Keywords

2.1 Introduction

Arbuscular mycorrhizae (AM) are geographically ubiquitous soil-borne microorganisms that establish a mutualistic symbiosis with the vast majority of terrestrial plants. They develop symbiotic mutualisms with roots of about 70–90% of vascular plant species (Smith and Read 2010). AM fungi are the members of an ancient phylum, Glomeromycota . They are the most abundant type of fungi found in the soil contributing 5–36% of the total soil biomass and about 9–55% of the soil microbial biomass (Olsson et al. 1999). AM fungi are obligate biotrophs , which need a host plant to complete their life cycle (Bago and Bécard 2002). However, the real mechanisms of their occurrence, diversity and dispersal under natural conditions are still obscure. The significance of mycorrhiza in sustainable agriculture has been established already several years ago, but the importance of these in the level of application was recognized only recently. AM fungi play a pivotal role in enhancing plant growth and fostering plant diversity. They also improve soil structure by forming extensive networks of hyphae in the soil. Therefore, AM fungi are important in organic farming systems and other sustainable agriculture practises. The sustainability concept in agriculture focus on increasing the productive capacity of the soil, to efficiently recycle the nutrients and organic matter and to minimize the required energy and resources. Sustainability demands effective utilization of nutrients by plants. This process can be facilitated through mycorrhizal associations (Jeffries and Barea 2001).

In plant-AM fungi association , a bidirectional trade of nutrients takes place between plant and AM fungi through extensively branched haustoria, termed arbuscules. The plant supplies up to 20% of carbon to the AM fungi from its fixed photosynthates, while AM fungi support the plant for the uptake of water, phosphates and other mineral nutrients available in soil. The development of AM fungi is accompanied by novel class of plant hormones, known as strigolactones, which act as the signalling molecule between the symbionts. Strigolactones produced by the plant root stimulate metabolism and branching in AM fungi, which in turn initiates the symbiotic association. AM fungi also play a key role in increasing host plant’s resistance to root pathogens and tolerance to abiotic stresses (Smith and Gianinazzi-Pearson 1988). Mycorrhizal symbiosis is a keystone to plant diversity and productivity as they influence nearly all metabolic processes of the plants (Bonfante and Genre 2015). Owing to their diverse functionality and host benefit interaction, utilizing mycorrhizal inoculants in sustainable agriculture and forestry has major potential for maintaining plant growth and development.

2.2 Characteristics of AM Fungal Symbiosis

In the rhizosphere, AM fungi live in symbiosis with plant roots, forming intra-radical (hyphae, arbuscules, vesicles) and extra radical (hyphae, spores) structures. They are one group of the beneficial soil mycobionts associated with plants that colonize roots and form the mycelial network to facilitate nutrient uptake and plant growth. The benefits acquired through AM-plant symbiosis can be physiological, nutritional or ecological. AM fungi have been widely utilized in agriculture, vegetation restoration and horticulture for around two decades. Mycorrhizal network, also termed as common mycorrhizal network (CMN), is one of the primary element of terrestrial ecosystem, which has substantial effect on different plant communities, especially on invasive plant species such as Lythrum salicaria (Pringle et al. 2009). The host plants get rewards of symbiosis based on the identity of AM fungal species (Facelli et al. 2010; Hoeksema et al. 2010). In plant-mycorrhizal symbiosis, fungal hyphae in the rhizosphere reach out in the soil and transport phosphorous, nitrogen and other essential nutrients to the plants (Yadav et al. 2020c).

AM fungi improve plants tolerance to different stress environments which may be biotic or abiotic via beneficial changes in their morphological and physiological traits (Feddermann et al. 2010; Hashem et al. 2015; Plassard and Dell 2010). A major challenge faced by the mycorrhizologist is to understand the signalling mechanisms and the colonization process of the extremely symbiotic AM fungi towards its host plants. AM fungi cannot be cultured in the absence of a host plant and that is the reason why they are often known as obligate biotrophs, which always need symbiotic relation with its host plant to complete its life cycle. It is an accepted fact that during the long run of evolution, AM fungi lost some of its carbon-fixing capabilities and the genetic machinery that supports their symbiotic relationship with the plants and became completely dependent on the host plant for a fixed carbon supply. A pragmatic evidence for this hypothesis is still lacking, but several indirect approaches to the study of this relationship have been developed. AM fungi are natural biofertilizers in soil as they nurture the growth of many terrestrial plants. Furthermore, AM fungi-enriched soil is remarkably more fertile and forms constant masses with significantly higher extra-radical fungal mycelium. Glomalin-related soil protein (GRSP), which is found abundantly in hyphae and spores of AM fungi, that helps to sustain the water content in soil subjected to diverse stress conditions which in turn regulates water frequencies between plants and soil thus triggers the plant growth and development (Wu et al. 2014). Glomalin and its relative compounds protect the soil from dehydration by enhancing soil aggregation and thus augmenting the water holding capacity in soil (Sharma et al. 2017). Therefore, researchers encourage the use of AM fungi as biofertilizers in sustainable crop improvement (Barrow 2012). Upon AM fungi inoculation, plant growth related functions such as photosynthesis, uptake of water and CO2 assimilation increases (Chandrasekaran et al. 2019).

An ecologically important association is detected in the rhizosphere between leguminous plants and rhizobia. This mutualistic relation is induced by a fungal factor called Myc, which is analogous to the rhizobial signalling molecules such as Nod factor. Myc factors are the AM fungal signals that stimulate and establish AM symbiosis in leguminous and other mycotrophic plant species. However, it is still unclear whether the Myc factors are induced by plant root generated strictolactones. Besides acting as stimulators of AM fungal symbiosis, Myc factors function as plant growth regulators (Maillet et al. 2011). Myc factor has been considered the ideal candidate for biofertilizers in green technology applications. For example, leguminous seeds treated with Myc factor and Nod factors increased yields of crops such as pea, alfalfa and soybean. Compared to Nod factors, Myc factors have much broad spectrum of activity that results in the form of improved mycorrhization in plant roots, which in turn facilitate a better uptake of water and nutrients and resistance to various stresses by the host plant. For large-scale application, an efficient synthesis and production of Myc factors by bacteria has already been developed (Maillet et al. 2011). In order to implement the Myc factors in agriculture, a detailed investigation is needed to understand the biological activity and specificity of Myc factors on the host plant, as well as the optimal conditions required for its application (López-Ráez and Pozo 2013).

2.3 Taxonomy/Phylogenetic Classification

Mostly, AM fungi form deep monophyletic branches within the fungi and are very diverse that they are ranked with a taxonomic phylum, Glomeromycota, which currently comprises of approximately 200 species distributed among 14 genera (Schüβler et al. 2001; Stürmer 2012). The phylum Glomeromycota contains all known AM fungi which are co-evolved with their host plants, which originated in the terrestrial habitat during the Ordovician period more than 430 million years ago. Molecular studies performed later in the 1990s validated the finding that the AM fungi originated at a time between the Ordovician and the Devonian period (Helgason et al. 2007; Simon et al. 1993). Excitingly, the mycorrhizal association existed before plants had evolved its true roots (Bonfante and Selosse 2010). According to the phylogenetic analyses of SSU ribosomal RNA gene sequences, AM fungi have been moved from the Zygomycota to a new phylum Glomeromycota (Schüßler and Christopher 2011). The conventional taxonomy of AM fungi works on the basis of its morphological features of the hyphae, spores and the layers of the cell wall (Morton and Msiska 2010). However, the evaluation of the actual distribution patterns of Glomeromycota assemblages in all ecosystems requires further scrutiny (Lee et al. 2013).

Recent revolutions in the molecular techniques have enabled re-evaluation of the taxonomy and systematics so that many robust classifications of AM fungi have been introduced. New classification systems are introduced based on morphological and ontogenic characters of AM fungal spores, as well as consensus nucleotide sequences (SSU, ITS, LSU, β-tubulin and nrDNA) (Błaszkowski et al. 2014; Oehl et al. 2011). Based on the latest classification, the phylum Glomeromycota comprise of four orders (Diversisporales, Archaeosporales, Paraglomerales and Glomerales), which consist of 11 families, 25 genera and approximately 250 species (Redecker et al. 2013). Goto et al. (2012) proposed a new classification based on combined molecular and morphological studies. Recent studies of root samples using next-generation sequencing indicate that the number of species may be several magnitudes higher than what is known to date (Chen et al. 2018).

2.4 Beneficial Aspects of AM Fungi

Various benefits acquired by plants establishing symbiotic association with AM fungi are mainly due to the well expanded extra radical mycelium produced by AM fungi, which take up the nutrients and other essential elements from the rhizosphere zone within the bulk soil and transfer it to the host plant root in exchange for carbon (Rastegari et al. 2020a, b; Yadav et al. 2020c). Compared to plant root hairs, AM hyphae are longer and thinner, which help them to move greater distances from the root and to get into soil pores which are unreachable to plant root hairs. It has been estimated that for each centimetre of colonized root by AM fungi, there will be an increase in the volume of soil explored by 15 cm3. This value can increase up to 200 cm3 depending on the environmental factors involved (Sieverding et al. 1991). The ratio of the length of AM fungal hyphae to that of roots in soil is expected to be 100:1 or greater (George et al. 1995). With effective colonization of AM fungi in the plant roots together with the ability of extra radical mycelium to transport nutrients is one of the well-known advantage of mycorrhizal formation, especially those nutrients (e.g. phosphorus) that have mobility limitations in soil. In addition, the extra radical hyphae provide greater stability of soil structure by enmeshing soil particles and by producing substances that bond soil particles together. AM fungi contribute substantially to the formation and aggregation of smaller soil particles into larger macro-aggregates (Rillig and Mummey 2006).

AM fungi provide many other benefits to host plants other than nutrient acquisition. These include stress alleviation to abiotic and biotic factors, such as pathogenic tolerance, water stress, drought, tolerance to toxic heavy metals, pH, salinity and adverse temperature (Singh et al. 2020; Singh and Yadav 2020). AM fungi association increases the efficiency of N fixation by legumes and a better plant performance following transplantation shock (Campanelli et al. 2013; Chen et al. 2018; Meddad-Hamza et al. 2010). AM plants show physiological and morphological changes, especially when they are growing in stressful conditions. This results in the form of modifying some essential growth regulators, such as indole-3-acetic acid (IAA), indole-3-butyric acid (IBA) and jasmonic acid, that help the host plant to have a better adaptation and homeostasis with the changing environmental conditions (Cameron et al. 2013; Foo et al. 2013). Reports state that even with a weaker AM fungi colonization, gene expression in plants can be altered. For an example, with a very weak AM fungal colonization, the mechanism involved in the expression of inorganic P (Pi) transporters get changed (Poulsen et al. 2005). Studies suggested that there will be an increase in the average yield of the crop plants upon increased AM fungal colonization (McGonigle and Fitter 1988).

2.5 Commercial Application of AM Fungi

The beneficial attributes of AM fungi have raised the possibility of their commercial application. In the last few decades, AM fungi market has increased and diversified with more patented products becoming available (Devi et al. 2020). Globally, the leading producers are located in the United States, China and India. In the last decade, the Indian market has seen remarkable progress in biofertilizer production (Chen et al. 2018). The European market is the leading marketplace for mycorrhizal-based biostimulants. As per surveys, the companies involved in producing and marketing AM fungi products are growing every year. In 1990s, the number of companies selling AM fungi products was 10; it has reached to 75 firms in 2017. The main areas of AM fungi application include agriculture, landscaping, forestry, horticulture, restoration of degraded land, soil remediation and research. Sometimes mycorrhizal inoculants are available in the form of mixed inocula, which have different strains of AM fungi and rhizobacteria or PGPR (Kour et al. 2019). The cost of mycorrhizal inoculation for potato field was estimated to be $135 per hectare in the United States (Hijri 2016). AM fungi inocula are nowadays utilized as biofertilizers for sustainable agriculture applications, but a larger volume of inocula production is possible only through conventional pot culture methods. AM inocula are available as spores, root fragments of plants colonized by AM fungi, or the combination of the two or by the incorporation of mycelium. The cultured or isolated inocula are usually mixed with a carrier material in either solid or liquid form and applied directly to the soil or plants. Mostly used carrier materials include perlite, clay, sand, vermiculite, soilrite and glass pellets.

Other alternative methods for AM inocula production include soil-free aeroponics systems (Jarstfer and Sylvia 1995), nutrient film (Elmes and Mosse 1984) and root organ culture (Mugnier and Mosse 1987), though they are not cost-effective, and large-scale production with them is poorly developed. Though AM fungi have been reported as excellent biofertilizers, their large-scale production and inoculation are not practical and achievable for a large-scale agriculture application because they are strictly produced by conventional pot culture method. The application has been limited more on the production of high-value nursery stocks, gardening practices and research purposes. Another aspect is the need for diverse communities of AM fungi in the product, as different species perform differently in the soil upon inoculation. This again influenced by various environmental conditions. Furthermore, research evidence suggests that different species of AM fungi vary in their ability to increase the crop yield and nutrient transport to its host plant (Rai 2006).

2.6 Significance of AM Fungi in Natural Habitats

The degree to which a plant benefits from AM fungal symbiosis mainly depends on the environmental conditions. AM fungi have always been considered important plant symbionts in natural habitats with poor soil conditions. Plant root cells with arbuscules receive more nutrients due to considerably increased contact surface (Alexander et al. 1989). Another way to absorb nutrients is through AM fungal hyphae networks. The AM fungi-colonized plants seem to develop special pathways and mechanisms to improve their nutrient uptake. Therefore, it is likely that the plants with AM fungi symbiosis thrive better than the non-AM plants in habitats with low nutrient contents. Phosphorus is one of the main nutrients, that is made available for plants in the form of phosphate via AM fungi symbiosis (Karandashov and Bucher 2005; MacLean et al. 2017). Studies have shown that apart from phosphorus, other nutrients are being transferred to plants via AM fungal symbiosis. Although the mechanisms and pathways of phosphate transfer are well studied, more information is needed to understand how AM fungi help plants in acquiring the necessary nutrients such as potassium (Garcia and Zimmermann 2014), nitrogen (Correa et al. 2015), sulphur (Casieri et al. 2012), and some micronutrients like as zinc (Smith et al. 2010) and Fe (Ouledali et al. 2018). Therefore, AM-associated plants in natural habitats with low nutrient availability have the advantage of easier access to nutrients compared to non-AM associated plants (Yadav et al. 2020a, b). When it comes to competition over the resources, AM-associated plants might have a better survival rate.

Under natural conditions, plants are always subjected to various environmental stresses, which have negative impact on plant growth and development and it often leads to a threat on their survival (Ruiz-Lozano 2003). AM fungi have been found in various environments. It is believed that apart from the nutrient exchange, they could assist plants in surviving some environmental stress such as salinity or drought in arid and semiarid areas. In arid lands, when plants are under stress due to low water availability, they undergo anatomical, physiological and metabolic adaptations (Bray 2004; Rossi et al. 2013). Some plant species evolved in the land to avoid drought while others tolerate it through certain dodges. In this respect, AM fungi play a crucial role in plants to develop tolerance to drought via root symbiosis (Rapparini and Peñuelas 2014). In such symbiosis, host plants attain an integrative drought response by achieving either a tolerance or avoidance strategies, which help the host plant to well adapt with the situation (Ouledali et al. 2018; Rapparini and Peñuelas 2014; Ruiz-Sánchez et al. 2010). AM fungi can enhance drought resistance of their host plants through affecting the physiological nutrient uptake, hormone balance, osmotic adjustment and antioxidant systems (Wu and Zou 2017). P nutrition enhancement (Bethlenfalvay et al. 1988; Sweatt and Davies Jr 1984), increasing water uptake capacity by hyphae (Zou et al. 2015), and longer roots (Bryla and Duniway 1997) in AM-associated plants are additional AM benefits assisting them in overcoming drought stress. In general, plant growth strongly gets affected by drought, while AM fungi symbiosis significantly mitigates the negative effects of drought stress in plants. Recent studies show that AM fungi are more common in drier/non-irrigated soils compared to irrigated soils in certain plant species (Landolt et al. 2020). It is believed that in root, microbial symbiosis, such as AM, could be the most important factor in the resistance of some tree species to drought (Calvo-Polanco et al. 2016).

Several studies have investigated the role of AM fungi symbiosis in saline environments (Pan et al. 2020; Sonjak et al. 2009; Wang et al. 2004). Presence of excess salt in the soil affect the water and nutrient uptake efficiency of plants resulting in disrupting the distribution of ions channels at the cellular level. This will create an osmotic and ionic imbalance in the plant cells and thus negatively influence the plant growth mechanisms (Saxena et al. 2017). Adaptations to high levels of salinity in AM fungi-colonized plants include improvements in host photosynthetic potential, water use efficiency, nutrition and tolerance to ion toxicity, as well as several metabolic adaptations. The metabolic adaptations facilitated by AM fungi include higher K+/Na+ ratios in host tissues, improved maintenance of ion homeostasis and the accumulation of essential amino acids such as glycine, proline, betaine or soluble sugars that improve osmotic adjustment (Porcel et al. 2012). Thus, AM fungi found in natural saline environments could help with plant salt resistance in agricultural plants as well. Being the most severe abiotic stress, soil salinity affects the plant growth and production worldwide. Therefore, the application of such fungi could be of importance regarding crop production in saline environments. Similarly, AM fungi symbiosis offer temperature stress resistance in host plant via increasing its nutrient and water uptake efficiency, improving the photosynthetic capacity, increasing the osmolyte accumulation and reducing the oxidative damage by producing more secondary metabolites (Zhu et al. 2017). These changes could help the host plant to overcome stress caused by temperature extremes. AM fungi could also have alleviating effects on heavy metal stress in plants growing in the polluted habitats. This adverse effects caused by elevated levels of heavy metals can be mitigated by increased water and nutrients uptake and production of plant hormones, changes to root activities, including heavy metal uptake, or indirectly via interactions with the other soil microbes (Garg and Pandey 2015; Miransari 2010; Miransari 2017; Vangronsveld et al. 2005).

The success of host plant survival under harsh and stressed environment depends on the AM fungi habitat adaptation and co-evolution with its host plants (Meharg and Cairney 1999; Querejeta et al. 2006). Plants that do not have the adaptive mechanisms to survive the environmental stress are more likely to depend on AM fungi symbiosis for survival. For example, in a recent study conducted by Pan and co-authors (Pan et al. 2020) indicated that glycophyte plants are more dependent on AM fungi symbiosis than halophyte plants to tolerate the saline environments. Interspecific differences in the tolerance of AM fungi to environmental stress and their different reaction to the stress when forming symbiosis with different plant species highlight the importance of AM fungi studies in the natural environments. Indeed, AM fungal diversity and composition are significantly affected by the environmental variables such as plant community composition (Krüger et al. 2017) and functional groups (Gui et al. 2018), climatic changes (Xiang et al. 2016), properties of the soil (Abdedaiem et al. 2020; Carballar-Hernández et al. 2017; Gai et al. 2012; Yang et al. 2016), as well as practices used in management (Binet et al. 2013; Borriello et al. 2012; Higo et al. 2013; Lu et al. 2018; Uibopuu et al. 2009). These changes in the AM fungi community could lead to substantial changes in their effects on plant communities. Understanding the factors affecting the AM fungi communities in different habitats is essential to understand and predict their role in ecosystem services under future climate changes and the consequences.

2.7 The Significant Role of AM Fungi on Crop Health

The AM symbiosis offers several benefits to host plants and their surrounding habitats. They boost plant defence against soil pathogens, increase abiotic stress tolerance, heavy metal tolerance, and adaptation to climate changes (French 2017). During stress conditions, especially in drought, the stress tolerance in plants can be increased by AM fungi symbiosis. This leads to a higher amount of sugar substances such as trehalose and mycose in the host plant tissues. Such substance improves the plant tolerance against biotic and abiotic stress by producing secondary substances, which in turn improve cellular structures, cell wall and lipid bilayers (Lunn et al. 2014). Inoculation of vascular plants with ectomycorrhizal and AM fungi activates the production of trehalose in root cells of host plant (Müller et al. 1995), which improves the carbohydrate metabolism in plants via changing the amount of starch or sugar in the plant tissue (Wagner et al. 1986) and provides stress tolerance benefits to the host plants via mutual symbiosis. For example, under extreme drought, the cells of the AM-associated plants have a better chance to become intact and return back to normal under favourable environmental conditions (Wingler 2002).

Studies show that AM fungi induced defence against bacteria, other pathogenic fungi, nematodes, and insects (Jung et al. 2012). This defence mechanism mostly results from increased plant secondary metabolism followed by the AM fungi symbiosis. Such secondary metabolites are alkaloids and phenolic compounds, which can be found in the trichomes and vacuoles of the AM-associated plants that can improve the plant tolerance against pathogens and insects (Champagne and Boutry 2016). During a pathogenic attack, internal and external hyphae sense the pathogen metabolic compounds in the soil surrounding the roots. AM fungi then warns the host cell by producing short chitooligosaccharides (Cos) and lipo-chitooligosaccharides (LCOs) (Bonfante and Genre 2015; Zipfel and Oldroyd 2017); this message then transmits from cell to cell in the host plant via plasmodesmata.

Another significant feature of AM fungi is heavy metal tolerance in crops. AM fungi have chitin and melanin compounds attached to the cell wall, which could form a chemical chain with the unfavourable elements in the rhizosphere soil around the roots (Eisenman and Casadevall 2012). The melanin compounds in fungi protect them from harsh environmental conditions (Zhdanova et al. 2000). A clear mechanism behind the role of AM fungi in metal tolerance is unclear. It is believed that AM fungi use multiple mechanisms to immobilize metal ions. In the case of some ectomycorrhizae, these ions are stored in the cell wall, cytoplasm, and vacuole. It is suggested that AM fungi also alters the host metabolisms to respond to metal toxicity. For example, Funneliformins mosseae increased the metallothioneins in the Festuca sp. plants that have been growing in a soil with high nickel contamination by transcription of the related genes (Shabani and Sabzalian 2016).

AM fungi are cosmopolitan in distribution and their diversity has been detected in all major ecosystems across the globe (Davison et al. 2018; Öpik et al. 2013). Some AM fungi isolates are reported to have restricted distribution in natural communities (Rosendahl et al. 2009). The diversity of AM fungi is reported in arctic regions, deserts in the Arabic peninsula, tropical forest and even in the higher Himalayas (Al-Yahya’ei et al. 2011; Liu et al. 2011; Lovelock et al. 2003; Varga et al. 2015). The presence of cosmopolitan AM fungi species indicates that they are highly adaptable and have a great impact on the environment.

Another important service provided by AM fungi to both natural and agricultural systems may be the improvement of the soil structure. AMF hyphae which colonize in and around the plant root form a dense hyphal network, which highly interacts with the soil particles due to increased surface that is in contact with the soil. The glycoprotein referred to as glomalin improves the soil structure by affecting the soil aggregates (Singh et al. 2013). Glomalin improves the soil quality, when it is produced by spores and hyphae of AM fungi in the roots and their surrounding soil. They act as a very stable carbon sink and decrease the organic carbon degradation via improving the soil aggregation, thus functioning as carbon sequestration in soil (Rillig et al. 2001). AM fungi also benefit plant growth via higher water retention capacity by improving soil qualities, especially for plants growing in arid/semiarid areas or soils with low water availability (Chen et al. 2018). Nutrient leaching is another major problem faced in agriculture, which results in loss of soil fertility and groundwater pollution (Cavagnaro et al. 2015). Inoculation with AM fungi improves soil structure and facilitates storage of nutrients in the aggregates of mycorrhizal soil, thus benefiting plant nutrient and water availability (Querejeta 2017). AM fungi also alter the available nutrient in the soil by creating closed nutrient cycles, which provide long-term soil fertility (Cavagnaro et al. 2015). The beneficial effects and the role of AM fungi in plant growth and development are depicted in the Fig. 2.1.

Fig. 2.1
figure 1

The beneficial role of AM fungi in plant growth and development

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2.8 Application of AM Fungi in Agricultural and Horticultural Crops

Majority of the agriculture crops are found to be potential hosts for AM fungi, and inoculation with AM fungi increases their productivity and fitness (Begum et al. 2019). AM fungi induce plant tolerance to environmental stress by interfering with phytohormone balance. AM fungi absorb and translocate minerals from the soil layers that are out of plant root zone and alter the secondary metabolisms leading to better metabolic trait. AM fungi also increase the root development and surface absorbing capability of host plants (Paszkowski and Gutjahr 2013). AM fungi have been widely used in agriculture and horticulture field applications. The success of AM fungi application always depends on external factors, that is management strategies such as weed control, pruning, ploughing and fertilizer usage (specially P), that interfere with AM fungi composition and colonization in the rhizosphere (Chen et al. 2018), as well as on the selection of an effective strain of AM fungi and the host plant (Njeru et al. 2015). In addition, selecting the ideal AM fungus is important for every crop (Njeru et al. 2015; Rouphael et al. 2015). The adaptation of plants produced by cuttings and micropropagation is a critical task in horticulture. Most horticulture practices involve sterile in vitro micropropagation production, but during the time of weaning, it can cause large losses. AM fungi inoculation is found to be an alternative solution to improve plant growth and nutrient uptake during the early stages, which results in larger products with higher commercial values (Schubert and Lubraco 2000). Many studies have reported the significance of AM fungi in the development of fruit seedlings in early stages. For example, in a study conducted by Schubert and Lubraco (2000), apple seedlings growth characteristics significantly improved by the AM fungi symbiosis.

Arbuscular mycorrhizal inoculation is profitable in agriculture. Large-scale production of AM fungi and coating seeds with them is the most suitable method of application. Many crop varieties have been significantly affected by inoculation with AM fungi (Ortaş et al. 2017). Researchers have suggested two main approaches of using AM fungi; inoculum production in the field and developing cultural practices that improve the native population of mycorrhizal fungi (Roy-Bolduc and Hijri 2011). A meta-analysis on potato carried out in 231 different crop fields of Europe and North America revealed a significant increase in tuber growth rate and size after inoculation with R. irregularis (DAOM 197198) (Hijri 2016). The average crop yield in the trials was 3.9 tons/ha, which constitute 9.5% of total crop yield. With an estimated profitability threshold of 0.67 tons/ha increased yield, nearly 80% of the trials were found to be more profitable. Though cultural methods often improve the effectiveness of native mycorrhiza, they do not create the best specific AM fungi-plant symbiosis for commercial production. This can be an important challenge when solving food security issues. Similarly, the selection of a suitable host plant is another concern (Ortas 2015; Ortas and Ustuner 2014). Targeted studies of mycorrhizal fungi could be a cost-effective option to solve these problems (Ortaş et al. 2017). In addition, profitability can be further increased by using AM fungi application to decrease fertilization without a decrease in yield (Chen et al. 2018).

2.9 Role of Subsoil AM Fungi in Sustainable Agriculture

AM fungal biomass abundance varies in the soil based on the soil depth and plant root length. AM fungi root colonization levels vary with soil depth. Almost half of AM fungi biomass is located below 30 cm (Higo et al. 2013). The AM fungi communities below 30 cm differ from the ones in topsoil both phylogenetically and morphologically (Säle et al. 2015). Growing evidence suggests that some AM fungal taxa are defined and limited by different soil layer characteristics (Sosa-Hernández et al. 2018b). According to a pot experiment with elevated CO2 levels performed by Rillig and Field (2003), there was no change in the AM fungi in the topsoil (up to 15 cm), while there was remarkable increase in AM fungi in the subsoil (about 15–45 cm soil layer), indicating that top and subsoil communities have differential reactions to above ground environmental variables. Evidence of AM colonization in deeper soil layers (4–8 m) was reported in many tree species such as honey mesquite (Virginia et al. 1986) Acacia, and Eucalyptus (de Araujo Pereira et al. 2018). Altogether, AM fungal associations of deeper layers are often overlooked, which are probably highly valuable for management and production improvement (Kour et al. 2020).

AM fungi communities in the subsoil are abundant and unique and contribute to better plant production and ecosystem services (Higo et al. 2013; Sosa-Hernández et al. 2018a). Reduced pore size, higher soil compaction, and lower oxygen availability make the subsoil different from topsoil (Lynch and Wojciechowski 2015). Subsoil AM fungi are expected to follow a high-stress resistance life cycle. As such, deeper soil AM fungi produce more long-lived hypha, as well as optimized resource use efficiency, representing an advantageous carbon cost/benefit investment for the plants. Plants may receive more benefits in return for every unit of carbon they provide for the AM fungi in the subsoil compared to that of topsoil. Subsoil AM fungi have a considerable role in soil formation (Leake and Read 2017) and weathering via various indirect mechanisms (Taylor et al. 2009). Deeper soil layers have lower biological activity, higher clay content and usually contain higher amounts of primary minerals with great potential for mineral weathering and nutrient availability.

AM fungi symbiosis expands the soil space that is reachable by their host root, which is known as the mycorrhizosphere (Linderman 1991), and this likely results in higher microbial activity in the subsoil. This alliance between the plant roots, AM fungi, and the associated soil microbial community has the potential to improve the soil structure, especially in shallow soils where the parent material or the bedrock is close to the root system.

2.10 Role of AM Fungi in Reforestation and Landscaping

Forest disturbances are created by human activities and make a dramatic change in the habitat, vegetation and soil. The disturbed habitats are usually described by aboveground and belowground diversity (Helgason et al. 1998). Utilization of AM fungi in reforestation and landscaping is a promising approach as the degraded and eroding lands can regain functionality with AM fungi. In arid regions, juvenile trees are vulnerable to stress conditions such as heat, drought and nutrient deficiency. With mycorrhizal associations, this critical phase can be overcome. An example is the mycorrhizal inoculation mediated increase in fitness and survival of young argan trees, which are considered endangered species in their original habitats due to excessive harvest (El Abbassi et al. 2014). Another approach by Ouahmane et al. (2007) was the inoculation of young cypress trees with a mixture of indigenous AM fungi, which were isolated from a natural site of C. atlantica, which increased the chances to form a symbiosis between AM fungi that is adapted to drought environments and the host plant.

AM fungi inoculation was a successful approach as it increased the growth and survival of these trees in the arid environment. AM fungi inoculation is in fact a suitable, sustainable and cost-effective approach in reforestation. AM symbiosis is considered to be a critical asset in preventing soil erosion, especially in sandy soil ecosystems (Moradi et al. 2017). The rhizosphere of mangroves species belonged to nine genera in the west coast of Goa yielded a variety of AM fungi (Sridhar 2005). Appropriate vegetation builds the ecosystem in favour of existence and interactions of flora, fauna and microbes. The costal ecosystem is a habitat for many inhabitants and provides food, fodder and bioactive compounds (Sridhar and Bhagya 2007).

2.11 AM Fungi Promote Bioremediation of Contaminated Soils

AM fungi act as a sequester of toxic compounds from the environment as a form of bioremediation. They prevent heavy metals from travelling past the plant roots (Rajkumar et al. 2012). Though heavy metals play a significant role in some biological cycles occurring in plants, but excess amount of these heavy metals can have adverse effects in plants. AM fungi can store the heavy metals in their vacuoles. In some cases, AM fungi increase the heavy metal tolerance of plants instead of decreasing the uptake of heavy metals by plants (Ferrol et al. 2016). Thus, AM fungi play an essential role in modulation of plant heavy metal accretion in different ecosystems, and they are considered a key factor in phytoremediation and micronutrient uptake by crops growing in polluted soils.

Heavy metal toxicity in plants results from the excessive uptake of elements from the polluted soil. The effect of AM fungi on plant growth and tolerance to heavy metals in a polluted soil depends on the fungal species, plant species and heavy metals involved in the consortium. Many case studies reported that the toxic effect by heavy metals decreased in plants mainly due to the reduction of their concentrations in the soil, which in turn resulted in higher uptake of P and the enhanced growth of mycorrhizal plants (Chen et al. 2003). However, plant growth improvement induced by the AM fungi symbiosis is not always related to the metal concentrations in plant tissues or in the soil. For example, a study carried out by Lingua et al. (2008) reports that Cu and Zn mitigation was found in white poplar trees colonized by R. irregularis or F. mosseae even when the metal concentrations was higher in the host plants. AM fungi often increase heavy metal accumulation in roots, but their effects on the heavy metal concentration in aboveground organs of host plants are not remarkable.

AM fungi have been reported to decrease Zn uptake and allocation of heavy metals in above and below ground organs of red clover and tomato when in symbiosis with AM fungi on Zn-polluted soils (Li and Christie 2001; Watts-Williams et al. 2013). AM fungi spores and their abundance in roots are lower in heavy metal contaminated soils than unpolluted soils. Usually, the native AM fungi of polluted environments are more resistant and efficient at improving heavy metal tolerance of plants compared to native AM fungi that are found in non-polluted areas. For example, the Rizhophagus irregularis Br1 ecotype isolated by Hildebrandt et al. (1999) from the soil under Viola calaminaria plants shown to be more effective in inducing heavy metal tolerance on a variety of plants (tomato, maize and M. truncatula) than an ecotype of the same species isolated from a non-contaminated soil (Kaldorf et al. 1999).

2.12 AM Fungi and Abiotic Stress Tolerance

AM fungi could alleviate plant’s response to different types of stresses or a combination of stresses that include salinity, drought, nutrients, heavy metals and temperature. Under stress conditions, reactive oxygen species (ROS) will be generated in host plants. Based on the severity, there will be an increase in ROS species, which in fact harmful to the metabolic activities of the plants (Bauddh and Singh 2012). The plants’ cellular mechanisms fight against the reactive oxygen species (ROS) by the production of several enzymes, superoxide dismutase (SOD), peroxidase (POD), catalase (CAT) and glutathione reductase (GR) (Ahanger and Agarwal 2017). Upon inoculation with AM fungi, the plant adaptability to stress get increased by processes such as increase in mineral nutrient uptake, improved photosynthetic rate and accumulation of osmoprotectants, increased antioxidant enzyme activity and manipulation in the rhizosphere ecosystem (Yin et al. 2016). A study by Duc and co-authors revealed that inoculation with Scolecobasidium constrictum in tomato plants which were set for a combined treatment of salinity and drought showed improvement in water uptake, stomatal conductance and biomass production compared to non-inoculated plants (Duc et al. 2018).

The AM fungi are capable of significantly enhancing plants’ tolerance to stress conditions and improve the plant growth and yield even under stress (Latef and Chaoxing 2014). Under stress conditions, AM fungi mediate alterations in the phytohormone level and up-regulate its antioxidant system. However, different mechanism of AM fungi action towards alleviating stress in plants depends on the stress type and the AM fungal species. For example, mechanisms such as production of phytochelatins, compartmentation and sequestration of toxic ions, and expression of stress proteins can be specific and show significant changes with AM species involved. The hydraulic conductivity changes occurring in the roots under salt stress can improve osmotic stress tolerance of the plant to a considerable level (Evelin et al. 2009). An investigation made by Zhang et al. (2018) shown that AM fungi made a remarkable influence in castor bean growing under saline condition by altering the levels of some essential plant metabolites and by altering the gas exchange traits. Thus, AM fungi offer a considerable importance in the production and management of different potential crops prone to stress conditions with high nutritional quality.

However, to achieve the benefits offered by AM fungi, an extensive study is necessary to unravel the role of AM fungi in neutralizing the effects of combined stresses.

2.13 Conclusion

AM fungi and their importance regarding plant growth, production and their effect on stress tolerance and nutrient uptake of their host have been studied during past decades. However, much remains to be investigated regarding their interaction with other root-colonizing microorganisms (e.g. endophytes) and the natural soil microbiome. Habitat adaptation and co-evolution with the host plant certainly need more attention from the scientists. Identifying the specific AM fungal species which have adapted to environmental stress in different habitats might be of value regarding agricultural production, especially under salt and drought stress, as well as poor soils. AM fungi contribute a major role in carbon sequestration through various mechanisms. But a thorough investigation is needed to study the mechanism of AM fungi-associated links between C fluxes in soil and the nutrient exchange to the host plants. AM fungi inoculation has shown to enhance crop productivity in many agriculture crop varieties. AM fungi inoculated alone or in combination with other microbial inoculants such as PGPR also help in alleviating plants against different stress conditions. In order to have better crop productivity, it is necessary to understand the AM fungi mediated cellular modulations in the tolerance mechanisms and the phenomenon by which the signals are transmitted to regulate plant performance. In order to promote sustainable agriculture, the use of synthetic fertilizers needs to be replaced with AM fungi inoculants which in fact recover the soil fertility and increase the crop productivity through its beneficial functions. Thus, the multiple benefits offered by AM fungi decipher its significant services in natural ecosystem as well as in sustainable agriculture.