Arbuscular Mycorrhizal Fungi (AMF) in Optimizing Nutrient Bioavailability and Reducing Agrochemicals for Maintaining Sustainable Agroecosystems

Abstract

Arbuscular mycorrhizal fungi (AMF) are one of the essential components of the soil microbiome playing a crucial role in nutrients cycling and mediation of plant responses to different environmental stresses. They also play pivotal role in controlling soil erosion, enhancing phytoremediation, and eliminating other harmful microorganisms and then sustaining agroecosystem. Several studies have investigated the positive effects of mycorrhizal symbiosis as biofertilizers those are capable of reducing use of chemical fertilizer by 25–90% particularly NPK depending on crop species, soil type, and management practices, while increasing productivity in the range of 16–78%. Similarly, AMF can also act as bio-controllers and decrease the application rate and frequency of pesticides. This is directly translated to the primary role of AMF in the sustaining agriculture services. Thus, understanding the interaction between AMF-soil, and plant plays a vital role in benefitting societies and agro-industries. In this regard, this review attempted to explore how can AMF symbiosis reduce agro-chemicals and maintain sustainable human welfare. It also addresses impact of agrochemicals on crop production and the main factor influencing the success of AMF symbioses. Generally, if this is applied wisely it keeps the food safe, the soil healthy, the water clean, the climate stable, and the ecosystem flourishing.

1. Introduction

Rapidly growing human population and modern agricultural system resulted in increased demand for agro-chemicals such as pesticides, fertilizers, preservatives, and disinfectant [1, 2] in which their excessive and indiscriminate use severely affects biodiversity, air, water, and soil healthy [1, 3, 4, 5]. They might also exert deleterious effects on human health and exacerbate subsequent socioeconomic effects on communities’ livelihoods by disturbing the ecological balance [2, 3, 5, 6, 7]. Furthermore, climate change, an ever-increasing human population, depletion of global rock phosphorus, and growing energy prices make current fertilizer production unsustainable and represent sizeable challenges to global food security [8]. These disastrous consequences promote new strategies that can reduce and/or substitute agrochemicals in sustainable way without jeopardizing human health and ecosystem services [2, 9].

Considering such alarming situations, beneficial microbial inoculants are proposed as a “clean and ecofriendly” option in agriculture sectors for their potential role in food safety and sustainable crop production [3, 10, 11]. They act as biofertilizers, bioherbicide, biopesticides, and biocontrol agents, which minimize the negative impact of chemical input and consequently increase the quantity and quality of produced food [2]. Among soil microbe, arbuscular mycorrhizal fungi (AMF) symbiosis is one of the most promising that partially or fully supplement agrochemicals and reduce their consecutive negative impacts [12, 13].

AMF promote plant growth by bringing morpho-physiological and biochemical changes in host plants by serving as “biofertilizers and bio-protectors” in sustainable way [14, 15] and providing water and mineral nutrients to the plant [16, 17]. This services can occur through the direct pathway (by roots) and by AMF pathway [13, 18, 19, 20]. Furthermore, it boosts the health of the subsequent crop by improving soil aggregation, providing nutrients, enhancing abiotic stress tolerance, protection against pathogens [9, 12], and altering the accumulation of contaminants in plants and is essential for the sustainable management of agricultural ecosystems and biodiversity [1, 16, 21, 22, 23]. It is the key for production of pesticide-free food crops and ensuring that high yields correspond [23, 24].

In general, it is more effective for improvement of crop yield, growth, and development in areas with low levels of agrochemical inputs (e.g., Africa and South America) [25, 26, 27]. Similarly, low soil fertility optimizes the expression of the multiple beneficial effects of AMF in agro-ecosystem and reduces nutrient seepage to the environment [10, 28]. This relationship is the best scenario and alternate technology for both farmers and society to increase the utilization efficiency of scarce nonrenewable fertilizers such as rock phosphate [18, 29], and use of agrochemicals is catastrophically hampered ecosystem [6, 30]. This is also a strategy to enhance the sustainability of agricultural systems through promoting internal regulatory ecosystem processes while reducing chemical fertilizer use without the concomitant loss of crop yield [26, 31]. However, the application of AMF has not been fully adopted by farmers so far [26]. Therefore, to optimize AMF effects on nutrient bioavailability and ecosystem service to achieving future food security in more sustainable agricultural systems, understanding the linkage of AMF with soil and plant nutrient dynamic plays a vital role for benefitting societies and agro-industries. In this regard, this chapter attempted to summarize published results on contribution of AMF in reducing agrochemical use in agriculture for sustainable maintenance of human welfare and ecological service. It also addresses main factor influencing the success of AMF symbioses and inoculation.

2. Characteristics of arbuscular mycorrhizal fungi (AMF)

Mycorrhizal (fungus-root) fungi are specialized members of the vast population of microorganisms, which are morphologically and physiologically diverse in nature that colonize the rhizosphere [16]. Among mycorrhizal symbiosis, AMF symbiosis is one of the most ancient and widespread than other types of mycorrhizal associations [16, 32]. It is belong to the Phylum Glomeromycota, Glomus spp., which are reproduced asexually and associate with approximately 80% of terrestrial plant species [33], including forest trees, wild grasses, and many crops [16, 34].

AMF is the name given to the endosymbiotic association of a plant root and a fungus from the Glomeromycota, which form two unique structures: a highly branched structure formed inside root cells called arbuscules that is considered to be the key element of the symbiotic nutrient exchanges and a balloon-like structure called vesicles for storage of nutrients within the plant root cortical cells of the host (Figure 1) [35]. AMF are classified into three (Archaeosporomycetes, Glomeromycetes, and Paraglomeromycetes) and the five orders: Archaeosporales (e.g., Geosiphon pyriformes, Archaeospora trappei), Diversisporales (e.g., Scutellospora calospora, Acaulospora laevis, Entrophospora infrequens), Gigasporales (e.g., Gigaspora margarita, G. rosea), Glomerales (e.g., Glomus intraradices, G. mosseae, G. geosporum), and Paraglomerales (e.g., Paraglomus occultum, P. laccatum) [17]. They are obligate biotrophs endophytes [34] that completely depend on a host plant for carbon and energy [32] due to lack of the ability to absorb carbohydrates from other source. This carbon cost is offset by the positive effects of AMF on plant growth and soil quality [10]. There are two types of root colonization in AMF symbiosis [36] (1) Arum-type, in which the symbiont spreads intercellularly between cortical root cells, forming terminal arbuscules on intracellular hyphal branches (2) while in the Paris-type, the fungus grows directly from cell to cell within the cortex and forms intracellular hyphal coils and intercalary arbuscules along the coils [17, 37].

Figure 1.

Process of root colonization in ectomycorrhizal (A) and arbuscular mycorrhizal (B) (adopted from [33]).

In AM roots the fungus penetrates intercellularly and intracellularly into the root cortex, whereas in ectomycorrhizal (ECM) roots the fungus only penetrates intercellularly into the root cortex (Figure 1) [17]. An ECM root is characterized by the presence of three structural components: a sheath or mantle, Hartig net (complex intercellular network system), and extraradical mycelium [16]. The mycelium can take nitrate and ammonium from the soil and transfer to the plants [3]. However, AMF mainly uptake ammonium from the soil and transfer to the plants [38, 39]. The host plant root exudates of Strigolactone bring recursive spore germination and hyphal branching, while Myc factors secreted by mycorrhiza perceived by host roots to trigger the signal transduction pathway or common symbiosis (SYM) pathway lead to adhesion of a hyphopodium to the root surface via Ca²⁺ spiking. Fungal hyphae emerging from this hyphopodium penetrate into the root through the prepenetration apparatus, which guides the fungal hyphae through the root cells toward the cortex. Eventually, a highly branched arbuscule occupies most of the cell volume, forming an extensive surface for nutrient exchange (Figure 1) [33].

AMF produce a high number of spores that grow faster even under different stress conditions [40] and produce thick-walled hyphae that penetrate the host root and extend from the roots out into the soil where they interface with soil particles [9]. Then they create a network of extraradical mycelium structure, which increases the fungal absorbing surface and facilitates the translocation of mineral nutrients from soil to host plants (Figure 1) [10, 16]. Despite its coenocytic nature, the mycelium that is formed within the root, the intraradical mycelium (IRM) differs morphologically and functionally from the ERM, the mycelium that grows into the soil. The ERM absorbs nutrients from the soil and transfers these nutrients to the host root. The IRM on the other hand releases nutrients into the interfacial apoplast and exchanges them against carbon from the host [17, 18]. Such a fungal structure represents one of the critical elements of the AMF symbiosis and provides increased surface area for nutrient uptake and bridges nutrient depletion zones [10, 37]. These extraradical hyphae acquire phosphate and initiate the colonization of other species [34, 41].

3. Contribution of AMF to plant productivity and agroecosystems

Sustainability of agricultural ecosystems can be restored by stimulating soil life and internally regulated ecosystem processes [31]. The real significance of mycorrhizal fungi is that they connect the primary producers of ecosystems and enable the flow of energy-rich compounds required for nutrient mobilization [32]. Mycorrhizal fungi are one of the commonly occurring living organisms in soil providing many ecosystem services, including N-fixation, soil carbon cycling, plant nutrition, soil erosion control by soil binding capacity [13], soil pollutants remediation, biodiversity, plant water economy [42], and enhanced C-sequestration [22]. AMF and rhizobia can act synergistically and stimulate plant productivity by supplying different limiting nutrients to the plant (e.g., N by rhizobia and P by AM fungi) [43].

Enhanced nutrient uptake and stress resistance are some of the mechanisms by which AM fungi can enhance plant productivity. AMF symbiosis is probably more favorable in conservative and sustainable agriculture to having the potentiality of major beneficial functions such as: (1) increased productivity in the range of 16–78% by gaining more N, P, and other less mobile nutrients increased [24, 43]; (2) increased water uptake and water holding capacity that initiate drought tolerance; (3) increased tolerance to other abiotic stresses such as soil salinity, heavy metal toxicity, etc.; (4) overcoming biotic stresses and offering bio-protection against pathogen; (5) improved soil quality; (6) enhanced plant vigor and yield, thus leading to the production of safe and high-quality foods, able to promote human health (Figure 2) [16, 44]. This is determined by fungal the strain, climate, soil type, and cultural practices (fertilization level) in which the soil type is the fundamental criterion to determine effective AMF symbiosis strains or species [24]. It is also to improve soil fertility, as they produce glomalin upon accumulation in soil that aids soil in soil stabilization [42, 45]. Furthermore, AMF prevent leaching losses, phosphorus (60%), and ammonium (7.5%) from grassland microcosms during periods of heavy rainfall that cause top environmental threats to ecosystems worldwide [46].

Figure 2.

Schematic representation of brief function of arbuscular mycorrhizal fungi (AMF) (source: [44]).

AMF fungi receive 100% of their carbon from the plant, and this increase in carbon flow to the roots, estimated at up to 20% of the plant’s photosynthate, translates to a huge amount of carbon worldwide that plays a significant role in carbon cycling between the atmosphere and biosphere [34]. Bender et al. [47] have demonstrated that AMF contribute to reducing emissions of N₂O by increasing N immobilization into microbial or plant biomass, which results in the reduction of soluble N in the soil and, consequently, in a limitation of denitrification. Thus, AMF could have an indirect influence on potent greenhouse gas (GHG) emissions through change of the physical conditions of soil that influence the production and transport of GHG in soil [26].

The AMF symbiosis can reduce nutrient loss from ecosystems in three main ways: (1) by improving crop nutrient extraction capacity [43] allowing the production of good yield at lower levels of soil fertility; (2) by increasing soil aggregation via physical particle enmeshment and cementing with “sticky” exudates, which results in better soil nutrient storage and retention [48]; and (3) by promoting growth of host crops, thus increasing the size of this desirable nutrient sink [46]. On average, plants inoculated with G. mosseae yielded 13% more biomass relative to non-mycorrhizal plants [49]. Therefore, AMF are vital endosymbionts playing an effective role in plant productivity and the functioning of the ecosystem service.

4. Impact of agrochemicals on crop production and ecosystem service

Excess use of agrochemicals caused tremendous a reduction in soil macro-fauna diversity and promotes the accumulation of toxic compounds in soils that severely harm the environment [6, 30]. Pesticides significantly reduced the diseases and increased the grain yield, yet more resistant pesticides to degradation by abiotic (physical, chemical, and other factors) and biotic (living organisms in the soil food web) agencies, leach into the lower strata of the soil, then absorbed by plant roots, and accumulate in the food chain and are ultimately biomagnified in the food web that is hazardous to human health. They may also affect non-target crop and potentially non-target endangered species by transporting from the sprayed area to non-target areas [6].

Several synthetic fertilizers contain acid radicals, such as hydrochloride and sulfuric radicals, and hence increase the soil acidity and adversely affect soil and plant health [2]. Highly persistent and toxic agrochemicals are available in water, fish, vegetables, and human fluids, which are in turns hazardous to human and ecosystem [30]. These chemical inputs gain access into human body systems through three major means: (i) oral ingestion, (ii) infiltration through the skin, and (iii) breathing causing chronic disease [30] from respiratory disorders and musculoskeletal illnesses due to lack of knowledge of the caution code for hazardous agrochemicals.

5. The possible mechanism of AMF for improving nutrients bioavailability and reducing chemical fertilizer

5.1 How can AMF symbiosis reduce chemical fertilizer?

5.1.1 Increasing the surface area for nutrient absorption of plant roots

The uptake of mineral nutrients from the soil by plants is greatly aided by mutualistic associations with mycorrhizal fungi, which have two pathways for nutrients uptake such as direct pathway that involves the uptake of nutrients via high- or low-affinity uptake transporters in the plant root hairs and the mycorrhizal pathway that involves rapid uptake and translocation of nutrients by fungal transporters in the ERM along the intraradical mycelium (IRM) to the plant root cortex [18, 34, 50, 51]. AMF colonization enhances plant growth performance, root morphology, and leaf nutrient levels that could greatly increase the root-soil interface area [52, 53]. AMF extraradical hyphae can reach a soil volume beyond the nutrient and water depletion zone of roots and may extend up to 8 cm from the root surface, and 1 g of soil contains up to 200 m fungal hyphae [10, 15]. This length is a common parameter used to quantifying fungal hyphae, which greatly increases the surface area for the uptake of immobile nutrients particularly P, N, and Cu [15]. Extraradical hyphae explore soil volumes for nutrient extraction [27] by physically and enzymatically expanding the rhizosphere. Furthermore, fungal hyphae are much thinner than roots and are therefore able to penetrate smaller pores and extract water under dry conditions [54]. It is also improving the efficiency of nutrient cycling and reducing nutrient losses from the soil-plant system [46] that ensures adequate nutrient availability in infertile or less fertile soil.

In additionally water, fungi are able to extract and assimilate soil P from non-plant-available forms such as DNA or P bound to mineral particles [8]. The AMF hyphal network is also able to uptake K and other important micronutrients such as Mg, Zn, Cu, Ca, S, Na, Mn, B, Mo, Fe, Al, and Si, essential for plant growth [16] and led to a mobilization of starch reserves in the apex of grapevine in winter, which was possibly responsible for enhancing root development [44, 55]. Mycorrhizal infection enhances plant growth by increasing nutrient uptake and significant delivery system for P (80%), Cu (60%), N (25%), Zn (25%), and K (10%) via increases in the absorbing surface area, by mobilizing sparingly available nutrient sources, or by excretion of chelating compounds or ectoenzyme [56].

5.1.2 Induces the expression of plant nutrient transporters

It is well known that AMF symbiosis specifically induces the expression of plant Pi transporters (PT4) (Figure 3) [3, 33] reducing the risk of wasteful P loss, thus preserving the quality of water and aquatic ecosystems [46]. In addition to the Pi transporters, mycorrhiza-inducible ammonium transporters (AMT) that not only deliver nutrients to the root cells but also trigger signaling that enables conditions for arbuscule maintenance [26]. Furthermore, the reviews [26] describe that the role AMF symbiosis improves the sulfur, K, and Zn nutritional status of the host plant, affecting the expression of plant transporters. AMF also produce other hydrolytic enzymes such as pectinase, cellulase, hemicellulases, xylanase, and chitinase, which may participate in key steps to mineralize organic chemicals [1].

Figure 3.

Scheme summarizing the main nutrient exchange processes in AMF symbiosis (adapted from [33]).

5.1.3 Reduce biotic and abiotic stress

Mycorrhizal fungi have also a lot of “non-nutritional” effects on plant physiology often alleviating plant stress caused by biotic and abiotic factors such as promoting osmotic adjustment under drought and salinity stresses [16, 57]. AMF symbiosis can also stimulate the synthesis of plant secondary metabolites, which are important for increased plant tolerance to abiotic and biotic stresses. A plant that is associated with diverse community of AMF may have a sort of “insurance” against fluctuating condition [12] through enhancing the activities of antioxidant enzymes (such as superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), and glutathione reductase (GR) [58]) and reduction in H₂O₂ production, then protecting plant cells from deleterious impact of reactive oxygen species (ROS). In plant tissues, excessive ROS induce oxidative damage of lipids, proteins, and nucleic acids that influence normal structure and function. AMF alleviate the oxidative stress from contaminants via mediating the plant antioxidant system, allowing plants to grow better under contamination stress [1] and contribute to better growth under normal as well as stress conditions [59]. This healthy and better growth plant increases nutrient capture by AMF crops [60].

Several studies suggest that enhanced tolerance of AMF plants to water deficit may involve modulation of drought-induced genes by enhancing osmotic adjustment, gas exchange, and water use efficiency of the host plants [57, 61]. This may play a role in the increased tolerance of AMF plants to stress while increasing plant biomass and uptake efficiency of immobile nutrients such as P, Zn, and Cu and decreasing metal toxicity to plants. Therefore, application of AMF in agriculture is used to reclamation waste places to productive agriculture field, which is a promising alternative to conventional fertilization practices, with a view to sustainable agriculture [26].

5.1.4 Improve synergistic interaction of beneficial soil microorganism

AMF colonization can induce quantitative and qualitative changes in root exudates and subsequently modify microbial community structure of the rhizosphere [58]. Particularly, extraradical mycelium fungi provide a direct pathway for translocation of photosynthetically derived carbon to microsites in the soil and a large surface area for interaction with other microorganisms [32]. This enhances synergistic interaction of soil microorganism such as nitrogen fixation P solubilization and the production of phytohormones, siderophores, and antibiotics [37] and then reduces N and P chemical fertilizer application by 10–25% [3, 62], resulting in better root nodulation, nutrient uptake, and plant yield [9]. Rhizobia and AMF fungi often interact synergistically, and their exoenzymes play pivotal roles in accessing, mobilizing, and transferring nutrients [27]. Dual inoculation of such fungi with a Rhizobium and other bacterium on plant enhanced the growth and other beneficial effects, namely resistance to disease and tolerance to adverse soil and climatic conditions [63]. Similarly, co-inoculation of AMF with rhizobium stimulated the N fixation efficiency while improving N transfer and P uptake resulting in the yield advantages of legume/non-legume intercropping [39, 64].

Use of selected native bacterial consortiums reduces the use of nitrogen fertilizer by up to 25%, increasing the productivity of rice cultivation [65]. Other researchers reported that only 25–50% of the recommended N, P, and K rates were required by inoculated crops compared with non-inoculated plants. While the rate of 75% N, P, and K was required by other crops (potato, tomato, pepper, and plantain). Thus, the use of AMF inoculation could lead to reduction of agrochemicals application and reduces their potentially negative impact agro-ecosystem.

5.1.5 Improve soil rhizosphere and plant absorption efficacy

AMF fungal mycelia can facilitate the formation of water-stable soil aggregates via biological, biophysical, and biochemical-based mechanisms such as entanglement and enmeshment of soil particles by AMF extraradical mycelia, production of mucilages, glycoprotein, glomalin (the soil organic matter pool), polysaccharides, and other extracellular compounds [48]. The AMF extraradical hyphal length significantly decreased total soil loss by increasing soil cohesion [66]. This improves plant absorption efficacy for water and nutrients of the low mobility in soil [10]. They also alter the rates of above- and below-ground litter decomposition due to chemical changes in the roots and interactions with the decomposer fungi [15]. Furthermore, increased soil stability can reduce soil erosion, loss of nutrients and organic matter leading to increased aeration and water-holding capacity. This improved soil structure is not only influencing the behavior of organic contaminants in soil, but also helps to maintain high microbial activity, accelerating the biodegradation process, and ultimately enhancing crop safety.

5.2 AMF symbiosis for uptake and translocation of phosphate

Even though phosphorus is a major essential nutrient for plants growth and development, its excess application causes eutrophication of water [67]. It is also bound to Ca and Mg in alkaline soils and readily complexed to charged Al and Fe oxides in acidic soils [68], resulting in a decline of directly absorbed Pi (inorganic phosphate) by the plant root. The arbuscular mycorrhizal fungi (AMF) increase its exploitation of organic P or orthophosphate ions through the organic ions and siderophore production [32] and the changes in sorption balance of soil solution caused by microbial biomass turnover in the rhizosphere [69] besides increasing the absorbing surface area. AMF-induced enhancement in phosphatase activity could possibly mediate the release of organically bound phosphorous, hence increasing transport and uptake of phosphorous in AMF inoculated plants [59]. The mycorrhizal plants displayed a larger phosphorus inflow than the non-mycorrhizal controls [51]. Likewise, AMF fungi possess high-affinity inorganic phosphate (Pi) transporters, which are localized to the extraradical hyphae of G. versiforme, the site of phosphate uptake from the soil (Figure 3) [33]. Similarly, Smith & Smith [19] summarize the possible mechanisms for increased uptake of P by arbuscular mycorrhizal plants: (1) extensive physical exploration of soil by fungal hyphae, thus decreasing the distance that P ions must diffuse before uptake; (2) faster P uptake from solution; (3) production of exudates by AM plants and change of rhizosphere pH. Variation may also occur among AMF fungi in their ability to utilize various inorganic or organic P sources, or in their ability to proliferate in nutrient-rich patches of soil [21]. In AMF-colonized rice, about 70% of the overall Pi acquired is delivered by the symbiotic fungi [60]. In some cases, AMF may be responsible for 100% of host nutrients and have a significant impact on plant growth, health, and subsequently on plant biodiversity and ecosystem productivity [34]. It is evident that such reductions in phosphate application have important economic and environmental benefit [22].

5.3 Transport and assimilation of nitrogen in AMF symbiosis

Plants take up more NH₄⁺ via the AM fungal from soils in very low concentrations than NO₃⁻ in agricultural soils due to its more efficient energetic and relatively immobile in the soil solution [19, 38, 39, 50], which is highly influenced by agricultural management decision [70]. This may be due to A high-affinity ammonium (NH₄⁺) transporter (AMT2;2) is also localized in the AMF [17]. There are two possible reasons why N delivery by the fungus was negligible for nitrate-N; (1) the hyphal ability to acquire nitrate was very low due to poor development of the extraradical hyphae in comparison with the ammonium supply related to high mobility of nitrate; and (2) the assimilation and deliver rate of nitrate was low [38]. After uptake of N from the soil it is assimilated into Arginine (Arg) in ERM and translocated to IRM, then Arg is broken down to NH₄⁺ via the catabolic arm of the urea cycle and reassimilated by plant through mycorrhiza-inducible transporters (Figure 4) [50, 71, 72]. The experiments of [71] show that fungi directly take up inorganic nitrogen and incorporate into amino acids and then transfer N from extraradical mycelium to the host plant without carbon.

Figure 4.

Model of nitrogen movement in the arbuscular mycorrhizal symbiosis (source: [71]).

Even though contribution of the AMF symbiosis to crop N nutrition is often thought to be small, as inorganic N(NO₃⁺ or NH₄⁺) in soil is much more mobile, and unlike ecto- and ericoid mycorrhizas organic N is not available for AMF due to lack of saprotrophic ability [18, 60]; several studies confirmed that AMF are able to take up organic N sources from the soil mainly in the form of amino acids using RiPTR2 transporter [50]. AMF also play vital role in accelerating the decomposition of organic material and nutrient cycling in soils through providing decomposers with plant-derived carbon inputs and transfer decomposition products to the plant [50]. Thus, AMF can play an indirect stimulatory role in the uptake of N from organic sources [36] by influencing organic matter decomposition through bacterial activity [49].

In sustainable system, mineral N levels should be kept low as NO₃⁺ can be reduced to N₂O, a potent greenhouse gas, or lost from the soil-plant system through leaching [46] and negatively impacting surface and ground water quality. Therefore, presence of AMF fungi in the plant-soil system can enhance mineralization of N from organic residues in soil, and the N released can be better used by plants tapping AMF networks located in the vicinity of mineralizing residues [46]. In AM root organ cultures, more than 21% of the total N in the roots was taken up by the ERM [73]. Similarly, Tanaka and Yano [38] demonstrated that maize leaves obtain up to 75% of the N taken up by AMF due to high expression levels of GintAMT1 in the ERM, which primarily involved in the NH₄⁺ acquisition of fungal hyphae from the soil. They conclude that the mycorrhizal fungus can rapidly deliver ammonium-N to the plants but lacks the capacity to transfer nitrate to the plant.

5.4 Metal ions transfer in AMF symbiosis

Besides providing resistance to disease and drought, AMF supply a range of limiting nutrients including copper, iron, and zinc to the plant in exchange for carbon [43]. Even though the roles of arbuscular mycorrhizal in the uptake of K, Ca, Mg, and S are poorly understood, numerous studies also reported that AMF increase uptake of K, Ca, and Mg [74]. AMF fungi can increase host plant uptake of K and modulate plant responses to long-term K limitation, by preventing ROS production and upregulating specific genes, including an ortholog of the plasma membrane K⁺/H⁺ exchanger AtCHX20 (cation/H⁺ exchanger) in Medicago truncatula [51].

Arbuscular mycorrhizal fungi (AMF) enhance the nutritional state of their host plant through acquiring and delivering a proportion of resource to their hosts and play potential role in sustainable crop production [75]. The utilization of microbial products has several advantages over conventional chemicals for agricultural purposes [2]: (i) microbial products are considered safer than many of the chemicals now in use; (ii) neither toxic substances nor microbes themselves will be accumulated in the food chain; (iii) self-replication of microbes circumvents the need for repeated application; (iv) target organisms seldom develop resistance as is the case when chemical agents are used to eliminate the pests harmful to plant growth; and (v) properly developed biocontrol agents are not considered harmful to ecological processes or the environment. Rini et al. [76] concluded that AMF application reduced 50% of compound fertilizer needed for oil palm seedlings. Hence, AMF is considered to be a good replacement for inorganic or chemical fertilizer in the future.

5.5 How AMF symbiosis reduces use of pesticides and other chemicals?

5.5.1 Bioremediation

A wide range of toxic pollutants including heavy metals are disposed of daily to the soil and water, which are the most are the most serious disaster affecting humans, plants, and the environment negatively [77, 78]. The conventional remediation methods cause high cost, intensive labor, irreversible changes in soil properties, and disturbance of native soil microflora. Thus, researchers obtain a novel approach called phytoremediation, which is an economically feasible and sustainable option to clean up heavy-metal-contaminated sites. It refers to a green technology that uses plants and associated soil microbes to reclaim HM and radionuclides from the environment by various detoxification mechanisms including phytoextraction, rhizofltration, phytostabilization, phytodesalination, photodegradation, and phytovolatilization; [77, 78, 79], which is one of the low-cost remediation techniques used by microorganisms to remove heavy metals [42].

AMF alleviate heavy metal toxicity due to the ability of fungal hyphae to bind heavy metals outside and inside the roots and restrict their uptake to upper parts [51, 59]. This binding ability is due to AMF hyphae being capable of secreting a glycoprotein called glomalin, which can bind heavy metals and subsequently remove heavy metals absorbed by the plants from contaminated soil. Glomalin can develop the properties and structure of the soil, which helps to enhance soil fertility by linked with soil carbon [42]. This binding of heavy metal to the cell walls of the fungal hyphae in roots and not release to the shoot as the presence of free amino acids, hydroxyl, carboxyl, and other groups are containing the cell wall of fungi representing as act as a filtration barrier against the transfer of heavy metals to plant shoots. Furthermore, metal dissolution by fungi may take place through proton-promoted or ligand-promoted mechanisms and organic acids provide both a source of protons for solubilization and metal-chelating anions to complex the metal cations [32]. The work of [40] suggested that mycorrhizal symbiosis becomes a promising and suitable as phytostabilizers of Cd stressed soil. Similarly, three arbuscular mycorrhizal fungi (AMF) from Glomus, Acaulospora, and Scutellospora, and four plant-growth-promoting rhizobacteria isolates related to genera Streptomyces, Azotobacter, Pseudomonas, and Paenibacillus were found to be effective in phytoremediation of Fe₃C contaminated soil [80]. In general, metal-tolerant fungi grew and solubilized toxic metal minerals better than non-tolerant isolates. Mycorrhizal colonization protects roots against metal such as Cd, Zn, Cu, Pb, Mn, and Ni, toxicity [40, 59, 81]. AMF that promote biodegradation will decrease contaminant residues in both crops and the environment.

5.5.2 As biocontrol agents (biopesticides, bioherbicides)

To prevent environmental pollution and occupational diseases, proactive preventative actions are needed [5]. AMF are particularly important in organic and/or sustainable farming systems that rely on biological processes rather than agrochemicals to control plant diseases. AMF can act as bio-controllers that allow host plants to grow healthier and decrease the application amount and frequency of pesticides and other environmentally harmful agrochemical products [1]. These processes protect plants against soil-borne pathogens and assist in contaminant removal [7] and reduce pesticide application via enhanced crop resistance to pathogens and improved competition with weeds [1]. The use of AMF as safe and sustainable biostimulators and bio-protectants is very promising alternative, as it does not harm the environment, resulting in sustainable food production [82].

The complex interactions between plant, pathogen, and AMF symbiosis can enhance host plant resistance or tolerance to root pathogenesis [83]. The major mechanisms related to bio-protection role of AMF are indirect mechanisms such as enhanced mineral nutrition status of plants (enhance resistance and tolerance), changes in root architecture (e.g., increase in lateral branches and cell wall lignification), competition for infection sites (the pathogen never penetrated arbuscule-containing cells), change in rhizodeposition (alter the chemotaxis to the roots by the pathogens), and activation of plant defense responses [83]. The mechanisms of biocontrol exercised by most microbial inoculants could be attributed to release of extracellular hydrolytic enzymes, competition for nutrients and secondary metabolites toxic to plant pathogens at very low concentrations [84].

AMF plants may be more appealing to herbivores, reduce disease symptoms for some disease, and more attractive to pollinators due to their altered architecture and improved nutrient status [12]. An interesting issue in mycorrhizal plant-parasite interaction is a recently reported potential of mycorrhiza to provide partly protection and control of Striga [85, 86]. They observed as AMF negatively impacted on Striga seed germination, reduced the number of Striga seedlings attaching and emerging, and delayed the emergence time of Striga both in pot and field experiments. Exudates from mycorrhizal sorghum plants resulted in much lower germination of Striga seeds than exudates of non-mycorrhizal sorghum plants. AMF also have an indirect beneficial effect by enhancing the fitness of the cereal host and thereby allowed the host to withstand Striga damage better. Therefore, AMF might be able to substitute for reduced fertilizer and biocide inputs in organic systems, which is not permitted in organic systems [74], while increasing productivity in the range of 16–78% by gaining more N, P, and other less mobile nutrients increased [24].

5.6 Factors affecting AMF-soil-environmental symbiosis

Mycorrhizal symbioses in agro-ecosystems are affected by various factors including species compatibility with the target environment, the degree of spatial competition with other soil organisms in the target niche, and the timing of inoculation [26, 87]. AMF symbiosis and growth are also influenced by the host plant genotype (for instance, legumes more mycotrophic than grasses [39]), AMF species, soil fertility, and percentage of root infection [13, 37, 56]. A very challenging for large-scale production of AMF is its obligate symbionts behaviors [26, 12] and having high degree of genetic and lack of a uninucleate cell stage in the life cycle of AMF [33]. Similarly, equally or even better performance of indigenous AMF [10] than commercial or culture collection isolates is another headache for producers [26], which may cause potential environmental risks without providing higher plant benefits [27]. This promotes encouraging farmers to autonomously produce their AMF to make technology affordable and sustainable.

Application of agrochemicals also reduces network complexity and the abundance of AMF particularly, the nutritional status of the plant and surrounding environment such as P [28, 51]. Because high levels of P repressed the expression of genes encoding carotenoid and strigolactone biosynthesis enzymes in plants, suggesting that high levels of P directly inhibit spore germination by reducing strigolactone biosynthesis then reducing the Pi flux from AM fungi, which in turn reduces the amount of carbohydrates transferred to AM fungi [51]. This reduces abundance of AMF in soil (e.g., by fertilization) could reduce the importance of AM fungi for ecosystem functioning, including their ability to reduce nutrient leaching losses [46].

Furthermore, land uses, crop rotations, and soil features affect the AMF diversity and their community functioning due to changes in soil physical and chemical characteristics [88]. Less-intensive tillage is a viable strategy for enhancing root colonization by indigenous AMF across soil types and crop species [27]. Reduced tillage, manures, and cover crops are recognized as a practical way to maintain high population of functional effective AMF eventually to support sustainable crop production [89]. This is true if you did not use herbicide such as glyphosate that hinders and detrimental for subsequent AMF recovery. This specificity suggests that crop species in rotations may influence the quality of the AMF population in the soil of a following crop [10]. Once AMF biodiversity is restored and well-established with AMF-friendly management before and after cultivation mycorrhizal hyphal network will remain unaltered and infective in the future [26].

Generally, for increasing effectiveness and success AMF inoculation reducing tillage rate, bare fallows, agrochemicals usage, and use of non-mycorrhizal crops in rotation vital for enhancing abundance and contribution of AMF fungi as ecological services in agriculture [22]. The review of [60] summarize the management of the AMF symbiosis is achievable through a variety of agronomic practices, in particular: (1) tillage, (2) crop nutrition, (3) grazing, and (4) integrated pest management, as well as by (5) the selection of crop genotypes and crop rotation sequences, (6) the use of AMF inoculants, and (7) the use of biotechnologies that enhance the AMF symbiosis of crop plants. Thus, understanding best management practice of AMF in crop production would insure good extraradical mycelium development leading to soil quality improvement and reduced activity of soil-borne pathogens [10].

6. Concluding remarks

Harnessing natural resources including beneficiary microorganisms is one of the most effective approaches to improving farm productivity and food quality in a sustainable way. Microbial inoculant technology will ensure healthy food security for the future population. AMF efficiently use for agricultural productivity in sustainable manner in which the diversity and function of soil microorganism is the decisive issue in the agrarian activities and ecosystem service [23]. AMF might be able to substitute chemical fertilizer and biocide inputs in organic systems [74], while increasing productivity in the range of 16–78% by gaining more nitrogen (N), phosphorus (P), and other less mobile nutrients increased [24]. This role of AMF can reduce the catastrophic effect indiscriminate use of agrochemicals in agricultural sectors and promotes. Hence, reintroducing AMF into agro-systems may also improve nutrient use efficiency, water-use efficiency, and tolerance to pathogens and herbivores [12]. Finlay [32] suggests more research on AMF as its relevant species have not yet been investigated since there has been a general concentration on agricultural systems in which additions of inorganic fertilizers, pesticides, and plant breeding may have selected against arbuscular mycorrhizal fungi with the capacity to mobilize organic substrates.

Mycorrhizal symbioses in agro-ecosystems are affected by various factors including all biotic, abiotic, and agronomic management factors related to complex interaction of soil-AMF and host plant. Thus, selection of new crop varieties giving yields on poor soils and in low fertilization conditions and understanding compatible management practice in crop production that would ensure good extraradical mycelium development leading to improvement of soil quality and crop productivity in holistic manner is paramount importance for successful exploitation of arbuscular mycorrhizal fungi.

Acknowledgments

The authors are highly thankful to researchers whose findings are included directly or indirectly in preparing this manuscript.

Conflicts of interest

The authors declare no conflict of interest.

Funding

The authors received no direct funding for this research.

Data availability

All data generated are included in this article reference’s part.

Abbreviations

AMT	ammonium transporters
AMF	arbuscular mycorrhizal fungi
SYM	common symbiosis
ECM	ectomycorrhizal
ERM	extraradical mycelium
GHG	greenhouse gas
IRM	intraradical mycelium
PT4	Pi transporters
ROS	reactive oxygen species