, L.; Six, J.; Wall, D.H. Soil biodiversity needs policy without borders soil health laws should account for global soil connections. Science 2023, 379, 32–34. [Google Scholar] [CrossRef]
  6. Cui, Z.; Zhang, H.; Chen, X.; Zhang, C.; Ma, W.; Huang, C.; Zhang, W.; Mi, G.; Miao, Y.; Li, X.; et al. Pursuing sustainable productivity with millions of smallholder farmers. Nature 2018, 555, 363–366. [Google Scholar] [CrossRef] [PubMed]
  7. Tian, H.; Xu, R.; Canadell, J.G.; Thompson, R.L.; Winiwarter, W.; Suntharalingam, P.; Davidson, E.A.; Ciais, P.; Jackson, R.B.; Janssens-Maenhout, G.; et al. A comprehensive quantification of global nitrous oxide sources and sinks. Nature 2020, 586, 248. [Google Scholar] [CrossRef] [PubMed]
  8. Guo, Y.; Chen, Y.; Searchinger, T.D.; Zhou, M.; Pan, D.; Yang, J.; Wu, L.; Cui, Z.; Zhang, W.; Zhang, F.; et al. Air quality, nitrogen use efficiency and food security in China are improved by cost-effective agricultural nitrogen management. Nat. Food 2020, 1, 648–658. [Google Scholar] [CrossRef] [PubMed]
  9. Gu, B.; Zhang, X.; Lam, S.K.; Yu, Y.; van Grinsven, H.J.M.; Zhang, S.; Wang, X.; Bodirsky, B.L.; Wang, S.; Duan, J.; et al. Cost-effective mitigation of nitrogen pollution from global croplands. Nature 2023, 613, 77–84. [Google Scholar] [CrossRef] [PubMed]
  10. Marris, E. A world without soil: The past, present, and precarious future of the Earth beneath our feet. Nature 2022, 601, 503–504. [Google Scholar] [CrossRef]
  11. Lu, X.; Mao, Q.; Gilliam, F.S.; Luo, Y.; Mo, J. Nitrogen deposition contributes to soil acidification in tropical ecosystems. Glob. Chang. Biol. 2014, 20, 3790–3801. [Google Scholar] [CrossRef] [PubMed]
  12. de Lange, E.; Sze, J.S.; Allan, J.; Atkinson, S.; Booth, H.; Fletcher, R.; Khanyari, M.; Saif, O. A global conservation basic income to safeguard biodiversity. Nat. Sustain. 2023, 6, 1016–1023. [Google Scholar] [CrossRef]
  13. Tilman, D.; Clark, M.; Williams, D.R.; Kimmel, K.; Polasky, S.; Packer, C. Future threats to biodiversity and pathways to their prevention. Nature 2017, 546, 73–81. [Google Scholar] [CrossRef] [PubMed]
  14. Godfray, H.C.J. Food and Biodiversity. Science 2011, 333, 1231–1232. [Google Scholar] [CrossRef]
  15. Li, R.; Ren, C.; Wu, L.; Zhang, X.; Mao, X.; Fan, Z.; Cui, W.; Zhang, W.; Wei, G.; Shu, D. Fertilizing-induced alterations of microbial functional profiles in soil nitrogen cycling closely associate with crop yield. Environ. Res. 2023, 231, 116194. [Google Scholar] [CrossRef]
  16. Hartmann, M.; Six, J. Soil structure and microbiome functions in agroecosystems. Nat. Rev. Earth Environ. 2023, 4, 4–18. [Google Scholar] [CrossRef]
  17. Crippa, M.; Solazzo, E.; Guizzardi, D.; Monforti-Ferrario, F.; Tubiello, F.N.; Leip, A. Food systems are responsible for a third of global anthropogenic GHG emissions. Nat. Food 2021, 2, 198–209. [Google Scholar] [CrossRef]
  18. Qian, H.; Zhu, X.; Huang, S.; Linquist, B.; Kuzyakov, Y.; Wassmann, R.; Minamikawa, K.; Martinez-Eixarch, M.; Yan, X.; Zhou, F.; et al. Greenhouse gas emissions and mitigation in rice agriculture. Nat. Rev. Earth Environ. 2023, 4, 716–732. [Google Scholar] [CrossRef]
  19. Steel, D.; DesRoches, C.T.; Mintz-Woo, K. Climate change and the threat to civilization. Proc. Natl. Acad. Sci. USA 2022, 119, e2210525119. [Google Scholar] [CrossRef]
  20. Webb, P.; Benton, T.G.; Beddington, J.; Flynn, D.; Kelly, N.M.; Thomas, S.M. The urgency of food system transformation is now irrefutable. Nat. Food 2020, 1, 584–585. [Google Scholar] [CrossRef]
  21. Brundrett, M.C.; Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 2018, 220, 1108–1115. [Google Scholar] [CrossRef] [PubMed]
  22. Wang, L.; Liu, Y.; Zhu, X.; Zhang, Y.; Yang, H.; Dobbie, S.; Zhang, X.; Deng, A.; Qian, H.; Zhang, W. Effects of arbuscular mycorrhizal fungi on crop growth and soil N2O emissions in the legume system. Agric. Ecosyst. Environ. 2021, 322, 107641. [Google Scholar] [CrossRef]
  23. Wong-Bajracharya, J.; Singan, V.R.; Monti, R.; Plett, K.L.; Ng, V.; Grigoriev, I.V.; Martin, F.M.; Anderson, I.C.; Plett, J.M. The ectomycorrhizal fungus Pisolithus microcarpus encodes a microRNA involved in cross-kingdom gene silencing during symbiosis. Proc. Natl. Acad. Sci. USA 2022, 119, e2103527119. [Google Scholar] [CrossRef] [PubMed]
  24. Ledford, W.C.; Silvestri, A.; Fiorilli, V.; Roth, R.; Rubio-Somoza, I.; Lanfranco, L. A journey into the world of small RNAs in the arbuscular mycorrhizal symbiosis. New Phytol. 2023, 237, e19394. [Google Scholar] [CrossRef]
  25. Zhang, L.; Zhou, J.; George, T.S.; Limpens, E.; Feng, G. Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends Plant Sci. 2022, 27, 402–411. [Google Scholar] [CrossRef]
  26. Lutz, S.; Bodenhausen, N.; Hess, J.; Valzano-Held, A.; Waelchli, J.; Deslandes-Hérold, G.; Schlaeppi, K.; van der Heijden, M.G.A. Soil microbiome indicators can predict crop growth response to large-scale inoculation with arbuscular mycorrhizal fungi. Nat. Microbiol. 2023, 8, 2277–2289. [Google Scholar] [CrossRef]
  27. Fan, K.; Chu, H.; Eldridge, D.J.; Gaitan, J.J.; Liu, Y.-R.; Sokoya, B.; Wang, J.-T.; Hu, H.-W.; He, J.-Z.; Sun, W.; et al. Soil biodiversity supports the delivery of multiple ecosystem functions in urban greenspaces. Nat. Ecol. Evol. 2023, 7, 113–126. [Google Scholar] [CrossRef]
  28. Durant, E.; Hoysted, G.A.; Howard, N.; Sait, S.M.; Childs, D.Z.; Johnson, D.; Field, K.J. Herbivore-driven disruption of arbuscular mycorrhizal carbon-for-nutrient exchange is ameliorated by neighboring plants. Curr. Biol. 2023, 33, 2566–2573.e4. [Google Scholar] [CrossRef]
  29. Müller, L.M. Underground connections: Arbuscular mycorrhizal fungi influence on interspecific plant-plant interactions. Plant Physiol. 2021, 187, 1270–1272. [Google Scholar] [CrossRef]
  30. Hawkins, H.-J.; Cargill, R.I.M.; Van Nuland, M.E.; Hagen, S.C.; Field, K.J.; Sheldrake, M.; Soudzilovskaia, N.A.; Kiers, E.T. Mycorrhizal mycelium as a global carbon pool. Curr. Biol. 2023, 33, 560–573. [Google Scholar] [CrossRef]
  31. Wang, L.; Zhang, L.; George, T.S.; Feng, G. A core microbiome in the hyphosphere of arbuscular mycorrhizal fungi has functional significance in organic phosphorus mineralization. New Phytol. 2023, 238, 859–873. [Google Scholar] [CrossRef] [PubMed]
  32. Mei, L.; Yang, X.; Zhang, S.; Zhang, T.; Guo, J. Arbuscular mycorrhizal fungi alleviate phosphorus limitation by reducing plant N:P ratios under warming and nitrogen addition in a temperate meadow ecosystem. Sci. Total Environ. 2019, 686, 1129–1139. [Google Scholar] [CrossRef] [PubMed]
  33. Xie, K.; Ren, Y.; Chen, A.; Yang, C.; Zheng, Q.; Chen, J.; Wang, D.; Li, Y.; Hu, S.; Xu, G. Plant nitrogen nutrition: The roles of arbuscular mycorrhizal fungi. J. Plant Physiol. 2022, 269, 153591. [Google Scholar] [CrossRef] [PubMed]
  34. Moreno Jiménez, E.; Ferrol, N.; Corradi, N.; Peñalosa, J.M.; Rillig, M.C. The potential of arbuscular mycorrhizal fungi to enhance metallic micronutrient uptake and mitigate food contamination in agriculture: Prospects and challenges. New Phytol. 2024, 242, 1441–1447. [Google Scholar] [CrossRef]
  35. Xu, Y.; Lambers, H.; Feng, J.; Tu, Y.; Peng, Z.; Huang, J. The role of arbuscular mycorrhizal fungi in micronutrient homeostasis and cadmium uptake and transfer in rice under different flooding intensities. Ecotoxicol. Environ. Saf. 2024, 284, 116978. [Google Scholar] [CrossRef]
  36. Zhang, J.; Zhao, R.; Li, X.; Zhang, J. Potential of arbuscular mycorrhizal fungi for soil health: A review. Pedosphere 2024, 34, 279–288. [Google Scholar] [CrossRef]
  37. Hu, X.; Chen, D.; Yan, F.; Zheng, X.; Fang, X.; Bai, Y.; Zhao, J.; Ma, X.; Ma, C.; Cai, X.; et al. Global research trends on the effects of arbuscular mycorrhizal fungi on the soil carbon cycle: A bibliometric analysis. Ecol. Indic. 2024, 158, 111543. [Google Scholar] [CrossRef]
  38. He, T.; Lin, W.; Yang, S.; Du, J.; Giri, B.; Feng, C.; Gilliam, F.S.; Zhang, F.; Zhang, X.; Zhang, X. Arbuscular mycorrhizal fungi reduce soil N2O emissions by altering root traits and soil denitrifier community composition. Sci. Total Environ. 2024, 933, 173065. [Google Scholar] [CrossRef]
  39. Shen, Y.; Zhu, B. Arbuscular mycorrhizal fungi reduce soil nitrous oxide emission. Geoderma 2021, 402, 115179. [Google Scholar] [CrossRef]
  40. Zhang, H.; Powell, J.R.; Power, S.A.; Churchill, A.C.; Plett, J.M.; Macdonald, C.A.; Jacob, V.; Kim, G.W.; Pendall, E.; Tissue, D.T.; et al. Arbuscular mycorrhizal fungal-mediated reductions in N2O emissions were not impacted by experimental warming for two common pasture species. Pedobiologia 2021, 87, 150744. [Google Scholar] [CrossRef]
  41. Storer, K.; Coggan, A.; Ineson, P.; Hodge, A. Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol. 2018, 220, 1285–1295. [Google Scholar] [CrossRef] [PubMed]
  42. Tang, B.; Man, J.; Lehmann, A.; Rillig, M.C. Arbuscular mycorrhizal fungi benefit plants in response to major global change factors. Ecol. Lett. 2023, 26, 2087–2097. [Google Scholar] [CrossRef] [PubMed]
  43. Das, D.; Ullah, H.; Himanshu, S.K.; Tisarum, R.; Cha-um, S.; Datta, A. Arbuscular mycorrhizal fungi inoculation and phosphorus application improve growth, physiological traits, and grain yield of rice under alternate wetting and drying irrigation. J. Plant Physiol. 2022, 278, 153829. [Google Scholar] [CrossRef] [PubMed]
  44. Liu, Z.; Bi, S.; Meng, J.; Liu, T.; Li, P.; Yu, C.; Peng, X. Arbuscular mycorrhizal fungi enhanced rice proline metabolism under low temperature with nitric oxide involvement. Front. Plant Sci. 2022, 13, 962460. [Google Scholar] [CrossRef]
  45. Bhantana, P.; Rana, M.S.; Sun, X.-c.; Moussa, M.G.; Saleem, M.H.; Syaifudin, M.; Shah, A.; Poudel, A.; Pun, A.B.; Bhat, M.A.; et al. Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation. Symbiosis 2021, 84, 19–37. [Google Scholar] [CrossRef]
  46. Tan, Q.; Guo, Q.; Wei, R.; Zhu, G.; Du, C.; Hu, H. Influence of arbuscular mycorrhizal fungi on bioaccumulation and bioavailability of As and Cd: A meta-analysis. Environ. Pollut. 2023, 316, e120619. [Google Scholar] [CrossRef]
  47. Riaz, M.; Kamran, M.; Fang, Y.; Wang, Q.; Cao, H.; Yang, G.; Deng, L.; Wang, Y.; Zhou, Y.; Anastopoulos, I.; et al. Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. J. Hazard. Mater. 2021, 402, 123919. [Google Scholar] [CrossRef]
  48. Souza, T.; Barros, I.C.; da Silva, L.J.R.; Laurindo, L.K.; dos Santos Nascimento, G.; de Lucena, E.O.; Martins, M.; dos Santos, V.B. Soil microbiota community assembling in native plant species from Brazil’s legal Amazon. Symbiosis 2022, 86, 93–109. [Google Scholar] [CrossRef]
  49. Dar, M.H.; Razvi, S.M.; Singh, N.; Mushtaq, A.; Dar, S.; Hussain, S. Arbuscular mycorrhizal fungi for salinity stress: Anti-stress role and mechanisms. Pedosphere 2023, 33, 212–224. [Google Scholar] [CrossRef]
  50. Chen, H.; Zhang, X.; Wang, H.; Xing, S.; Yin, R.; Fu, W.; Rillig, M.C.; Chen, B.; Zhu, Y. Arbuscular mycorrhizal fungi can inhibit the allocation of microplastics from crop roots to aboveground edible parts. J. Agric. Food Chem. 2023, 71, 18323–18332. [Google Scholar] [CrossRef]
  51. Lehmann, A.; Leifheit, E.F.; Feng, L.; Bergmann, J.; Wulf, A.; Rillig, M.C. Microplastic fiber and drought effects on plants and soil are only slightly modified by arbuscular mycorrhizal fungi. Soil Ecol. Lett. 2022, 4, 32–44. [Google Scholar] [CrossRef]
  52. Zhang, S.; Lehmann, A.; Zheng, W.; You, Z.; Rillig, M.C. Arbuscular mycorrhizal fungi increase grain yields: A meta-analysis. New Phytol. 2019, 222, 543–555. [Google Scholar] [CrossRef] [PubMed]
  53. Campos, C.; Coito, J.L.; Cardoso, H.; da Silva, J.M.; Pereira, H.S.; Viegas, W.; Nogales, A. Dynamic Regulation of Grapevine’s microRNAs in Response to Mycorrhizal Symbiosis and High Temperature. Plants 2023, 12, e982. [Google Scholar] [CrossRef] [PubMed]
  54. Jumrani, K.; Bhatia, V.S.; Kataria, S.; Alamri, S.A.; Siddiqui, M.H.; Rastogi, A. Inoculation with Arbuscular Mycorrhizal Fungi Alleviates the Adverse Effects of High Temperature in Soybean. Plants 2022, 11, 2210. [Google Scholar] [CrossRef]
  55. Mathur, S.; Sharma, M.P.; Jajoo, A. Improved photosynthetic efficacy of maize (Zea mays) plants with arbuscular mycorrhizal fungi (AMF) under high temperature stress. J. Photochem. Photobiol. B Biol. 2018, 180, 149–154. [Google Scholar] [CrossRef]
  56. Mathura, S.; Jajoo, A. Arbuscular mycorrhizal fungi protects maize plants from high temperature stress by regulating photosystem II heterogeneity. Ind Crops Prod 2020, 143, 11934. [Google Scholar] [CrossRef]
  57. Zhu, X.-C.; Song, F.-B.; Liu, S.-Q.; Liu, T.-D. Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 2011, 346, 189–199. [Google Scholar] [CrossRef]
  58. Li, W.; Wu, H.; Hua, J.; Zhu, C.; Guo, S. Arbuscular mycorrhizal fungi enhanced resistance to low-temperature weak-light stress in snapdragon (Antirrhinum majus L.) through physiological and transcriptomic responses. Front Plant Sci. 2024, 15, 1330032. [Google Scholar] [CrossRef]
  59. Liu, Y.; Lu, J.; Cui, L.; Tang, Z.; Ci, D.; Zou, X.; Zhang, X.; Yu, X.; Wang, Y.; Si, T. The multifaceted roles of arbuscular mycorrhizal fungi in peanut responses to salt, drought, and cold stress. BMC Plant Biol. 2023, 23, 36. [Google Scholar] [CrossRef]
  60. Zhang, H.; Qi, H.; Lu, G.; Zhou, X.; Wang, J.; Li, J.; Zheng, K.; Fan, Y.; Zhou, H.; Wang, J.; et al. Non-targeted metabolomics analysis reveals the mechanism of arbuscular mycorrhizal symbiosis regulating the cold-resistance of Elymus nutans. Front. Microbiol. 2023, 14, 1134585. [Google Scholar] [CrossRef]
  61. Hajiboland, R.; Joudmand, A.; Aliasgharzad, N.; Tolrà, R.; Poschenrieder, C. Arbuscular mycorrhizal fungi alleviate low-temperature stress and increase freezing resistance as a substitute for acclimation treatment in barley. Crop Pasture Sci. 2019, 70, 218–233. [Google Scholar] [CrossRef]
  62. Zhu, X.C.; Song, F.B.; Xu, H.W. Effects of arbuscular mycorrhizal fungi on photosynthetic characteristics of maize under low temperature stress. Yingyong Shengtai Xuebao 2010, 21, 470–475. [Google Scholar] [PubMed]
  63. Xu, J.; Liu, S.; Song, S.; Guo, H.; Tang, J.; Yong, J.W.H.; Ma, Y.; Chen, X. Arbuscular mycorrhizal fungi influence decomposition and the associated soil microbial community under different soil phosphorus availability. Soil Biol. Biochem. 2018, 120, 181–190. [Google Scholar] [CrossRef]
  64. Liu, S.; Lu, X.; Yang, G.; He, C.; Shi, Y.; Li, C.; Liu, S.; Wang, Y.; Wang, Z.; Chen, L.; et al. Variation of arbuscular mycorrhizal fungi communities in the rhizosphere soil of Eucalyptus plantations based on different stand ages and its effect on phosphorus fractionation. Appl. Soil Ecol. 2023, 189, 104908. [Google Scholar] [CrossRef]
  65. Qin, Z.; Peng, Y.; Yang, G.; Feng, G.; Christie, P.; Zhou, J.; Zhang, J.; Li, X.; Gai, J. Relationship between phosphorus uptake via indigenous arbuscular mycorrhizal fungi and crop response: A 32P-labeling study. Appl. Soil Ecol. 2022, 180, 104624. [Google Scholar] [CrossRef]
  66. Porcel, R.; Aroca, R.; Ruiz-Lozano, J.M. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev. 2012, 32, 181–200. [Google Scholar] [CrossRef]
  67. Li, J.; Zhou, L.; Chen, G.; Yao, M.; Liu, Z.; Li, X.; Yang, X.; Yang, Y.; Cai, D.; Tuerxun, Z.; et al. Arbuscular mycorrhizal fungi enhance drought resistance and alter microbial communities in maize rhizosphere soil. Environ. Technol. Innov 2025, 37, 103947. [Google Scholar] [CrossRef]
  68. Sun, R.-T.; Zhang, Z.-Z.; Zhou, N.; Srivastava, A.K.; KuCa, K.; Abd-allah, E.F.; Hashem, A.; Wu, Q.-S. A review of the interaction of medicinal plants and arbuscular mycorrhizal fungi in the rhizosphere. Not. Bot. Horti Agrobot. Cluj-Napoca 2021, 49, e12454. [Google Scholar] [CrossRef]
  69. Zhang, W.; Wang, C.; Lu, T.; Zheng, Y. Cooperation between arbuscular mycorrhizal fungi and earthworms promotes the physiological adaptation of maize under a high salt stress. Plant Soil 2018, 423, 125–140. [Google Scholar] [CrossRef]
  70. Sun, W.; Shahrajabian, M.H. The application of arbuscular mycorrhizal fungi as microbial biostimulant, sustainable approaches in modern agriculture. Plants 2023, 12, e3101. [Google Scholar] [CrossRef]
  71. Khaliq, A.; Perveen, S.; Alamer, K.H.; Zia Ul Haq, M.; Rafique, Z.; Alsudays, I.M.; Althobaiti, A.T.; Saleh, M.A.; Hussain, S.; Attia, H. Arbuscular mycorrhizal fungi symbiosis to enhance plant-soil interaction. Sustainability 2022, 14, e7840. [Google Scholar] [CrossRef]
  72. Etesami, H.; Li, Z.; Maathuis, F.J.M.; Cooke, J. The combined use of silicon and arbuscular mycorrhizas to mitigate salinity and drought stress in rice. Environ. Exp. Bot. 2022, 201, e104955. [Google Scholar] [CrossRef]
  73. Fileccia, V.; Ruisi, P.; Ingraffia, R.; Giambalvo, D.; Frenda, A.S.; Martinelli, F. Arbuscular mycorrhizal symbiosis mitigates the negative effects of salinity on durum wheat. PLoS ONE 2017, 12, e0184158. [Google Scholar] [CrossRef]
  74. Yin, R.; Hao, Z.; Yuan, X.; Wang, M.; Li, S.; Zhang, X.; Chen, B. Arbuscular mycorrhizal symbiosis alleviates ozone injury in ozone-tolerant poplar clone but not in ozone-sensitive poplar clone. Sci. Total Environ. 2023, 894, e165023. [Google Scholar] [CrossRef]
  75. Yin, R.; Hao, Z.; Zhou, X.; Wu, H.; Feng, Z.; Yuan, X.; Chen, B. Ozone does not diminish the beneficial effects of arbuscular mycorrhizas on Medicago sativa L. in a low phosphorus soil. Mycorrhiza 2022, 32, 33–43. [Google Scholar] [CrossRef]
  76. Sun, S.; Feng, Y.; Huang, G.; Zhao, X.; Song, F. Rhizophagus irregularis enhances tolerance to cadmium stress by altering host plant hemp Cannabis sativa L. photosynthetic properties. Environ. Pollut. 2022, 314, e120309. [Google Scholar] [CrossRef]
  77. Li, W.; Zhai, Y.-L.; Xing, H.-S.; Xing, L.-J.; Guo, S.-X. Arbuscular mycorrhizal fungi promote photosynthesis in Antirrhinum majus L. under low-temperature and weak-light conditions. Not. Bot. Horti Agrobot. Cluj-Napoca 2023, 51, 13012. [Google Scholar] [CrossRef]
  78. Miller, R.M.; Jastrow, J.D. Mycorrhizal Fungi Influence Soil Structure. In Arbuscular Mycorrhizas: Physiology and Function; Kapulnik, Y., Douds, D.D., Eds.; Springer Netherlands: Dordrecht, The Netherlands, 2000; pp. 3–18. [Google Scholar]
  79. Leifheit, E.F.; Lehmann, A.; Rillig, M.C. Potential effects of microplastic on arbuscular mycorrhizal fungi. Front. Plant Sci. 2021, 12, e626709. [Google Scholar] [CrossRef]
  80. Rillig, M.C.; Mummey, D.L. Mycorrhizas and soil structure. New Phytol. 2006, 171, 41–53. [Google Scholar] [CrossRef]
  81. Lehmann, A.; Leifheit, E.F.; Rillig, M.C. Chapter 14—Mycorrhizas and Soil Aggregation. In Mycorrhizal Mediation of Soil; Johnson, N.C., Gehring, C., Jansa, J., Eds.; Elsevier: Amsterdam, The Netherlands, 2017; pp. 241–262. [Google Scholar]
  82. Gehring, C.A. Chapter 13—Introduction: Mycorrhizas and Soil Structure, Moisture, and Salinity. In Mycorrhizal Mediation of Soil; Johnson, N.C., Gehring, C., Jansa, J., Eds.; Elsevier: Amsterdam, The Netherlands, 2017; pp. 235–240. [Google Scholar]
  83. Singh, G.; Pankaj, U. Arbuscular Mycorrhizal Fungi-Assisted Phytoextraction of Toxic Metals by Zea mays L. From Tannery Sludge. Soil Sediment Contam. Int. J. 2019, 28, 729–746. [Google Scholar] [CrossRef]
  84. Chen, B.D.; Zhu, Y.G.; Duan, J.; Xiao, X.Y.; Smith, S.E. Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ. Pollut. 2007, 147, 374–380. [Google Scholar] [CrossRef] [PubMed]
  85. Janoušková, M.; Pavlíková, D.; Vosátka, M. Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil. Chemosphere 2006, 65, 1959–1965. [Google Scholar] [CrossRef] [PubMed]
  86. Chen, X.-H.; Zhao, B. Arbuscular mycorrhizal fungi mediated uptake of lanthanum in Chinese milk vetch (Astragalus sinicus L.). Chemosphere 2007, 68, 1548–1555. [Google Scholar] [CrossRef]
  87. Sudová, R.; Vosátka, M. Differences in the effects of three arbuscular mycorrhizal fungal strains on P and Pb accumulation by maize plants. Plant Soil 2007, 296, 77–83. [Google Scholar] [CrossRef]
  88. Radka, S.; Pavla, D.; Miroslav, V. Mycorrhizal association of Agrostis capillaris and Glomus intraradices under heavy metal stress: Combination of plant clones and fungal isolates from contaminated and uncontaminated substrates. Appl. Soil Ecol. 2008, 40, 19–29. [Google Scholar] [CrossRef]
  89. Azcón, R.; Perálvarez, M.d.C.; Biró, B.; Roldán, A.; Ruíz-Lozano, J.M. Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multicontaminated soil amended with treated lignocellulosic agrowaste. Appl. Soil Ecol. 2009, 41, 168–177. [Google Scholar] [CrossRef]
  90. Xu, Z.; Wu, Y.; Xiao, Z.; Ban, Y.; Belvett, N. Positive effects of Funneliformis mosseae inoculation on reed seedlings under water and TiO2 nanoparticles stresses. World J. Microbiol. Biotechnol. 2019, 35, 81. [Google Scholar] [CrossRef]
  91. Zhang, X.; Zhang, H.; Lou, X.; Tang, M. Mycorrhizal and non-mycorrhizal Medicago truncatula roots exhibit differentially regulated NADPH oxidase and antioxidant response under Pb stress. Environ. Exp. Bot. 2019, 164, 10–19. [Google Scholar] [CrossRef]
  92. Zhan, F.; Li, B.; Jiang, M.; Li, T.; He, Y.; Li, Y.; Wang, Y. Effects of arbuscular mycorrhizal fungi on the growth and heavy metal accumulation of bermudagrass [Cynodon dactylon (L.) Pers.] grown in a lead-zinc mine wasteland. Int. J. Phytoremed. 2019, 21, 849–856. [Google Scholar] [CrossRef]
  93. Guangjuan, C.; Shaoying, A.; Kang, C.; Xiurong, W. Arbuscular mycorrhiza augments cadmium tolerance in soybean by altering accumulation and partitioning of nutrient elements, and related gene expression. Ecotoxicol. Environ. Saf. 2019, 171, 231–239. [Google Scholar] [CrossRef]
  94. Abdelhameed, R.E.; Metwally, R.A. Alleviation of cadmium stress by arbuscular mycorrhizal symbiosis. Int. J. Phytoremed. 2019, 21, 663–671. [Google Scholar] [CrossRef]
  95. Ould Amer, S.; Aliat, T.; Kucher, D.E.; Bensaci, O.A.; Rebouh, N.Y. Investigating the Potential of Arbuscular Mycorrhizal Fungi in Mitigating Water Deficit Effects on Durum Wheat (Triticum durum Desf.). Agriculture 2023, 13, 552. [Google Scholar] [CrossRef]
  96. Yooyongwech, S.; Tisarum, R.; Samphumphuang, T.; Phisalaphong, M.; Cha-um, S. Integrated strength of osmotic potential and phosphorus to achieve grain yield of rice under water deficit by arbuscular mycorrhiza fungi. Sci. Rep. 2023, 13, 5999. [Google Scholar] [CrossRef]
  97. Madouh, T.A.; Quoreshi, A.M. The Function of Arbuscular Mycorrhizal Fungi Associated with Drought Stress Resistance in Native Plants of Arid Desert Ecosystems: A Review. Diversity 2023, 15, 391. [Google Scholar] [CrossRef]
  98. Fu, W.; Chen, B.; Jansa, J.; Wu, H.; Ma, W.; Luo, W.; Xu, C.; Hao, Z.; Wu, H.; Yu, Q.; et al. Contrasting community responses of root and soil dwelling fungi to extreme drought in a temperate grassland. Soil Biol. Biochem. 2022, 169, 108670. [Google Scholar] [CrossRef]
  99. Battini, F.; Gronlund, M.; Agnolucci, M.; Giovannetti, M.; Jakobsen, I. Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Sci. Rep. 2017, 7, 4686. [Google Scholar] [CrossRef]
  100. Al-Arjani, A.-B.F.; Hashem, A.; Abd_Allah, E.F. Arbuscular mycorrhizal fungi modulates dynamics tolerance expression to mitigate drought stress in Ephedra foliata Boiss. Saudi J. Biol. Sci. 2020, 27, 380–394. [Google Scholar] [CrossRef]
  101. Gao, X.; Guo, H.; Zhang, Q.; Guo, H.; Zhang, L.; Zhang, C.; Gou, Z.; Liu, Y.; Wei, J.; Chen, A.; et al. Arbuscular mycorrhizal fungi (AMF) enhanced the growth, yield, fiber quality and phosphorus regulation in upland cotton (Gossypium hirsutum L.). Sci. Rep. 2020, 10, 2084. [Google Scholar] [CrossRef]
  102. Jansa, J.; Smith, F.A.; Smith, S.E. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol. 2008, 177, 779–789. [Google Scholar] [CrossRef]
  103. Jajoo, A.; Mathur, S. Role of arbuscular mycorrhizal fungi as an underground saviuor for protecting plants from abiotic stresses. Physiol. Mol. Biol. Plants 2021, 27, 2589–2603. [Google Scholar] [CrossRef]
  104. De La Providencia, I.E.; De Souza, F.A.; Fernández, F.; Delmas, N.S.; Declerck, S. Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenic groups. New Phytol. 2005, 165, 261–271. [Google Scholar] [CrossRef]
  105. Giovannetti, M.; Avio, L.; Sbrana, C. Functional significance of anastomosis in arbuscular mycorrhizal networks. In Mycorrhizal Networks; Horton, T.R., Ed.; Springer: Dordrecht, The Netherlands, 2015; pp. 41–67. [Google Scholar]
  106. Liu, M.; Wang, H.; Lin, Z.; Ke, J.; Zhang, P.; Zhang, F.; Ru, D.; Zhang, L.; Xiao, Y.; Liu, X. Arbuscular mycorrhizal fungi inhibit necrotrophic, but not biotrophic, aboveground plant pathogens: A meta-analysis and experimental study. New Phytol. 2024, 241, 1308–1320. [Google Scholar] [CrossRef]
  107. Duan, S.; Feng, G.; Limpens, E.; Bonfante, P.; Xie, X.; Zhang, L. Cross-kingdom nutrient exchange in the plant–arbuscular mycorrhizal fungus–bacterium continuum. Nat. Rev. Microbiol. 2024, 22, 773–790. [Google Scholar] [CrossRef]
  108. Hestrin, R.; Hammer, E.C.; Mueller, C.W.; Lehmann, J. Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun. Biol. 2019, 2, 233. [Google Scholar] [CrossRef]
  109. Rozmoš, M.; Bukovská, P.; Hršelová, H.; Kotianová, M.; Dudáš, M.; Gančarčíková, K.; Jansa, J. Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by specific soil bacteria and a protist. ISME J. 2022, 16, 676–685. [Google Scholar] [CrossRef]
  110. Faghihinia, M.; Jansa, J.; Halverson, L.J.; Staddon, P.L. Hyphosphere microbiome of arbuscular mycorrhizal fungi: A realm of unknowns. Biol. Fertil. Soils 2023, 59, 17–34. [Google Scholar] [CrossRef]
  111. Seleiman, M.F.; Al-Suhaibani, N.; Ali, N.; Akmal, M.; Alotaibi, M.; Refay, Y.; Dindaroglu, T.; Abdul-Wajid, H.H.; Battaglia, M.L. Drought stress impacts on plants and sifferent approaches to alleviate its adverse effects. Plants 2021, 10, 10020259. [Google Scholar] [CrossRef]
  112. Al-Yasi, H.; Attia, H.; Alamer, K.; Hassan, F.; Ali, E.; Elshazly, S.; Siddique, K.H.M.; Hessini, K. Impact of drought on growth, photosynthesis, osmotic adjustment, and cell wall elasticity in Damask rose. Plant Physiol. Biochem. 2020, 150, 133–139. [Google Scholar] [CrossRef]
  113. Kuromori, T.; Fujita, M.; Takahashi, F.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Inter-tissue and inter-organ signaling in drought stress response and phenotyping of drought tolerance. Plant J. 2022, 109, 342–358. [Google Scholar] [CrossRef]
  114. Soualiou, S.; Duan, F.; Li, X.; Zhou, W. Crop production under stress: An understanding of plant responses, acclimation processes, and management strategies. Plant Physiol. Biochem. 2022, 190, 47–61. [Google Scholar] [CrossRef]
  115. Mahajan, S.; Tuteja, N. Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys. 2005, 444, 139–158. [Google Scholar] [CrossRef]
  116. Pantha, S.; Kilian, B.; Özkan, H.; Zeibig, F.; Frei, M. Physiological and biochemical changes induced by drought stress during the stem elongation and anthesis stages in the Triticum genus. Environ. Exp. Bot. 2024, 228, 106047. [Google Scholar] [CrossRef]
  117. Tominaga, J.; Shimada, H.; Kawamitsu, Y. Direct measurement of intercellular CO2 concentration in a gas-exchange system resolves overestimation using the standard method. J. Exp. Bot. 2018, 69, 1981–1991. [Google Scholar] [CrossRef]
  118. Cramer, P. Organization and regulation of gene transcription. Nature 2019, 573, 45–54. [Google Scholar] [CrossRef]
  119. Wang, W.; Shi, J.; Xie, Q.; Jiang, Y.; Yu, N.; Wang, E. Nutrient Exchange and Regulation in Arbuscular Mycorrhizal Symbiosis. Mol. Plant 2017, 10, 1147–1158. [Google Scholar] [CrossRef]
  120. Saxena, B.; Sharma, K.; Kapoor, R.; Wu, Q.S.; Giri, B. Insights into the molecular aspects of salt stress tolerance in mycorrhizal plants. World J. Microbiol. Biotechnol. 2022, 38, 253. [Google Scholar] [CrossRef]
  121. Tao, J.; Dong, F.; Wang, Y.; Chen, H.; Tang, M. Arbuscular mycorrhizal fungi enhance photosynthesis and drought tolerance by regulating MAPK genes expressions. Physiol. Plant. 2022, 174, e13829. [Google Scholar] [CrossRef]
  122. Begum, N.; Xiao, Y.; Wang, L.; Li, D.; Irshad, A.; Zhao, T. Arbuscular mycorrhizal fungus Rhizophagus irregularis alleviates drought stress in soybean with overexpressing the GmSPL9d gene by promoting photosynthetic apparatus and regulating the antioxidant system. Microbiol. Res. 2023, 273, 127398. [Google Scholar] [CrossRef]
  123. Zayova, E.; Stancheva, I.; Geneva, M.; Hristozkova, M.; Dimitrova, L.; Petrova, M.; Sichanova, M.; Salamon, I.; Mudroncekova, S. Arbuscular mycorrhizal fungi enhance antioxidant capacity of in vitro propagated garden thyme (Thymus vulgaris L.). Symbiosis 2018, 74, 177–187. [Google Scholar] [CrossRef]
  124. Wang, Y.; Branicky, R.; Noë, A.; Hekimi, S. Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling. J. Cell Biol. 2018, 217, 1915–1928. [Google Scholar] [CrossRef]
  125. Xu, F.-Q.; Meng, L.-L.; Kuča, K.; Wu, Q.-S. The mechanism of arbuscular mycorrhizal fungi-alleviated manganese toxicity in plants: A review. Plant Physiol. Biochem. 2024, 213, 108808. [Google Scholar] [CrossRef] [PubMed]
  126. Dong, F.; Wang, Y.; Tao, J.; Xu, T.; Tang, M. Arbuscular mycorrhizal fungi affect the expression of PxNHX gene family, improve photosynthesis and promote Populus simonii×P. nigra growth under saline-alkali stress. Front. Plant Sci. 2023, 14, 1104095. [Google Scholar] [CrossRef] [PubMed]
  127. Li, C.; Shi, L.; Chen, D.; Ren, A.; Gao, T.; Zhao, M. Functional analysis of the role of glutathione peroxidase (GPx) in the ROS signaling pathway, hyphal branching and the regulation of ganoderic acid biosynthesis in Ganoderma lucidum. Fungal Genet. Biol. 2015, 82, 168–180. [Google Scholar] [CrossRef] [PubMed]
  128. Gullner, G.; Komives, T.; Király, L.; Schröder, P. Glutathione S-Transferase Enzymes in Plant-Pathogen Interactions. Front. Plant Sci. 2018, 9, 1836. [Google Scholar] [CrossRef]
  129. Qausain, S.; Basheeruddin, M. Unraveling the Peroxidase Activity in Peroxiredoxins: A Comprehensive Review of Mechanisms, Functions, and Biological Significance. Cureus 2024, 16, e66117. [Google Scholar] [CrossRef]
  130. Kumari, P.; Gupta, A.; Yadav, S. Thioredoxins as Molecular Players in Plants, Pests, and Pathogens. In Plant-Pest Interactions: From Molecular Mechanisms to Chemical Ecology: Chemical Ecology; Singh, I.K., Singh, A., Eds.; Springer: Singapore, 2021; pp. 107–125. [Google Scholar]
  131. Chandrasekaran, M.; Paramasivan, M. Arbuscular mycorrhizal fungi and antioxidant enzymes in ameliorating drought stress: A meta-analysis. Plant Soil 2022, 480, 295–303. [Google Scholar] [CrossRef]
  132. Marín, R.; Abad, C.; Rojas, D.; Chiarello, D.I.; Alejandro, T.-G. Chapter Four—Biomarkers of oxidative stress and reproductive complications. In Advances in Clinical Chemistry; Makowski, G.S., Ed.; Elsevier: Amsterdam, The Netherlands, 2023; Volume 113, pp. 157–233. [Google Scholar]
  133. Liu, R.; Yang, L.; Zou, Y.; Wu, Q. Root-associated endophytic fungi modulate endogenous auxin and cytokinin levels to improve plant biomass and root morphology of trifoliate orange. Hortic. Plant J. 2023, 9, 463–472. [Google Scholar] [CrossRef]
  134. Lou, X.; Zhang, X.; Zhang, Y.; Tang, M. The synergy of arbuscular mycorrhizal fungi and exogenous abscisic acid benefits Robinia pseudoacacia L. growth through altering the distribution of Zn and endogenous abscisic acid. J. Fungi 2021, 7, e34436210. [Google Scholar] [CrossRef]
  135. Herrera-Medina, M.J.; Steinkellner, S.; Vierheilig, H.; Ocampo Bote, J.A.; García Garrido, J.M. Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol. 2007, 175, 554–564. [Google Scholar] [CrossRef]
  136. Tominaga, T.; Miura, C.; Takeda, N.; Kanno, Y.; Takemura, Y.; Seo, M.; Yamato, M.; Kaminaka, H. Gibberellin Promotes Fungal Entry and Colonization during Paris-Type Arbuscular Mycorrhizal Symbiosis in Eustoma grandiflorum. Plant Cell Physiol. 2019, 61, 565–575. [Google Scholar] [CrossRef]
Agriculture 14 02361 g001
Figure 1. Arbuscular mycorrhizal fungi colonize root cortical cells through germinating spores, forming hyphal branches, and developing an extraradical mycelium that forms an extensive network in the soil. The initial colonization involves hyphal contact on root surfaces through the outer cortex, the formation of a dense hyphal sheath surrounding the colonized surface (ectomycorrhizas), or the penetration of fungal hyphae into host tissues (endomycorrhizas), establishing the mutual-benefit symbiosis.
Figure 1. Arbuscular mycorrhizal fungi colonize root cortical cells through germinating spores, forming hyphal branches, and developing an extraradical mycelium that forms an extensive network in the soil. The initial colonization involves hyphal contact on root surfaces through the outer cortex, the formation of a dense hyphal sheath surrounding the colonized surface (ectomycorrhizas), or the penetration of fungal hyphae into host tissues (endomycorrhizas), establishing the mutual-benefit symbiosis.
Agriculture 14 02361 g001
Agriculture 14 02361 g002
Figure 2. Arbuscular mycorrhizal fungi colonize roots to form a mutually beneficial symbiosis that induces upward nutrient flow and downward carbon flow in the plant–soil–rhizosphere continuum. AM fungi require C sources from host plants for spore propagation and extraradical hyphal development. In contrast, AM fungi produce a network of extraradical mycelium, spreading from host roots into the surrounding soil and establishing belowground interconnections to supply plant-required nutrients like P, N, Zn, Cu, and Mg. These functioning features occur in the hyphosphere with hyphal exudates and other enzymes involved in the nutrient flow process. While the plant–AM fungi symbiotic relationship is a nutrient trade-off, the mutually beneficial association can enhance plant ability to acquire essential minerals, which is crucial for enhancing soil health through the contribution of hyphosphere microbiomes to nutrient cycling, carbon sequestration, and soil aggregation.
Figure 2. Arbuscular mycorrhizal fungi colonize roots to form a mutually beneficial symbiosis that induces upward nutrient flow and downward carbon flow in the plant–soil–rhizosphere continuum. AM fungi require C sources from host plants for spore propagation and extraradical hyphal development. In contrast, AM fungi produce a network of extraradical mycelium, spreading from host roots into the surrounding soil and establishing belowground interconnections to supply plant-required nutrients like P, N, Zn, Cu, and Mg. These functioning features occur in the hyphosphere with hyphal exudates and other enzymes involved in the nutrient flow process. While the plant–AM fungi symbiotic relationship is a nutrient trade-off, the mutually beneficial association can enhance plant ability to acquire essential minerals, which is crucial for enhancing soil health through the contribution of hyphosphere microbiomes to nutrient cycling, carbon sequestration, and soil aggregation.
Agriculture 14 02361 g002
Agriculture 14 02361 g003
Figure 3. Physiological mechanisms of osmotic adjustment at the (a) cellular, (b) whole plant, and (c) system scale in a typical dryland agroecosystem. It is typical that a water–carbon linear correlation occurs in plant scale, whereas at the ecosystem scale water–carbon correlation becomes nonlinear. Abbreviations: intercellular CO2 concentration (ci), ambient stomatal CO2 concentration (ca), conductance (gs), seasonal air temperature (Ta), relative humidity (Rh), vapor pressure deficit (VPD), soil water content (SWC), leaf area index (LAI), water use efficiency (WUE), and seasonal total evapotranspiration (ET), transpiration (T), soil evaporation (E), net ecosystem exchange (NEE), and gross primary productivity (GPP).
Figure 3. Physiological mechanisms of osmotic adjustment at the (a) cellular, (b) whole plant, and (c) system scale in a typical dryland agroecosystem. It is typical that a water–carbon linear correlation occurs in plant scale, whereas at the ecosystem scale water–carbon correlation becomes nonlinear. Abbreviations: intercellular CO2 concentration (ci), ambient stomatal CO2 concentration (ca), conductance (gs), seasonal air temperature (Ta), relative humidity (Rh), vapor pressure deficit (VPD), soil water content (SWC), leaf area index (LAI), water use efficiency (WUE), and seasonal total evapotranspiration (ET), transpiration (T), soil evaporation (E), net ecosystem exchange (NEE), and gross primary productivity (GPP).
Agriculture 14 02361 g003
Agriculture 14 02361 g004
Figure 4. Arbuscular mycorrhizal fungi enhance plant resistance to abiotic stress, which is through increasing photosynthesis, improving root-to-stem ratio, increasing nutrient uptake, increasing root surface areas, promoting metabolisms, balancing hormones, stimulating enzyme activities, and interacting with other microbiomes in the hyphosphere.
Figure 4. Arbuscular mycorrhizal fungi enhance plant resistance to abiotic stress, which is through increasing photosynthesis, improving root-to-stem ratio, increasing nutrient uptake, increasing root surface areas, promoting metabolisms, balancing hormones, stimulating enzyme activities, and interacting with other microbiomes in the hyphosphere.
Agriculture 14 02361 g004
Table 1. Examples of the AMF functioning in alleviating various abiotic stresses in agroecosystems.
Table 1. Examples of the AMF functioning in alleviating various abiotic stresses in agroecosystems.
StressImpacts of Abiotic Stress AM Fungi-Induced Functional EffectsAM Fungal SpeciesHost Plant SpeciesRefer.
Extreme high temp.Excessive heat amplifies existing conditions and results in premature deathPromoting miRNAs isomiRs expression in mycorrhizal plants via upregulating homeobox-leucine zipper proteins and auxin receptors Rhizophagus intraradices; Funneliformis mosseae; Funneliformis geosporumZea mays; Acacia pachyceras; Pennisetum divisum; Glycine max[53,54,55,56,57]
Cold stressCausing cell membrane to rupture and lead to cell deathEnhancing stomatal conductance, maximal photochemical efficiency, promoting activities of antioxidant enzymes, and K+: Na+ ratio while lowering leaf relative electrolyte conductivityRhizophagus irregularis; Rhizophagus clarus;Rhizophagus intraradices;Glomus lamellose; Funneliformis mosseaeArachis hypogaea L.; Hordeum vulgare [58,59,60,61,62]
Low-P soil environmentAffecting the expected life of an organismIt helps acquire P and other nutrients from organic matter decomposition, alters bacterial and fungal communities, and enhances soil microbial diversity.Funneliformiscaledonium; Funneliformisgeosporum; Gigaspora margaritaZea mays L.; Triticum aestivum L.[63,64,65]
High salinityAffecting reactive oxygen species, damaging biomolecules Helping hormone balance, stomatal conductance, and osmotic adjustment via chlorophyll biosynthesis; Improving Mg2+ concentration; enhancing antioxidant enzyme activity Rhizophagus irregularis; Funneliformis message;Arachis hypogaea L.; Oryza sativa L.; Cucumis sativus[49,66,67,68,69,70,71,72,73]
Enriched ozone (O3)Entering plant cells, upsetting the antioxidant defense system, reducing photosynthesisMediating antioxidant enzyme (superoxide dismutase and peroxidase) activity and reducing the plant O3 sensitivity, thus minimizing species-dependent O3 injury in plants.Rhizophagus irregularis; Septoglomus viscosum; Claroideoglomushanlinii, Claroideoglomus claroideumMedicago sativa L.; Populus spp.[74,75]
Weak light Weak light affects the growth and flower quality of horticultural plantsEnhancing net photosynthetic rate, stomatal conductance, and chlorophyll content, the potential activity of photosystem II; reduced the intercellular CO2 concentration Rhizophagus irregularis; Funneliformis mosseae; Glomus versiformeCannabis sativa L.; Antirrhinum majus L.[58,76,77]
Poor soil structureLow infiltration, poor nutrient provision, poor formation of aggregates Hyphal decomposition provides nucleation sites for micro aggregate coating C; absorptive mycelium provides the ’backbone’ of a stabilizing network on aggregates affecting hydrophobicityRhizophagus irregularis; Septoglomus viscosum; Claroideoglomushanlinii; R. fasciculatusA variety of crops[67,78,79,80,81,82]
Heavy metal (Cu, Cd, Cr, Pb, Zn, Mo, Mn, Al, As, Ni, Ar, Cr, Pb, Zn) pollutionPollution in water bodies, soils, and food products affecting human healthAlleviating heavy metals in host plant; improving nutrient uptake and antioxidants in host plant; remediating heavy metal by accumulating large part of heavy metals in fungal structuresRhizophagus irregularis; Funneliformis mosseae; Glomus versiforme; Glomus deserticola; GlomusclaroideumBrassica indica; Coreopsis drummondii; Pteris vittate; Eucalyptus globulus; Glycine max; Medicago sativa[83,84,85,86,87,88,89,90,91]
MicroplasticsThreatening soil health: the risk of entering food productsEnhancing antagonistic interactions with soil properties and microbial communities. Helping microplastics biodegradableGlomus lamellosu; Paraglomus occultum;Oryza sativa L.; Zea mays L.; Affium cepa[92]
NutrientdeficiencyReducing plant growth, lowering yieldsIncreasing N, K, Ca, and P uptake; increasing antioxidant activity (CAT, SOD, etc.); improving soil moistureGlomus intraradicesZea mays[93]
Water loggingDamaging root systemsUpregulating aquaporins, increasing entry points of fungi to increase nutrient uptake, maintaining ion and cellular homeostasisFunneliformismosseaePrunus persica[94]
Water deficitInfluencing plant–microbiome interaction, hormone balance, stomatal conductance, and osmotic adjustmentIncreased height of aerial part, length of internodes, length of ear, plant dry weight, and chlorophyll content; increased phosphorus content and osmotic potential in plantsFunneliformis mosseae; Rhizophagus intraradices; Funneliformis geosporus; Claroideoglomus etunicatum; Glomus aggregatumTriticum durumO. sativa[95,96]
Prolonged droughtThreatening plant growth and development, thus the socio-economic and ecological environmentIncreasing AMF richness, strengthening plant–microbiome interaction, improving hormone balance, stomatal conductance, osmotic adjustment, and photosynthetic activityRhizophagus intraradices; Glomus proliferum; Glomus etunicatum; Glomus diaphanum; Glomus constricted; RhizophagusirregularisCeratonia siliqua L.; Triticum durum; Glycine max[55,97,98]
Table 2. Yield responses (95% CI) of different crops inoculated with or without AM fungi under laboratory and field conditions.
Table 2. Yield responses (95% CI) of different crops inoculated with or without AM fungi under laboratory and field conditions.
Type of CropType of Study
Field
(95% CI)		nLab
(95% CI)		nPOverall
(95% CI)		n
All0.127
(0.084, 0.168)		2180.195
(0.132, 0.265) 		1740.050.185
(0.146, 0.230)		402
Barely−0.003
(−0.058, 0.055)		11−0.016
(−0.097, 0.061)		170.81
Maize0.133
(0.042, 0.229) 		820.262
(0.094, 0.432)		140.32
Millet0.162
(0.045, 0.297) 		30.295
(0.116, 0.494)		50.21
Rice0.182
(0.132, 0.242) 		290.312
(0.094, 0.539)		480.34
Wheat0.107
(0.061, 0.155) 		830.166
(0.113, 0.219)		880.11
n denotes the number of studies included in the meta-analysis. P represents the statistical significance between laboratory and field studies for each crop (Data source: Zhang et al. 2019 [52]).
Table 3. Yield responses (95% CI) of maize and wheat inoculated with or without AM fungi under different interventions, including inoculation, crop rotation, and tillage.
Table 3. Yield responses (95% CI) of maize and wheat inoculated with or without AM fungi under different interventions, including inoculation, crop rotation, and tillage.
InterventionType of Crop
AllMaize Wheat
Inoculation
(95% CI)		0.143
(0.113, 0.17) 		0.093
(0.05, 0.13) 		0.160
(0.11, 0.207)
n1454458
Rotation
(95% CI)		0.077
(−0.023, 0.173) 		0.077
(−0.06, 0.203) 		−0.067
(−0.163, 0.03)
n431013
Tillage
(95% CI)		−0.033
(−0.15, 0.08) 		0.003
(−0.123, 0.133) 		0.127
(−0.15, 0.417)
n28242
P0.0010.180.02
Overall (95% CI)0.130 (0.086, 0.176)
n218
n denotes the number of studies included in the meta-analysis. P represents the statistical significance among the three interventions for each crop (Data source: Zhang et al. 2019 [52]).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Sun, D.; Shang, X.; Cao, H.; Lee, S.-J.; Wang, L.; Gan, Y.; Feng, S. Physio-Biochemical Mechanisms of Arbuscular Mycorrhizal Fungi Enhancing Plant Resistance to Abiotic Stress. Agriculture 2024, 14, 2361. https://doi.org/10.3390/agriculture14122361

AMA Style

Sun D, Shang X, Cao H, Lee S-J, Wang L, Gan Y, Feng S. Physio-Biochemical Mechanisms of Arbuscular Mycorrhizal Fungi Enhancing Plant Resistance to Abiotic Stress. Agriculture. 2024; 14(12):2361. https://doi.org/10.3390/agriculture14122361

Chicago/Turabian Style

Sun, Dandi, Xiaoqian Shang, Hanwen Cao, Soon-Jae Lee, Li Wang, Yantai Gan, and Shoujiang Feng. 2024. "Physio-Biochemical Mechanisms of Arbuscular Mycorrhizal Fungi Enhancing Plant Resistance to Abiotic Stress" Agriculture 14, no. 12: 2361. https://doi.org/10.3390/agriculture14122361

APA Style

Sun, D., Shang, X., Cao, H., Lee, S.-J., Wang, L., Gan, Y., & Feng, S. (2024). Physio-Biochemical Mechanisms of Arbuscular Mycorrhizal Fungi Enhancing Plant Resistance to Abiotic Stress. Agriculture, 14(12), 2361. https://doi.org/10.3390/agriculture14122361

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop