Review Article | Volume 10, Issue 6, November, 2022

Implications of abiotic stress tolerance in arbuscular mycorrhiza colonized plants: Importance in plant growth and regulation

Madhulika Singh Sanskriti Bisht Shatrupa Singh Jai Gopal Sharma   

Open Access   

Published:  Sep 20, 2022

DOI: 10.7324/JABB.2022.100601
Abstract

Arbuscular mycorrhizal fungi (AMF) are crucial for the growth and development of most terrestrial plants, enabling them to withstand abiotic stresses. Abiotic stress such as salinity, drought, extreme temperature, heavy metals, and carbon dioxide hampers plant growth. Abiotic stresses are being elevated because of abrupt climatic changes and agricultural malpractices such as excessive fertilizer and pesticide use, which is also hazardous for human consumption. To cope with the adverse effects, we need a reliable system that can monitor and control all these deleterious effects on plants, and AMF is one of the appropriate methods to create a sustainable platform for agriculture. Mycorrhizal symbionts grow together with the roots of higher plants, aiding them in the uptake of minerals and nutrients, which results in improved plant growth and yield even under stressed conditions. In return, these symbionts receive carbohydrates for the completion of their lifecycle. The role of AMF, as a bio-fertilizer, can strengthen the quality of crop plants, by elevating soil health and enhancing ecosystem stability. In this review, we will investigate how different abiotic stress factors can negatively affect plant growth, the role of AMF in controlling those stresses, its impact and effect on plant growth and yield, its use as a bio-fertilizer in agricultural fields, and its interaction with other organisms.


Keyword:     Arbuscular mycorrhizal fungi Abiotic stress Plant growth Stress tolerance Biofertilizer


Citation:

Singh M, Bisht S, Sharma JG, Singh S. Implications of abiotic stress tolerance in arbuscular mycorrhiza colonized plants: Importance in plant growth and regulation. J App Biol Biotech.2022;10(6):1-11. https://doi.org/10.7324/JABB.2022.100601

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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1. INTRODUCTION

Many abiotic stresses, such as salinity, drought, extreme temperatures, heavy metals, and excessive fertilizer and pesticide use, have contributed to soil degradation, and today, they pose a threat to agriculture, as they are responsible for most of the crop and yield losses globally [1]. Fortunately, several microorganisms, particularly bacteria and fungi, can counteract the negative effects of environmental stresses, thereby monitoring the plants’ performance during stressful conditions [2].

One of them is AMF, a member of the subphylum Glomeromycota, which includes three classes (Glomeromycetes, Archaeosporomycetes, and Paraglomeromycetes) in the phylum Mucoromycota. So far, this subphylum has been classified into four orders and 25 genera, containing about 250 species [3]. Glomeromycota depends on plants for carbon substrate to survive. In return, the symbiont provides an abundance of minerals and nutrients to the host plants, such as nitrogen, phosphorus, and potassium through an intraradical network of hyphae and arbuscules, and the root apoplast interface. In addition, AMF improves the quality of the soil since fungal hyphae accelerate decomposition much earlier, thus improving soil quality [4].

The AMF establishes symbiotic relationships with the roots of most of the terrestrial plants, including 80−90% of the vascular plants, and 90% of the agricultural plants [5], such as cereals, vegetables, and horticultural plants. The application of AMF has been found to increase plant growth and regulation by enhancing nutrient uptake and stress tolerance. Considering the research and development associated with AMF in agriculture, the present review aims to present an overview of the current knowledge on the relationship between AMF and host plants in regulation and development, improved nutrient uptake even under stress conditions, and the emergence of AMF as biofertilizers.


2. FEATURES OF AMF SYMBIOSIS

According to molecular data and fossil evidence, the symbiosis dates back to 400−450 million years ago [5] around the time land plants first appeared. Through the succession of biological processes, such links can result in a variety of beneficial effects in natural ecosystems. One of the examples of a mutualistic relationship is the symbiotic associations of mycorrhizal symbionts and the roots of higher terrestrial plants [Figure 1]. A hyphal network extends beneath the roots and enhances the uptake of nutrients and minerals by the host plants.

Figure 1: An overview of some of the mycorrhizal functions that regulate plant growth and development during abiotic stress.



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The mycelium of fungi colonizes the roots of a wide range of plants, even if they are from different species, producing a common mycorrhizal network (CMN). CMN is a critical component of the terrestrial ecosystem, affecting a wide range of plant communities, including invasive species [6], as well as the supply of nitrogen (N) and phosphorus (P) to plants through fungal symbionts [7]. It also increases the quality of the soil and its aggregation and allows host plants to grow even in the most stressed conditions.

AMF is considered a bio-inoculant, and scientists are continually promoting its usage as a leading bio-fertilizer for long-term agricultural production and development [8]. The soil protein Glomalin-related soil protein (GRSP) is thought to maintain the water content of the soil during abiotic stress [9], which then regulates the total water frequency between soil and plants, resulting in higher plant growth and development. AMF inoculation had an effect on other parameters related to growth, including relative water content (RWC), leaf water potential, stomatal conductivity, PSII efficiency, and carbon dioxide uptake [10].

Studies have shown that AMF affects plant growth and physiological elements in a wide range of species, including Solanum Lycopersicum [11], Sorghum bicolor [12], Cucurbita maxima [13], and Withania somnifera [14]. It also contributes to 20% of total plant uptake [15], emphasizing the role of symbiosis in maintaining adequate water levels in the host plant. The inoculation of the fungus increases plant growth as well as the contents of various phytochemicals, such as flavonoids, tannins, phenols, and sugars.


3. DIFFERENT ROLES OF AMF

3.1. An AMF-based Bio-fertilizer

As bio-fertilizers, these materials contain a mixture of natural ingredients, called microorganisms, used to improve the fertility and quality of the soil. Besides being very useful for improving the soil’s health, these fertilizers also help plants to grow and develop [16]. Numerous studies have shown the benefits of AMF on soil health and crop productivity. Thus, AMF is thought of as a biological tool that can be used to fight the problems regarding crop yield and productivity, hence, is a good substitute for inorganic fertilizers in the near future, fostering organic farming and sustainable agriculture [17]. Mycorrhizal symbionts are effective at reducing the quantitative use of chemical fertilizers, especially phosphorus.

Continuous use of inorganic fertilizers, pesticides, and fungicides has drastically caused havoc to the soil environment, leading to the infertility of soil and also associated with the risk of human health and life [18]. AMF is thought to reduce inorganic chemical use up to 50% for agricultural production; however, the reduced use depends on the species of plants and the stress regime.


3.2. AMF in Enhancing Mineral Nutrition

AMF transfers nutrients to plants, like inorganic carbon as sugars and lipids [19]. It is widely believed that AMF colonization stimulates plant nutrition uptake [Figure 2]. Increased biomass accumulation and photosynthate production are evident by inoculating AMF with host species, as it increases the concentration of various micronutrients and macronutrients [20]. Additionally, to macronutrients, the AMF association is reported to increase the phytoavailability of micronutrients copper and zinc. To obtain nutrients from the roots of host plants, AMF forms symbiotic relationships with them, providing minerals such as phosphorus, potassium, calcium, nitrogen, zinc, and sulfur. AMF have structures called arbuscules, which aid in the exchange of inorganic minerals, carbon compounds, and phosphorous compounds, enhancing plant growth [21]. Thus, they improve the concentration of phosphorous in both root and shoot systems. Nitrogen is the major source of nutrients required by plants for growth and development, AMF inoculation helps in the absorption and transfer of nitrogen to nearby plants [21]. There is wide acceptance of the fact that decomposed and dead matter can supply fungi with a considerable amount of nitrogen which, in the future, can improve their ability to grow and live. Nitrogen is effectively trapped by chlorophyll molecules in plants colonized by AMF, which results in higher chlorophyll content [22]. AMF mediated improvement in N content of host plants have several pieces of evidence in the literature.

Figure 2: A diagrammatic representation contrasting the differences of the plants inoculated with mycorrhizal and non-mycorrhizal association.



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3.3. AMF in Increasing the Plant Yield with Inoculation

The nutrient status of the crops is not only improved by beneficial microorganisms, but they also contribute to the enhancement of the crop quality and yield. AMF also affects the production of carotenoids and other volatile compounds, associated with an enhancement in the dietary quality of crops [23]. Increased content of Vitamin C, other organic acids, sugars, minerals, and flavonoids occurs due to the AMF colonization resulting in the improved quality of citrus fruits [24]. Accumulation of carotenoids, anthocyanin, tocopherol, phenolic compounds, chlorophyll, and various other mineral nutrients [Figure 3] is enhanced by mycorrhizal symbiosis [25]. Large-scale field production of maize, yam, and potato has been done by the progressive use of AMF in the agricultural fields, confirming the potential value of AMF for increasing the plant yield. In addition, AMF increases the biosynthesis of beneficial phytochemicals. AMF inoculation maintains the pH of the soil, protecting the horticultural value [26].

Figure 3: Summarized details have been provided in the diagram below, which shows list of various Molecular and Biochemical responses shown by AMF inoculated host plants, under various abiotic stresses.



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3.4. AMF and Various Abiotic Stresses

3.4.1. Drought

Stresses such as drought affect plant life in a negative way. Plant development is drastically reduced as shortage of water provokes a reduction in the rate of transpiration, oxidative stress, the closure of stomata, with subsequent reduction in the influx of CO2, causing a reduction in the overall rate of photosynthesis, plant productivity, carbon partitioning, and overall, a clear-cut reduction of the agricultural yield, dropping its core value.

A drought increases oxidative stress and reduces transpiration [27,28]. Drought stress causes deleterious effects on the overall plant growth and productivity, by affecting several functions, such as nutrient assimilation, uptake of ions, and enzymatic activity [29]. However, strong evidence shows that drought stress is minimized by AMF inoculation in several crops such as strawberry, barley, onion, wheat, and soybean [30-33]. The extra radical network of hyphae in fungi helps in tolerance against drought in plants, and another primary reason is that large volumes of soil are explored by the hyphal network [34-37].

Symbiotic association of mycorrhiza and plants is believed to control the variety of physio-biochemical processes like increase in the osmotic adjustment [38], ABA metabolism controls the stomatal regulation [39], increase in the accumulation of proline contents [40,41], and glutathione levels are also increased [42]. Furthermore, a symbiotic association of plants with AMF improves the leaf area index, size of the root, and its efficiency and biomass under an instant drought environment [43].

Moreover, AMF and its relationship with host plants are quite helpful and supportive in shielding against unfavorable conditions [31]. AMF association enhances gaseous exchange, transpiration, stomatal conductance, and enhanced leaf water relations [30]. In addition, it assists in regulating stomatal conductivity and other physiological processes [44].

AMF inoculation provides resistance against unfavorable conditions like drought, by increasing the radical hyphae-like structures in the soil and improving the performance of plants even under stressful conditions. Different effects of AMF inoculation with host plants, under drought conditions, ions have been mentioned in [Table 1] [45-48]. Mycorrhizal symbionts deal with water deficit through drought tolerance and drought mitigation mechanisms.

Table 1: Beneficial role of AMF inoculation in host plants, under drought conditions.

Host plantsFungal speciesAMF inoculations - responsesReferences
Olea europaeaAMFDrought impact is mitigated, turgor potential and mineral uptake are maximized[45]
Glycine maxAMFEnhancement in a leaf area index, increased rate of photosynthesis, increased growth rate and dry weight of seeds[46]
Digitaria erianthaRhizophagus irregularisEnhanced stomatal conductivity, peroxidation of lipids and shoot dry matter[47]
Triticum aestivumGlomus mosseaIncrease in the chlorophyll content, osmotic potential, rise in the enzymes linked to antioxidant activities and contents of N, P and K[42]
Allium cepaGlomus etunicatusHigher fresh and dry biomass and phosphorus content[48]

3.4.2. Salinity

Salinization of soils is a major alarming environmental concern, raising concerns for global food security. The growth of the plant is suppressed by the salinity stress, affecting the total vegetative development and assimilation. There is evidence that AMF is naturally present in saline conditions, and that it provides tolerance to salinity in plants that have been inoculated with it. The contribution of AMF resisting salinity stress involves several parameters such as physiological, biochemical, and nutritional effects. Salinity stress inhibits plant growth and productivity by affecting the number of parameters like assimilation rate is reduced resulting in the low yield productivity [28,49]. Reactive oxygen species are generated in high numbers [29,50] Various attempts are made to explore the methods used to enhance crop production even under stressful saline conditions. The use of AMF judiciously is one way we find to mitigate the damages caused by salinity [51]. Various studies have revealed that plant productivity is enhanced by AMF under stressful conditions [52,53].

Nashar (2017) [54] has reported that leaf water potential, growth rate, and water-use efficiency are enhanced in great snapdragon plants. Under saline conditions, AMF increases stomatal conductance, leaf water relations, and photosynthetic rate [55]. AMF inoculation improves gaseous exchange, photosynthetic rate, chlorophyll contents, and efficient utilization of water in Ocimum basilicum during salinity stress [56]. Wang et al. (2018) [57] reported enhanced dry and fresh weights, N concentration in roots, and shoots during salt stress when inoculated with AMF. Furthermore, plants inoculated with AMF show much synthesis of hormones such as salicylic and jasmonic acid, and other inorganic minerals. Mycorrhizal inoculation with lettuce plant shows an increase in biomass production, increase in the uptake of N, high synthesis of proline, changes in ionic relations specifically decrease in the accumulation of Na+ with contrast to non-mycorrhizal plant, under-stressed environment [51]. In addition, plant growth mediated via AMF promotes the alteration in the pool of polyamine [58]. AMF inoculated lettuce plants showed an increase in strigolactone content mitigating effects of salt stress [59]. Among the mechanisms that contribute to salinity tolerance are ionic homeostasis, accumulation of osmoregulatory such as sugars, and reduction in the Na and Cl uptake. [Table 2] summarizes the tolerance of salt stress in different plant species when inoculated with AMF [60-64].

Table 2: Salinity tolerance in plant inoculated with AMF.

Host plantsFungal speciesAMF inoculations - responsesReferences
Solanum lycopersicumGlomus intraradicesIon uptake, chlorophyll content, growth parameters and dry matter is improved[60]
Solanum lycopersicumRhizophagus irregularisShoot, root, area of leaf, leaf number and the growth hormone content are enhanced[61]
Aeluropus littoralisClaroideoglomus etunicatumStomatal conductance, root and shoot dry biomass, free alpha amino acids, soluble sugars and Na and Cl uptake is increased[62]
Acacia niloticaGlomus fasciculateShoot and Root dry weight are improved along with Zn, Cu and P contents[63]
Cucumis sativusGlomus mosseae, Glomus etunicatum, Glomus intraradicesBiomass is increased, Biosynthesis of antioxidant enzymes and photosynthetic pigments[64]

3.4.3. Extreme temperature

Loss of plant vigor, retardation in the growth rate, senescence, discoloration of fruit, yield reduction, and decreased biomass production are the causes of heat stress, fluctuations in the temperature, or extreme temperature. Temperature stress is among the most important factors, which negatively impact the productivity of the plants [65]. AMF improves the performance of plants to tolerate the vivid temperature by improving photosynthetic efficacy [Table 3], shields plants from severe oxidative stress, and increases the osmolytes content [66]. During salinity stress, shoot and dry root biomass inoculated with mycorrhiza showed higher numbers as compared with non-mycorrhizal association [67]. AMF develops the root system for water absorption in plants at higher temperatures to increase photosynthetic rate and prevention of photosynthetic units from damage [68]. The study of Hajiboland et al. (2019) [69] pointed out that G. versiforme was significantly better at minimizing the cold stress experienced during winter and spring than R. irregularis. The inoculation of the Barley (Hordeum vulgare) with AMF increased the number of parameters such as osmotic homeostasis, plant growth, photosynthesis, and potassium uptake [69].

Table 3: Physiological response of plants related to AMF inoculation.

Host plantsFungal species AMF inoculations - responsesReferences
Hordeum vulgareR. irregularis G. versiformeSurvival rate is increased and alleviation of low temperature stress[69]
Zea maysFunneliformis (Glomus) species.Controlled photosystem (PS) II heterogeneity[68]
Cucumis sativusR. irregularisIncreased photosynthetic rate of cucumber seedlings subjected to cold stress[71]
Elymus nutansF. mosseaePromotes the plant growth with less oxidative damage, the antioxidant and chlorophyll levels are enhanced.[72]

AMF plays a very crucial role in tolerating a vivid range of temperatures (high and low), mitigation of climate change [70]. It also improves the N uptake and its assimilation by reducing the emission of N2O. However, too many fluctuations in the temperature, climatic, and seasonal changes can affect the communities of AMF [71,72].


3.4.4. Heavy metals

In soil contaminated with heavy metals, AMF can establish a plant community because it enhances the defense system of inoculated plants, thereby promoting plant growth and development. Heavy metals are found in soils that are contaminated by mining or polluted sites, which contain AMF that are adapted to soil pollution. A number of studies have shown that around 80% of plants growing on or near mining sites are infested with AMF. Heavy metals can accumulate in various fruits, crop plants, vegetables, and soil posing a threat and causing a wide range of health problems [73,74]. In the soil where cadmium and zinc are quite abundant, suppresses root and shoot growth, results in leaf chlorosis, and even kills plants [75]. A fungal hypha of external and internal origin [76] can immobilize the heavy metals in the cell wall, storing some of them in vacuoles, or chelating them with substances in the cytoplasm [77] and reducing their toxicity significantly in plants. Chelation or enhanced growth in the soil of rhizospheric origin can cause the dilution of metals in plant cells and tissues [58,78]. AMF also binds to the Zn and Cd, in the cell walls of cortical cells and mantle hyphae, thereby, refraining from the excessive uptake of these minerals and improving the entire nutrient status of plants [79,80]. Uptake of several heavy metals by plants and subsequent movement from roots to the aerial parts are highly disturbed by mycorrhiza symbiosis [81,82]. Mycelia of many strains of AMF have a high cation exchange capacity and can absorb heavy metals [83]. AMF regulates the uptake of important inorganic minerals [Table 4], such as higher uptake of silicon has been reported in Zea Mays [84] and Glycine max [85]. Hammer et al. (2011) [86] has recorded that hyphae and spores of Rhizophagus irregularis have seen a considerable uptake in Si amounts. AMF inoculation increased cadmium tolerance in alfalfa species [87]. Bioremediation by AMF occurs by the dense hyphal network which binds heavy metals. Heavy metal toxicity is solely affected by the type of mycorrhizal association and the type of plant. Inoculation with AMF has been shown to enhance germination of seeds, plant growth, fresh, and dry weight [88-92].

Table 4: Responses of host plants related to AMF inoculation.

Host plantsFungal species AMF inoculations - responsesReferences
Zea maysGlomus isolatesEnhanced production of Mg, P and K are increased, improved dry weight and distinction in the distribution of essential and heavy metals in cells[88]
Trigonella foenum- graceumF. mosseaeImproves the plant growth and yield[89]
Lonicera japonicaG. versiformeCd content is reduced in roots and shoots[90]
Populus alba Populus nigraR. irregularis or F. mosseaeAlleviation in the Zn and Cu phytotoxicity[91]
Trifolium pratenseGlomus mosseaeRoot and Shoot concentrations are decreased along with reduction in Zn uptake[92]

3.4.5. Flooding tolerance

AMF no matter is a wonder provides resistance to several abiotic stresses. Furthermore, some AMF is capable of facing and tolerating other constraints such as flood [93]. A high diversity of AMF is found in the wetland systems, beneficial against flooding stress [94]. AMF in such abrupt conditions improves plant growth through the absorption of various minerals and nutrients [95]. The authors listed in [Table 5] have found that under wetland conditions, some phosphorous was transported through the mycorrhizal pathway to the rice plants. Liang et al. (2018) [96] reported that AMF may help Phragmites australis in resisting adverse changes. Fougnies et al. (2006) [97] reported that Pterocarpus officinalis contributes to resisting flood tolerance. The better growth of host plants with mycorrhizal inoculation with a condition like flooding stress can be combated with osmotic adjustment improvement [98]. Another study was conducted by Rodriguez et al. (2020) [99] which had indicated that AMF distributions in tropical low flooding forests are directly related to vegetation characteristics and soil parameters [100].

Table 5: Responses of host plants related to AMF inoculation.

Host plantsFungal species AMF inoculations - responsesReferences
Panicum hemitomon Leersia hexandraAcaulospora trappei, Glomus leptotichum, Scutellospora heterogama, A Acaulospora laevis, Glomus leptotichum, G. etunicatum and G. gerdemanniiEnhanced phosphorus content in plants[100]
Pterocarpus officinalisGlomus intraradicesHigher plant growth and phosphorus content in leaves[97]
Aster tripoliumGlomus geosporumHigher sugars and proline content[99]

3.5. Role of AMF in Combined Abiotic Stresses

AMF is believed to be capable of alleviating various abiotic stresses as well as the combinations of similar stresses including drought, salinity, extreme heat, heavy metals, and flooding tolerance. Such as if plants are subjected to stressful environments like salinity and drought higher amounts of ROS are generated which are injurious for the plant life [101]. Enzymes such as peroxidase (POD), catalase (CAT), superoxide dismutase (SOD), and glutathione reductase (GR) help in the detoxification of a higher amount of ROS produced by plants subjected to stressful conditions [29]. Under stress conditions such as salinity and drought, tomato plants inoculated with Scolecobasidium constrictum show improved stomatal conductance, biomass production, leaf water relation, and Fv/Fm ratios than those without mycorrhizae. Thus, AMF helps in improving plant yield and growth [67]. Few research reports are found which tell about mitigation of combined effects of more than two stresses in AMF. AMF inoculation shields plants against several abiotic stresses using parameters such as accumulation and uptake of mineral nutrients, regulation of anti-oxidant enzymatic activity, changes in the ecosystem of the rhizosphere, and increased photosynthetic rate [102-104]. There have been a number of studies showing that AMF inoculated plants have improved in nutritional status even under stressful conditions [105-107] caused by the irrigation system or salinity levels. Similarities have been found in the tolerance mechanism which occurs in response due to the combined stress adaptations in the AMF mediated plants. Furthermore, nutrient uptake and assimilation, accumulation of osmolytes, and the anti-oxidant system are some of the common mechanisms that occur under different stressful cues. Specific mechanisms such as sequestration and compartmentation of toxic ions, excessive generation of phytochelatins, and protein can be species-specific, display changes during different stress conditions. The characteristics of roots like hydraulic conductivity may alleviate the osmotic stress to some levels [108]. Zhang et al. (2018) [109] have reported that castor bean is protected by AMF against salinity, by making changes in the gas exchange property and some specific metabolites. The above characteristics of AMF may lead to the enhancement of nutraceutical crop quality and could lead to its application in large-scale agricultural production. But still, a lot of research is required to unravel the AMF’s role in combating the combined abiotic stresses.


3.6. Association of AMF with Important Soil Microbes

AMF plays an important role in laying establishment with a wide range of soil microorganisms [110,111]. Interactions between the associations can be either positive, negative, or neutral depending on the type of AMF strain and microbes in the rhizosphere [112-115]. In addition, it helps to acquire nutrients, control root pathogens, and improve plant resilience to stress [116].

3.6.1. AMF and rhizobia interaction

Rhizobia are the nitrogen-fixing bacteria that provide all essential minerals and nutrients to the plants, together with AMF inoculation, excellent synergistic effects are seen. A lot of experiments have been conducted in the past which shows positive effects in the interaction of AMF and nodulating Rhizobium [117]. Several reports have shown that interaction between rhizobia and AMF have beneficial effects in legume plants such as Glycine max [98,118], Amorpha canescens, Lens culinaris [119,120], Pisum sativum [121], Lathyrus sativus [122], and Vicia faba [123]. All these interactions modify the environment of microbes through secretions [124]. It was demonstrated by Chatarpaul et al. (1989) [124] that Faba beans grow very well in alkaline soil when AMF and rhizobium are inoculated concurrently.


3.6.2. AMF and Frankia interaction

Actinorhizal plant performance is improved by Frankia in the different environments [35,125-130]. In Casuarina equisetifolia and Casuarina cunninghamiana, dual inoculation with Frankia and mycorrhizal fungi, enhance the trees and seedlings height, depending on the availability of phosphorous contents. Dual inoculation of Rhizophagus intraradices and Frankia spp. with plants of Black alder, in highly anthropogenic alkaline sediment, increases the shoot length, P and N contents of leaf, overall biomass, and leaf area when compared with another control which was uninoculated the Rhizophagus intraradices and Frankia spp. treatments alone [126]. In addition to this, dual inoculation increased the symbiosis of AMF, indicating a synergistic effect demonstrated by a high number of nodules in dry weight and a high degree of root development. Although a lot of study and research says that not always a relationship between AMF and Frankia yields good results, sometimes it may be negative [125].


3.6.3. Tripartite symbiosis and its beneficiaries

A lot of benefits have been known about tripartite symbiosis (nitrogen fixers, plant growth-promoting rhizobacteria or mycorrhizal fungi, and AMF) by a lot of researchers [131-133]. Rajendran and Devaraj (2004) [131] found that inoculating C. equisetifolia plants with AMF, Azospirillum, Frankia, and Phosphobacterium increased the overall height and biomass.

AMF also co-exists with EMF which is Ectomycorrhizal fungi that enhance plant growth [131,134]. There is no simultaneous colonization of AMF and EMF. In general, the colonization of AMF is first, followed by the EMF, but it is much less, as EMF establishes itself first, further reducing the colonization of AMF by forming a mantle that prevents infection. However, if AMF establishes itself first, it shows no deleterious effects on infection by EMF [134]. According to Emumalai and Raaman (2009) [135], inoculating C. equisetifolia plants with both AMF and EMF increases the phosphorous content and biomass compared to inoculating them with either one of them.


3.6.4. Mycorrhization helper bacteria and its interaction with AMF

Interaction of AMF with Mycorrhization Helper Bacteria (MHB) is positive [136-138]. Due to bacterial effects that are beneficial to mycorrhizal associations, Mycorrhization Helper Bacteria (MHB) concept was developed. MHB and its five possible actions were proposed by [138] on the mycorrhizal association like proper receptivity between root and its mycobiont, recognition of root and fungus, modifications in the soil of rhizospheric nature, growth and germination of propagules of fungus. MHB is fungus-specific and not plant-specific; the study was shown by the authors mentioned above.



4. CONCLUSION AND FUTURE PERSPECTIVES

Numerous research reports have demonstrated that AMF inoculation improves many plant attributes, including the growth and development of the plant under the most stressful conditions. Consequently, this review highlights current information about AMF in a coherent manner to gain a better understanding of how AMF interacts with a large number of plants in unfavorable conditions. The AMF is known to act as one of the beneficial elements in mineral uptake from the soil. Furthermore, AMF plays an important role in the alleviation of a number of different environmental stress factors on plants such as drought, salinity, temperature extremes, heavy metals, and flooding. These factors thereby provide an increase in the yield per hectare of many vegetables and crops. AMF is a potential tool to restore the degraded ecosystem. It is considered one of the key indicators for detecting soil pollution. They play a crucial role in increasing the yield and plant growth, tolerance against hazardous compounds, which can be toxic and lethal for human life, and subsequent growth. An alternative approach of switching to AMF inoculation can provide an environment-friendly solution to reduce the excessive use of pesticides and industrial fertilizers. The application of this knowledge should be implemented on a wide scale, to boost organic farming and sustainable development. Industrial production of AMF is to be done at a large scale to ensure that there is no lack of food availability and food scarcity. Isolation of indigenous AMF which are adapted to stressful conditions can be proved as one of the potential biotechnological tools to combat the problems of stresses in plants and for the excellent restoration of the degraded ecosystems. Screening of such indigenous and pollution tolerant isolates should be done effectively to provide beneficiaries of the mycorrhizal symbiotic association, for the restoration of the contaminated soils. In addition, combining selected plants with particular AMF which are adaptable to the various stress cues is the subject of research in agricultural farming in order to increase the use of organic manures. New methods and mechanisms should be followed and encouraged to boost up this entire process which is quite a good subject to combat the problems of environmental stress. People should be encouraged to adopt this method, which is quite affordable and accessible. Consistent sustainability can occur only by much encouragement given to the AMF usage throughout at global level. The exploitation of AMF will lower the dependence on inorganic chemicals, fertilizers, and pesticides, promoting healthy sustainable development and the environment. Environment-friendly technologies should be given a chance to represent and address the critical issues, and thereby coming up with a solution, is one of the healthy approaches to address this issue and solve it. Future research should primarily focus on some objective of identifying genes and gene products that directly control AMF symbiosis and regulate plant growth under stressful cues.


5. AUTHORS’ CONTRIBUTIONS

All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agreed to be accountable for all aspects of the work. All the authors are eligible to be an author as per the International Committee of Medical Journal Editors (ICMJE) requirements/guidelines.


6. FUNDING

There is no funding for this research.


7. CONFLICTS OF INTEREST

The authors report no financial or any other conflicts of interest in this work.


8. ETHICAL APPROVALS

This study does not involve experiments on animals or human subjects.


9. DATA AVAILABILITY

All data generated and analyzed are included within this research article.


10. PUBLISHER’S NOTE

This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.


REFERENCES

1. Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures:Towards genetic engineering for stress tolerance. Planta 2003;218:1-14. [CrossRef]

2. Gary H, Ram K, Doni F, Norman U. Benefits to plant health and productivity from enhancing plant microbial symbionts. Front Plant Sci 2021;11:2001. [CrossRef]

3. Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 2016;108:1028-46. [CrossRef]

4. Parniske M. Arbuscular mycorrhiza:The mother of plant root endosymbioses. Nat Rev Microbiol 2008;6:763-75. [CrossRef]

5. Smith SE, Read DJ. Mycorrhizal Symbiosis. Cambridge, MA:Academic Press;2010.

6. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN. Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 2009;40:699-715. [CrossRef]

7. Smith S, Read D. Mycorrhiza Symbiosis. 3rd ed. San Diego:Academic Press;2008.

8. Barrow CJ. Biochar potential for countering land degradation and for improving agriculture. Appl Geogr 2012;34:21-8. [CrossRef]

9. Wu Z, McGrouther K, Huang J, Wu P, Wu W, Wang H. Decomposition and the contribution of glomalin-related soil protein (GRSP) in heavy metal sequestration:Field experiment. Soil Biol Biochem 2014;68:283-90. [CrossRef]

10. Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T. Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress a meta-analysis. Front Plant Sci 2019;10:457. [CrossRef]

11. Bona E, Cantamessa S, Massa N, Manassero P, Marsano F, Copetta A, et al. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato:A field study. Mycorrhiza 2017;27:1-11. [CrossRef]

12. Nakmee PS, Techapinyawat S, Ngamprasit S. Comparative potentials of native arbuscular mycorrhizal fungi to improve nutrient uptake and biomass of Sorghum bicolor Linn. Agric Nat Resour 2016;50:173-8. [CrossRef]

13. Al-Hmoud G, Al-Momany A. Effect of four mycorrhizal products on squash plant growth and its effect on physiological plant elements. Adv Crop Sci Technol 2017;5:260.

14. Parihar P, Bora M. Effect of mycorrhiza (Glomus mosseae) on morphological and biochemical properties of Ashwagandha (Withania somnifera) (L.) Dunal. J Appl Natl Sci 2018;10:1115-23. [CrossRef]

15. Ruth B, Khalvati M, Schmidhalter U. Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 2011;342:459-68. [CrossRef]

16. Sadhana B. Arbuscular mycorrhizal fungi (AMF) as a biofertilizers a review. Int J Curr Microbiol Appl Sci 2014;3:384-400.

17. Ortas I. The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions. Field Crops Res 2012;125:35-48. [CrossRef]

18. Yang S, Li F, Malhi SS, Wang P, Suo D, Wang J. Long-term fertilization effects on crop yield and nitrate nitrogen accumulation in soil in Northwestern China. Agron J 2004;96:1039-49. [CrossRef]

19. Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, et al. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 2017;356:1175-8. [CrossRef]

20. Mitra D, Navendra U, Panneerselvam U, Ansuman S, Ganeshamurthy AN, Divya J. Role of mycorrhiza and its associated bacteria on plant growth promotion and nutrient management in sustainable agriculture. Int J Life Sci Appl Sci 2019;1:1-10.

21. Prasad R, Bhola D, Akdi K, Cruz C, Sairam KV, Tuteja N, et al. Introduction to mycorrhiza:Historical development. In:Varma A, Prasad R, Tuteja N, editors. Mycorrhiza. Cham:Springer;2017. 1-11. [CrossRef]

22. De Andrade SA, Domingues AP, Mazzafera P. Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere 2015;134:141-9. [CrossRef]

23. Hart M, Ehret DL, Krumbein A, Leung C, Murch S, Turi C, et al. Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza 2015;25:359-76. [CrossRef]

24. Zeng L, JianFu L, JianFu L, MingYuan W. Effects of arbuscular mycorrhizal (AM) fungi on citrus quality under nature conditions. Southwest China J Agric Sci 2014;27:2101-5.

25. Baslam M, Garmendia I, Goicoechea N. Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse grown lettuce. J Agric Food Chem 2011;59:5504-15. [CrossRef]

26. Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, et al. Arbuscular mycorrhizal fungi act as bio-stimulants in horticultural crops. Sci Hortic 2015;196:91-108. [CrossRef]

27. Impa SM, Nadaradjan S, Jagadish SV. Drought stress induced reactive oxygen species and anti-oxidants in plants. In:Ahmad P, Prasad MN, editors. Abiotic Stress Responses in Plants:Metabolism, Productivity and Sustainability. Berlin:Springer Science and Business Media;2012. 131-47. [CrossRef]

28. Hasanuzzaman M, Gill SS, Fujita M. Physiological role of nitric oxide in plants grown under adverse environmental conditions. In:Tuteja N, Gill SS, editors. Plant Acclimation to Environmental Stress. New York:Springer Science Business Media;2013. 269-322. [CrossRef]

29. Ahanger MA, Agarwal RM. Potassium up-regulates antioxidant metabolism and alleviates growth inhibition under water and osmotic stress in wheat (Triticum aestivum L.). Protoplasma 2017;254:1471-86. [CrossRef]

30. Mena-Violante HG, Ocampo-Jiménez O, Dendooven L, Martínez-Soto G, González-Castañeda J, Davies FT, et al. Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv S. Luis) plants exposed to drought. Mycorrhiza 2006;16:261-7. [CrossRef]

31. Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R, et al. Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 2016;39:441-52. [CrossRef]

32. Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-Um S. Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 2016;198:107-17. [CrossRef]

33. Moradtalab N, Hajiboland R, Aliasgharzad N, Hartmann TE, Neumann G. Silicon and the association with an arbuscular-mycorrhizal fungus (Rhizophagus clarus) mitigate the adverse effects of drought stress on strawberry. Agronomy 2019;9:41. [CrossRef]

34. Gianinazzi S, Gollotte A, Binet MN, Van Tuinen D, Redecker D, Wipf D. Agroecology:The key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 2010;20:519-30. [CrossRef]

35. Orfanoudakis M, Wheeler CT, Hooker JE. Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 2010;20:117-26. [CrossRef]

36. Gutjahr C, Paszkowski U. Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Front Plant Sci 2013;4:204. [CrossRef]

37. Zhang X, Li W, Fang M, Jixian Y, Meng S. Effects of arbuscular mycorrhizal fungi inoculation on carbon and nitrogen distribution and grain yield and nutritional quality in rice (Oryza sativa L.). J Sci Food Agric 2016;97:2919-25. [CrossRef]

38. Kubikova E, Jennifer LM, Bonnie HO, Michael DM, AugéMR. Mycorrhizal impact on osmotic adjustment in Ocimum basilicum during a lethal drying episode. J Plant Physiol 2001;158:1227-30. [CrossRef]

39. Duan X, Neuman DS, Reiber JM, Green CD, Saxton AM, AugéRM. Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 1996;47:1541-50. [CrossRef]

40. Ruiz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM. The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 2010;167:862-9. [CrossRef]

41. Yooyongwech S, Phaukinsang N, Cha-Um S, Supaibulwatana K. Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regul 2013;69:285-93. [CrossRef]

42. Rani B. Effect of Arbuscular Mycorrhiza Fungi on Biochemical Parameters in Wheat Triticum aestivum L. under Drought Conditions [Doctoral Dissertation]. Hisar, India:CCSHAU;2016.

43. Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A. Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 2013;117:106-14. [CrossRef]

44. Ludwig-Müller J. Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In:Koltai H, Kapulnik Y, editors. Arbuscular mycorrhizas:Physiology and Function. Dordrecht:Springer;2010. 169-90. [CrossRef]

45. Ouledali S, Ennajeh M, Zrig A, Gianinazzi S, Khemira H. Estimating the contribution of arbuscular mycorrhizal fungi to drought tolerance of potted olive trees (Olea europaea). Acta Physiol Plant 2018;40:1-81. [CrossRef]

46. Pavithra D, Yapa N. Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundwater Sustain Dev 2018;7:490-4. [CrossRef]

47. Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B, Ruiz-Lozano JM. Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 2016;26:141-52. [CrossRef]

48. Nelsen CE, Safir GR. Increased drought tolerance of mycorrhizal onion plants caused by improved phosphorus nutrition. Planta 1982;154:407-13. [CrossRef]

49. Ahanger MA, Tittal M, Mir RA, Agarwal RM. Alleviation of water and osmotic stress-induced changes in nitrogen metabolizing enzymes in Triticum aestivum L. cultivars by potassium. Protoplasma 2017;254:1953-63. [CrossRef]

50. Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S. Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 2010;30:161-75. [CrossRef]

51. Santander C, Sanhueza M, Olave J, Borie F, Valentine A, Cornejo P. Arbuscular mycorrhizal colonization promotes the tolerance to salt stress in lettuce plants through an efficient modification of ionic balance. J Soil Sci Plant Nutr 2019;19:321-31. [CrossRef]

52. Talaat NB, Shawky BT. Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot 2014;98:20-31. [CrossRef]

53. Abdel Latef AA, Chaoxing HJ. Does the inoculation with Glomus mosseae improve salt tolerance in pepper plants?J Plant Growth Regul 2014;33:644-53. [CrossRef]

54. El-Nashar YI. Response of snapdragon Antirrhinum majus L. to blended water irrigation and arbuscular mycorrhizal fungi inoculation:Uptake of minerals and leaf water relations. Photosynthetica 2017;55:201-9. [CrossRef]

55. Ait-El-Mokhtar M, Laouane RB, Anli M, Boutasknit A, Wahbi S, Meddich A. Use of mycorrhizal fungi in improving tolerance of the date palm (Phoenix dactylifera L.) seedlings to salt stress. Sci Hortic 2019;253:429-38. [CrossRef]

56. Elhindi KM, El-Din AS, Elgorban AM. The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L.). Saudi J Biol Sci 2017;24:170-9. [CrossRef]

57. Wang Y, Wang M, Li Y, Wu A, Huang J. Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLoS One 2018;13:e0196408. [CrossRef]

58. Kapoor R, Evelin H, Mathur P, Giri B. Arbuscular mycorrhiza:Approaches for abiotic stress tolerance in crop plants for sustainable agriculture. In:Tuteja N, Gill SS, editors, Plant Acclimation to Environmental Stress. New York:Springer;2013. 359-401. [CrossRef]

59. Aroca R, Ruiz-Lozano JM, Zamarreño AM, Paz JA, García-Mina JM, Pozo MJ, et al. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 2013;170:47-55. [CrossRef]

60. Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C. Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato Solanum lycopersicum L. plants. Plant Soil 2010;331:313-27. [CrossRef]

61. Khalloufi M, Martínez-Andújar C, Lachaâl M, Karray-Bouraoui N, Pérez-Alfocea F, Albacete A. The interaction between foliar GA3 application and arbuscular mycorrhizal fungi inoculation improves growth in salinized tomato Solanum lycopersicum L. plants by modifying the hormonal balance. J Plant Physiol 2017;214:134-44. [CrossRef]

62. Hajiboland R, Dashtebani F, Aliasgharzad N. Physiological responses of halophytic C4 grass, Aeluropus littoralis to salinity and arbuscular mycorrhizal fungi colonization. Photosynthetica 2015;53:572-84. [CrossRef]

63. Giri B, Kapoor R, Mukerji KG. Improved tolerance of acacia nilotica, to salt stress by arbuscular mycorrhiza, Glomus fasciculatum, may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 2007;54:753-60. [CrossRef]

64. Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani AF, Aldehaish HA, Egamberdieva D, et al. Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J Biol Sci 2018;25:1102-14. [CrossRef]

65. Zhu XC, Song FB, Liu SQ, Liu TD. Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 2011;346:189-99. [CrossRef]

66. Zhu X, Song F, Liu F. Arbuscular mycorrhizal fungi and tolerance of temperature stress in plants. In:Arbuscular Mycorrhizas and Stress Tolerance of Plants. Berlin, Germany:Springer Science Business Media LLC;2017. 163-94. [CrossRef]

67. Abdel Latef AA, Chaoxing H. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 2011;127:228-33. [CrossRef]

68. Mathur S, Jajoo A. Arbuscular mycorrhizal fungi protects maize plants from high temperature stress by regulating photosystem II heterogeneity. Ind Crops Prod 2020;143:111934. [CrossRef]

69. Hajiboland R, Joudmand A, Aliasgharzad N, TolráR, 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;70:218-33. [CrossRef]

70. Bender SF, Plantenga F, Neftel A, Jocher M, Oberholzer HR, Köhl L, et al. Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. ISME J 2014;8:1336-45. [CrossRef]

71. Ma J, JanouškováM, Ye L, Bai LQ, Dong RR, Yan Y, et al. Role of arbuscular mycorrhiza in alleviating the effect of cold on the photosynthesis of cucumber seedlings. Photosynthetica 2019;57:86-95. [CrossRef]

72. Chu XT, Fu JJ, Sun YF, Xu YM, Miao YJ, Xu YF, et al. Effect of arbuscular mycorrhizal fungi inoculation on cold stress-induced oxidative damage in leaves of Elymus nutans Griseb. S Afr J Bot 2016;104:21-9. [CrossRef]

73. Liu X, Song Q, Tang Y, Li W, Xu J, Wu J, et al. Human health risk assessment of heavy metals in soil-vegetable system:A multi-medium analysis. Sci Total Environ 2013;463-464:530-40. [CrossRef]

74. Yousaf B, Liu G, Wang R, Imtiaz M, Zia-Ur-Rehman M, Munir MA, et al. Bioavailability evaluation, uptake of heavy metals and potential health risks via dietary exposure in urban-industrial areas. Environ Sci Pollut Res Int 2016;23:22443-53. [CrossRef]

75. Moghadam HR. Application of super absorbent polymer and ascorbic acid to mitigate deleterious effects of cadmium in wheat. Pesqui Agropecu Trop 2016;46:9-18. [CrossRef]

76. Ouziad F, Hildebrandt U, Schmelzer E, Bothe H. Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 2005;162:634-49. [CrossRef]

77. Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Da P. Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass Chrysopogon zizanioides L. J Hazard Mater 2010;177:465-74. [CrossRef]

78. Audet P. Arbuscular mycorrhizal fungi and metal phytoremediation:Ecophysiological complementarity in relation to environmental stress. In:Ahmad P, Rasool S, editors. Emerging Technologies and Management of Crop Stress Tolerance. San Diego:Academic Press;2014. 133-60. [CrossRef]

79. Andrade SA, Silveira AP. Mycorrhiza influence on maize development under Cd stress and P supply. Braz J Plant Physiol 2008;20:39-50. [CrossRef]

80. Garg N, Chandel S. Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 2012;31:292-308. [CrossRef]

81. Dong Y, Zhu YG, Smith FA, Wang Y, Chen B. Arbuscular mycorrhiza enhanced arsenic resistance of both white clover Trifolium repens L. and ryegrass Lolium perenne L. plants in an arsenic-contaminated soil. Environ Pollut 2008;155:174-81. [CrossRef]

82. Li H, Chen XW, Wong MH. Arbuscular mycorrhizal fungi reduced the ratios of inorganic/organic arsenic in rice grains. Chemosphere 2016;145:224-30. [CrossRef]

83. Takács T, Vörös I. Effect of metal non-adapted arbuscular mycorrhizal fungi on Cd, Ni and Zn uptake by ryegrass. Acta Agron Hung 2003;51:347-54. [CrossRef]

84. Clark RB, Zeto SK. Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 2000;23:867-902. [CrossRef]

85. Yost RS, Fox RL. Influence of mycorrhizae on the mineral contents of cowpea and soybean grown in an oxisol 1. Agron J 1982;74:475-81. [CrossRef]

86. Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H. Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 2011;21:117-29. [CrossRef]

87. Wang Y, Jing H, Gao Y. Arbuscular mycorrhizal colonization alters subcellular distribution and chemical forms of cadmium in Medicago sativa L. and resists cadmium toxicity. PLoS One 2012;7:3161-4. [CrossRef]

88. Kaldorf M, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H. Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 1999;154:718-28. [CrossRef]

89. Kelkar TS, Bhalerao SA. Beneficiary effect of arbuscular mycorrhiza to Trigonella foenum-graceum in contaminated soil by heavy metal. Res J Recent Sci 2013;2:29-32.

90. Jiang QY, Zhuo F, Long SH, Zhao HD, Yang DJ, Ye ZH, et al. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils?Sci Rep 2016;6:21805. [CrossRef]

91. Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, et al. Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 2008;153:137-47. [CrossRef]

92. Li XL, Christie P. Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 2001;42:201-7. [CrossRef]

93. Khanam D. Influence of flooding on the survival of arbuscular mycorrhiza. Bangladesh J Microbiol 2008;25:111-4. [CrossRef]

94. Wang Y, Huang Y, Qiu Q, Xin G, Yang Z, Shi S. Flooding greatly affects the diversity of arbuscular mycorrhizal fungi communities in the roots of wetland plants. PLoS One 2011;6:e24512. [CrossRef]

95. Bao X, Wang Y, Li PA, Olsson PA. Arbuscular mycorrhiza under water carbon phosphorus exchange between rice and arbuscular mycorrhizal fungi under different flooding regimes. Soil Biol Biochem 2019;129:169-77. [CrossRef]

96. Liang W, Ma X, Wan P, Liu L. Plant salt-tolerance mechanism:A review. Biochem Biophys Res Commun 2018;495:286-91. [CrossRef]

97. Fougnies L, Renciot S, Müller F, Plenchette C, Prin Y, De Faria SM, et al. Arbuscular mycorrhizal colonization and nodulation improve flooding tolerance in Pterocarpus officinalis Jacq. seedlings. Mycorrhiza 2007;17:159-66. [CrossRef]

98. Wang Y, Qiu Q, Yang Z, Hu Z, Tam NF, Xin G. Arbuscular mycorrhizal fungi in two mangroves in South China. Plant Soil 2010;331:181-91. [CrossRef]

99. Solís-Rodríguez UR, Ramos-Zapata JA, Hernández-Cuevas L, Salinas-Peba L, Guadarrama P. Arbuscular mycorrhizal fungi diversity and distribution in tropical low flooding forest in Mexico. Mycol Progress 2020;19:195-204. [CrossRef]

100. Miller SP, Sharitz RR. Manipulation of flooding and arbuscular mycorrhiza formation influences growth and nutrition of two semiaquatic grass species. Funct Ecol 2000;14:738-48. [CrossRef]

101. Bauddh K, Singh RP. Growth:Tolerance efficiency and phytoremediation potential of Ricinus communis (L.) and Brassica juncea (L.) in salinity and drought affected cadmium contaminated soil. Ecotoxicol Environ Saf 2012;85:13-22. [CrossRef]

102. Bárzana G, Aroca R, Ruiz-Lozano JM. Localized and nonlocalized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 2015;38:1613-27. [CrossRef]

103. Calvo-Polanco M, Sánchez-Romera B, Aroca R, Asins MJ, Declerck S, Dodd IC, et al. Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Environ Exp Bot 2016;131:47-57. [CrossRef]

104. Yin N, Zhang Z, Wang L, Qian K. Variations in organic carbon, aggregation, and enzyme activities of gangue-fly ash-reconstructed soils with sludge and arbuscular mycorrhizal fungi during 6-year reclamation. Environ Sci Pollut Res Int 2016;23:17840-9. [CrossRef]

105. AugéRM, Toler HD, Saxton AM. Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress:A meta-analysis. Front Plant Sci 2014;5:562. [CrossRef]

106. Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC. Arbuscular mycorrhizal influence on zinc nutrition in crop plants:A meta-analysis. Soil Biol Biochem 2014;69:123-31. [CrossRef]

107. Lehmann A, Rillig MC. Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops a meta-analysis. Soil Biol Biochem 2015;81:147-58. [CrossRef]

108. Evelin H, Kapoor R, Giri B. Arbuscular mycorrhizal fungi in alleviation of salt stress:A review. Ann Bot 2009;104:1263-80. [CrossRef]

109. Zhang T, Hu Y, Zhang K, Tian C, Guo J. Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind Crops Prod 2018;117:13-9. [CrossRef]

110. Wilson GW, Rice CW, Rillig MC, Springer A, Hartnett DC. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi:Results from long-term field experiments. Ecol Lett 2009;12:452-61. [CrossRef]

111. Nacoon S, Jogloy S, Riddech N, Mongkolthanaruk W, Kuyper TW, Boonlue S. Interaction between phosphate solubilizing bacteria and arbuscular mycorrhizal fungi on growth promotion and tuber inulin content of Helianthus tuberosus L. Sci Rep 2020;10:4916. [CrossRef]

112. Mar Vázquez MM, César S, Azcón R, Barea JM. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 2000;15:261-72. [CrossRef]

113. Khan MS, Zaidi A. Synergistic effects of the inoculation with plant growth-promoting rhizobacteria and an arbuscular mycorrhizal fungus on the performance of wheat. Turk. J Agric 2007;31:355-62.

114. Diagne N, Baudoin E, Svistoonoff S, Ouattara C, Diouf D, Kane A, et al. Effect of native and allochthonous arbuscular mycorrhizal fungi on Casuarina equisetifolia growth and its root bacterial community. Arid Land Res Manag 2018;32:212-28. [CrossRef]

115. Nanjundappa A, Bagyaraj DJ, Saxena AK, Kumar M, Chakdar H. Interaction between arbuscular mycorrhizal fungi and Bacillus spp. in soil enhancing growth of crop plants. Fungal Biol Biotechnol 2019;6:23. [CrossRef]

116. Barea JM, Azcón R, Azcón-Aguilar C. Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Leeuwenhoek 2002;81:343-51. [CrossRef]

117. Tang T, Xie M, Chen S, Zhang S, Wu Q. Effects of arbuscular mycorrhizal fungi and rhizobia on physiological activities in white clover (Trifolium repens). Biotechnology 2019;18:49-54. [CrossRef]

118. Bagyaraj DJ, Manjunath A, Patil RB. Interaction between a vesicular-arbuscular mycorrhiza and rhizobium and their effects on soybean in the field. New Phytol 1979;82:141-5. [CrossRef]

119. Larimer AL, Clay K, Bever JD. Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 2014;95:1045-54. [CrossRef]

120. Xavier L. Response of lentil under controlled conditions to co-inoculation with arbuscular mycorrhizal fungi and rhizobia varying in efficacy. Soil Biol Biochem 2002;34:181-8. [CrossRef]

121. Xavier LJ, Germida JJ. Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol Fertil Soils 2003;37:261-7. [CrossRef]

122. Jin L, Sun X, Wang X, Shen Y, Hou F, Chang S, et al. Synergistic interactions of arbuscular mycorrhizal fungi and rhizobia promoted the growth of Lathyrus sativus under sulphate salt stress. Symbiosis 2010;50:157-64. [CrossRef]

123. Abd-Alla MH, El-Enany AW, Nafady NA, Khalaf DM, Morsy FM. Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 2014;169:49-58. [CrossRef]

124. Chatarpaul L, Chakravarty P, Subramaniam P. Studies in tetrapartite symbioses. Plant Soil 1989;118:145-50. [CrossRef]

125. Orfanoudakis MZ, Hooker JE, Wheeler-Jones CT. Early interactions between arbuscular mycorrhizal fungi and Frankia during colonisation and root nodulation of Alnus glutinosa. Symbiosis 2004;36:69-82.

126. Oliveira RS, Castro PM, Dodd JC, Vosátka M. Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 2005;60:1462-70. [CrossRef]

127. Andrade DS, Leal AC, Ramos AL, De Goes KC. Growth of Casuarina cunninghamiana inoculated with arbuscular mycorrhizal fungi and Frankia actinomycetes. Symbiosis 2015;66:65-73. [CrossRef]

128. Chonglu Z, Mingqin G, Yu C, Fengzhen W. Inoculation of Casuarina with ectomycorrhizal fungi, vesicular-arbuscular mycorrhizal fungi and Frankia. In:Mycorrhizas for Plantation Forestry in Asia ACIAR. Proceedings of the International Symposium and Workshop, Kaiping, China;November 7-11;2014. 122.

129. Wheeler CT, Tilak M, Scrimgeour CM, Hooker JE, Handley LL. Effects of symbiosis with Frankia and arbuscular mycorrhizal fungus on the natural abundance of 15N in four species of Casuarina. J Exp Bot 2000;51:287-97. [CrossRef]

130. Visser S, Danielson RM, Parkinson D. Field performance of Elaeagnus commutata and Shepherdia canadensis (Elaeagnaceae) inoculated with soil containing Frankia and vesicular arbuscular mycorrhizal fungi. Can J Bot 1991;69:1321-8. [CrossRef]

131. Lesueur D, Duponnois R. Relations between rhizobial nodulation and root colonization of Acacia crassicarpa provenances by an arbuscular mycorrhizal fungus, Glomus intraradices Schenk and Smith or an ectomycorrhizal fungus, Pisolithus tinctorius Coker and Couch. Ann For Sci 2005;62:467-74. [CrossRef]

132. Rajendran K, Devaraj P. Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with biofertilizers in farm land. Biomass Bioenergy 2004;26:235-49. [CrossRef]

133. Chilvers GA, Lapeyrie FF, Horan DP. Ectomycorrhizal vs endomycorrhizal fungi within the same root system. New Phytol 1987;107:441-8. [CrossRef]

134. Duponnois R, Diédhiou S, Chotte JL, Sy MO. Relative importance of the endomycorrhizal and (or) ectomycorrhizal associations in Allocasuarina and Casuarina genera. Can J Microbiol 2003;49:281-7. [CrossRef]

135. Elumalai S, Raaman N. In vitro synthesis of Frankia and mycorrhiza with Casuarina equisetifolia and ultrastructure of root system. Indian J Exp Biol 2009;47:289-97.

136. Duponnois R. Mycorrhiza helper bacteria:Their ecological impact in mycorrhizal symbiosis. Handb Microb Biofertil 2006;117:231-50.

137. Frey-Klett P, Garbaye J, Tarkka M. The mycorrhiza helper bacteria revisited. New Phytol 2007;176:22-36. [CrossRef]

138. Rigamonte TA, Pylro VS, Duarte GF. The role of mycorrhization helper bacteria in the establishment and action of ectomycorrhizae associations. Braz J Microbiol 2010;41:832-40. [CrossRef]

Reference

1. Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta 2003;218:1-14. https://doi.org/10.1007/s00425-003-1105-5

2. Gary H, Ram K, Doni F, Norman U. Benefits to plant health and productivity from enhancing plant microbial symbionts. Front Plant Sci 2021;11:2001. https://doi.org/10.3389/fpls.2020.610065

3. Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 2016;108:1028-46. https://doi.org/10.3852/16-042

4. Parniske M. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat Rev Microbiol 2008;6:763-75. https://doi.org/10.1038/nrmicro1987

5. Smith SE, Read DJ. Mycorrhizal Symbiosis. Cambridge, MA: Academic Press; 2010.

6. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN. Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 2009;40:699-715. https://doi.org/10.1146/annurev.ecolsys.39.110707.173454

7. Smith S, Read D. Mycorrhiza Symbiosis. 3rd ed. San Diego: Academic Press; 2008. https://doi.org/10.1016/B978-012370526-6.50013-1

8. Barrow CJ. Biochar potential for countering land degradation and for improving agriculture. Appl Geogr 2012;34:21-8. https://doi.org/10.1016/j.apgeog.2011.09.008

9. Wu Z, McGrouther K, Huang J, Wu P, Wu W, Wang H. Decomposition and the contribution of glomalin-related soil protein (GRSP) in heavy metal sequestration: Field experiment. Soil Biol Biochem 2014;68:283-90. https://doi.org/10.1016/j.soilbio.2013.10.010

10. Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T. Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress a meta-analysis. Front Plant Sci 2019;10:457. https://doi.org/10.3389/fpls.2019.00457

11. Bona E, Cantamessa S, Massa N, Manassero P, Marsano F, Copetta A, et al. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: A field study. Mycorrhiza 2017;27:1-11. https://doi.org/10.1007/s00572-016-0727-y

12. Nakmee PS, Techapinyawat S, Ngamprasit S. Comparative potentials of native arbuscular mycorrhizal fungi to improve nutrient uptake and biomass of Sorghum bicolor Linn. Agric Nat Resour 2016;50:173-8. https://doi.org/10.1016/j.anres.2016.06.004

13. Al-Hmoud G, Al-Momany A. Effect of four mycorrhizal products on squash plant growth and its effect on physiological plant elements. Adv Crop Sci Technol 2017;5:260.

14. Parihar P, Bora M. Effect of mycorrhiza (Glomus mosseae) on morphological and biochemical properties of Ashwagandha (Withania somnifera) (L.) Dunal. J Appl Natl Sci 2018;10:1115-23. https://doi.org/10.31018/jans.v10i4.1797

15. Ruth B, Khalvati M, Schmidhalter U. Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 2011;342:459-68. https://doi.org/10.1007/s11104-010-0709-3

16. Sadhana B. Arbuscular mycorrhizal fungi (AMF) as a biofertilizers a review. Int J Curr Microbiol Appl Sci 2014;3:384-400.

17. Ortas I. The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions. Field Crops Res 2012;125:35-48. https://doi.org/10.1016/j.fcr.2011.08.005

18. Yang S, Li F, Malhi SS, Wang P, Suo D, Wang J. Long-term fertilization effects on crop yield and nitrate nitrogen accumulation in soil in Northwestern China. Agron J 2004;96:1039-49. https://doi.org/10.2134/agronj2004.1039

19. Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, et al. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 2017;356:1175-8. https://doi.org/10.1126/science.aan0081

20. Mitra D, Navendra U, Panneerselvam U, Ansuman S, Ganeshamurthy AN, Divya J. Role of mycorrhiza and its associated bacteria on plant growth promotion and nutrient management in sustainable agriculture. Int J Life Sci Appl Sci 2019;1:1-10.

21. Prasad R, Bhola D, Akdi K, Cruz C, Sairam KV, Tuteja N, et al. Introduction to mycorrhiza: Historical development. In: Varma A, Prasad R, Tuteja N, editors. Mycorrhiza. Cham: Springer; 2017. p. 1-11. https://doi.org/10.1007/978-3-319-53064-2_1

22. De Andrade SA, Domingues AP, Mazzafera P. Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere 2015;134:141-9. https://doi.org/10.1016/j.chemosphere.2015.04.023

23. Hart M, Ehret DL, Krumbein A, Leung C, Murch S, Turi C, et al. Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza 2015;25:359-76. https://doi.org/10.1007/s00572-014-0617-0

24. Zeng L, JianFu L, JianFu L, MingYuan W. Effects of arbuscular mycorrhizal (AM) fungi on citrus quality under nature conditions. Southwest China J Agric Sci 2014;27:2101-5.

25. Baslam M, Garmendia I, Goicoechea N. Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse grown lettuce. J Agric Food Chem 2011;59:5504-15. https://doi.org/10.1021/jf200501c

26. Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, et al. Arbuscular mycorrhizal fungi act as bio-stimulants in horticultural crops. Sci Hortic 2015;196:91-108. https://doi.org/10.1016/j.scienta.2015.09.002

27. Impa SM, Nadaradjan S, Jagadish SV. Drought stress induced reactive oxygen species and anti-oxidants in plants. In: Ahmad P, Prasad MN, editors. Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability. Berlin: Springer Science and Business Media; 2012. p. 131-47. https://doi.org/10.1007/978-1-4614-0634-1_7

28. Hasanuzzaman M, Gill SS, Fujita M. Physiological role of nitric oxide in plants grown under adverse environmental conditions. In: Tuteja N, Gill SS, editors. Plant Acclimation to Environmental Stress. New York: Springer Science Business Media; 2013. p. 269-322. https://doi.org/10.1007/978-1-4614-5001-6_11

29. Ahanger MA, Agarwal RM. Potassium up-regulates antioxidant metabolism and alleviates growth inhibition under water and osmotic stress in wheat (Triticum aestivum L.). Protoplasma 2017;254:1471-86. https://doi.org/10.1007/s00709-016-1037-0

30. Mena-Violante HG, Ocampo-Jiménez O, Dendooven L, Martínez- Soto G, González-Castañeda J, Davies FT, et al. Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv S. Luis) plants exposed to drought. Mycorrhiza 2006;16:261-7. https://doi.org/10.1007/s00572-006-0043-z

31. Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R, et al. Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 2016;39:441-52. https://doi.org/10.1111/pce.12631

32. Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-Um S. Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 2016;198:107-17. https://doi.org/10.1016/j.scienta.2015.11.002

33. Moradtalab N, Hajiboland R, Aliasgharzad N, Hartmann TE, Neumann G. Silicon and the association with an arbuscular-mycorrhizal fungus (Rhizophagus clarus) mitigate the adverse effects of drought stress on strawberry. Agronomy 2019;9:41. https://doi.org/10.3390/agronomy9010041

34. Gianinazzi S, Gollotte A, Binet MN, Van Tuinen D, Redecker D, Wipf D. Agroecology: The key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 2010;20:519-30. https://doi.org/10.1007/s00572-010-0333-3

35. Orfanoudakis M, Wheeler CT, Hooker JE. Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 2010;20:117-26. https://doi.org/10.1007/s00572-009-0271-0

36. Gutjahr C, Paszkowski U. Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Front Plant Sci 2013;4:204. https://doi.org/10.3389/fpls.2013.00204

37. Zhang X, Li W, Fang M, Jixian Y, Meng S. Effects of arbuscular mycorrhizal fungi inoculation on carbon and nitrogen distribution and grain yield and nutritional quality in rice (Oryza sativa L.). J Sci Food Agric 2016;97:2919-25. https://doi.org/10.1002/jsfa.8129

38. Kubikova E, Jennifer LM, Bonnie HO, Michael DM, Augé MR. Mycorrhizal impact on osmotic adjustment in Ocimum basilicum during a lethal drying episode. J Plant Physiol 2001;158:1227-30. https://doi.org/10.1078/0176-1617-00441

39. Duan X, Neuman DS, Reiber JM, Green CD, Saxton AM, Augé RM. Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 1996;47:1541-50. https://doi.org/10.1093/jxb/47.10.1541

40. Ruiz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM. The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 2010;167:862-9. https://doi.org/10.1016/j.jplph.2010.01.018

41. Yooyongwech S, Phaukinsang N, Cha-Um S, Supaibulwatana K. Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regul 2013;69:285-93. https://doi.org/10.1007/s10725-012-9771-6

42. Rani B. Effect of Arbuscular Mycorrhiza Fungi on Biochemical Parameters in Wheat Triticum aestivum L. under Drought Conditions [Doctoral Dissertation]. Hisar, India: CCSHAU; 2016.

43. Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A. Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 2013;117:106-14. https://doi.org/10.1016/j.agwat.2012.11.007

44. Ludwig-Müller J. Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Koltai H, Kapulnik Y, editors. Arbuscular mycorrhizas: Physiology and Function. Dordrecht: Springer; 2010. p. 169-90. https://doi.org/10.1007/978-90-481-9489-6_8

45. Ouledali S, Ennajeh M, Zrig A, Gianinazzi S, Khemira H. Estimating the contribution of arbuscular mycorrhizal fungi to drought

tolerance of potted olive trees (Olea europaea). Acta Physiol Plant 2018;40:1-81.

46. Pavithra D, Yapa N. Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundwater Sustain Dev 2018;7:490-4. https://doi.org/10.1016/j.gsd.2018.03.005

47. Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B, Ruiz-Lozano JM. Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 2016;26:141-52. https://doi.org/10.1007/s00572-015-0653-4

48. Nelsen CE, Safir GR. Increased drought tolerance of mycorrhizal onion plants caused by improved phosphorus nutrition. Planta 1982;154:407-13. https://doi.org/10.1007/BF01267807

49. Ahanger MA, Tittal M, Mir RA, Agarwal RM. Alleviation of water and osmotic stress-induced changes in nitrogen metabolizing enzymes in Triticum aestivum L. cultivars by potassium. Protoplasma 2017;254:1953-63. https://doi.org/10.1007/s00709-017-1086-z

50. Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S. Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 2010;30:161-75. https://doi.org/10.3109/07388550903524243

51. Santander C, Sanhueza M, Olave J, Borie F, Valentine A, Cornejo P. Arbuscular mycorrhizal colonization promotes the tolerance to salt stress in lettuce plants through an efficient modification of ionic balance. J Soil Sci Plant Nutr 2019;19:321-31. https://doi.org/10.1007/s42729-019-00032-z

52. Talaat NB, Shawky BT. Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot 2014;98:20-31. https://doi.org/10.1016/j.envexpbot.2013.10.005

53. Abdel Latef AA, Chaoxing HJ. Does the inoculation with Glomus mosseae improve salt tolerance in pepper plants? J Plant Growth Regul 2014;33:644-53. https://doi.org/10.1007/s00344-014-9414-4

54. El-Nashar YI. Response of snapdragon Antirrhinum majus L. to blended water irrigation and arbuscular mycorrhizal fungi inoculation: Uptake of minerals and leaf water relations. Photosynthetica 2017;55:201-9. https://doi.org/10.1007/s11099-016-0650-7

55. Ait-El-Mokhtar M, Laouane RB, Anli M, Boutasknit A, Wahbi S, Meddich A. Use of mycorrhizal fungi in improving tolerance of the date palm (Phoenix dactylifera L.) seedlings to salt stress. Sci Hortic 2019;253:429-38. https://doi.org/10.1016/j.scienta.2019.04.066

56. Elhindi KM, El-Din AS, Elgorban AM. The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L.). Saudi J Biol Sci 2017;24:170-9. https://doi.org/10.1016/j.sjbs.2016.02.010

57. Wang Y, Wang M, Li Y, Wu A, Huang J. Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLoS One 2018;13:e0196408. https://doi.org/10.1371/journal.pone.0196408

58. Kapoor R, Evelin H, Mathur P, Giri B. Arbuscular mycorrhiza: Approaches for abiotic stress tolerance in crop plants for sustainable agriculture. In: Tuteja N, Gill SS, editors, Plant Acclimation to Environmental Stress. New York: Springer; 2013. p. 359-401. https://doi.org/10.1007/978-1-4614-5001-6_14

59. Aroca R, Ruiz-Lozano JM, Zamarreño AM, Paz JA, García-Mina JM, Pozo MJ, et al. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 2013;170:47-55. https://doi.org/10.1016/j.jplph.2012.08.020

60. Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C. Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato Solanum lycopersicum L. plants. Plant Soil 2010;331:313-27. https://doi.org/10.1007/s11104-009-0255-z

61. Khalloufi M, Martínez-Andújar C, Lachaâl M, Karray-Bouraoui N, Pérez-Alfocea F, Albacete A. The interaction between foliar GA3 application and arbuscular mycorrhizal fungi inoculation improves growth in salinized tomato Solanum lycopersicum L. plants by modifying the hormonal balance. J Plant Physiol 2017;214:134-44. https://doi.org/10.1016/j.jplph.2017.04.012

62. Hajiboland R, Dashtebani F, Aliasgharzad N. Physiological responses of halophytic C4 grass, Aeluropus littoralis to salinity and arbuscular mycorrhizal fungi colonization. Photosynthetica 2015;53:572-84. https://doi.org/10.1007/s11099-015-0131-4

63. Giri B, Kapoor R, Mukerji KG. Improved tolerance of acacia nilotica, to salt stress by arbuscular mycorrhiza, Glomus fasciculatum, may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 2007;54:753-60. https://doi.org/10.1007/s00248-007-9239-9

64. Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani AF, Aldehaish HA, Egamberdieva D, et al. Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J Biol Sci 2018;25:1102-14. https://doi.org/10.1016/j.sjbs.2018.03.009

65. Zhu XC, Song FB, Liu SQ, Liu TD. Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 2011;346:189-99. https://doi.org/10.1007/s11104-011-0809-8

66. Zhu X, Song F, Liu F. Arbuscular mycorrhizal fungi and tolerance of temperature stress in plants. In: Arbuscular Mycorrhizas and Stress Tolerance of Plants. Berlin, Germany: Springer Science Business Media LLC; 2017. p. 163-94. https://doi.org/10.1007/978-981-10-4115-0_8

67. Abdel Latef AA, Chaoxing H. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 2011;127:228-33. https://doi.org/10.1016/j.scienta.2010.09.020

68. Mathur S, Jajoo A. Arbuscular mycorrhizal fungi protects maize plants from high temperature stress by regulating photosystem II heterogeneity. Ind Crops Prod 2020;143:111934. https://doi.org/10.1016/j.indcrop.2019.111934

69. Hajiboland R, Joudmand A, Aliasgharzad N, Tolrá 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;70:218-33. https://doi.org/10.1071/CP18385

70. Bender SF, Plantenga F, Neftel A, Jocher M, Oberholzer HR, Köhl L, et al. Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. ISME J 2014;8:1336-45. https://doi.org/10.1038/ismej.2013.224

71. Ma J, Janoušková M, Ye L, Bai LQ, Dong RR, Yan Y, et al. Role of arbuscular mycorrhiza in alleviating the effect of cold on the photosynthesis of cucumber seedlings. Photosynthetica 2019;57:86-95. https://doi.org/10.32615/ps.2019.001

72. Chu XT, Fu JJ, Sun YF, Xu YM, Miao YJ, Xu YF, et al. Effect of arbuscular mycorrhizal fungi inoculation on cold stress-induced oxidative damage in leaves of Elymus nutans Griseb. S Afr J Bot 2016;104:21-9. https://doi.org/10.1016/j.sajb.2015.10.001

73. Liu X, Song Q, Tang Y, Li W, Xu J, Wu J, et al. Human health risk assessment of heavy metals in soil-vegetable system: A multi-medium analysis. Sci Total Environ 2013;463-464:530-40. https://doi.org/10.1016/j.scitotenv.2013.06.064

74. Yousaf B, Liu G, Wang R, Imtiaz M, Zia-Ur-Rehman M, Munir MA, et al. Bioavailability evaluation, uptake of heavy metals and potential health risks via dietary exposure in urban-industrial areas. Environ Sci Pollut Res Int 2016;23:22443-53. https://doi.org/10.1007/s11356-016-7449-8

75. Moghadam HR. Application of super absorbent polymer and ascorbic acid to mitigate deleterious effects of cadmium in wheat. Pesqui Agropecu Trop 2016;46:9-18. https://doi.org/10.1590/1983-40632016v4638946

76. Ouziad F, Hildebrandt U, Schmelzer E, Bothe H. Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 2005;162:634-49. https://doi.org/10.1016/j.jplph.2004.09.014

77. Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Da P. Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass Chrysopogon zizanioides L. J Hazard Mater 2010;177:465-74. https://doi.org/10.1016/j.jhazmat.2009.12.056

78. Audet P. Arbuscular mycorrhizal fungi and metal phytoremediation: Ecophysiological complementarity in relation to environmental stress. In: Ahmad P, Rasool S, editors. Emerging Technologies and Management of Crop Stress Tolerance. San Diego: Academic Press; 2014. p. 133-60. https://doi.org/10.1016/B978-0-12-800875-1.00006-5

79. Andrade SA, Silveira AP. Mycorrhiza influence on maize development under Cd stress and P supply. Braz J Plant Physiol 2008;20:39-50. https://doi.org/10.1590/S1677-04202008000100005

80. Garg N, Chandel S. Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis

in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 2012;31:292-308. https://doi.org/10.1007/s00344-011-9239-3

81. Dong Y, Zhu YG, Smith FA, Wang Y, Chen B. Arbuscular mycorrhiza enhanced arsenic resistance of both white clover Trifolium repens L. and ryegrass Lolium perenne L. plants in an arsenic-contaminated soil. Environ Pollut 2008;155:174-81. https://doi.org/10.1016/j.envpol.2007.10.023

82. Li H, Chen XW, Wong MH. Arbuscular mycorrhizal fungi reduced the ratios of inorganic/organic arsenic in rice grains. Chemosphere 2016;145:224-30. https://doi.org/10.1016/j.chemosphere.2015.10.067

83. Takács T, Vörös I. Effect of metal non-adapted arbuscular mycorrhizal fungi on Cd, Ni and Zn uptake by ryegrass. Acta Agron Hung 2003;51:347-54. https://doi.org/10.1556/AAgr.51.2003.3.13

84. Clark RB, Zeto SK. Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 2000;23:867-902. https://doi.org/10.1080/01904160009382068

85. Yost RS, Fox RL. Influence of mycorrhizae on the mineral contents of cowpea and soybean grown in an oxisol 1. Agron J 1982;74:475-81. https://doi.org/10.2134/agronj1982.00021962007400030018x

86. Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H. Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 2011;21:117-29. https://doi.org/10.1007/s00572-010-0316-4

87. Wang Y, Jing H, Gao Y. Arbuscular mycorrhizal colonization alters subcellular distribution and chemical forms of cadmium in Medicago sativa L. and resists cadmium toxicity. PLoS One 2012;7:3161-4. https://doi.org/10.1371/journal.pone.0048669

88. Kaldorf M, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H. Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 1999;154:718-28. https://doi.org/10.1016/S0176-1617(99)80250-8

89. Kelkar TS, Bhalerao SA. Beneficiary effect of arbuscular mycorrhiza to Trigonella foenum-graceum in contaminated soil by heavy metal. Res J Recent Sci 2013;2:29-32.

90. Jiang QY, Zhuo F, Long SH, Zhao HD, Yang DJ, Ye ZH, et al. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Sci Rep 2016;6:21805. https://doi.org/10.1038/srep21805

91. Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, et al. Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 2008;153:137-47. https://doi.org/10.1016/j.envpol.2007.07.012

92. Li XL, Christie P. Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 2001;42:201-7. https://doi.org/10.1016/S0045-6535(00)00126-0

93. Khanam D. Influence of flooding on the survival of arbuscular mycorrhiza. Bangladesh J Microbiol 2008;25:111-4. https://doi.org/10.3329/bjm.v25i2.4872

94. Wang Y, Huang Y, Qiu Q, Xin G, Yang Z, Shi S. Flooding greatly affects the diversity of arbuscular mycorrhizal fungi communities in the roots of wetland plants. PLoS One 2011;6:e24512. https://doi.org/10.1371/journal.pone.0024512

95. Bao X, Wang Y, Li PA, Olsson PA. Arbuscular mycorrhiza under water carbon phosphorus exchange between rice and arbuscular mycorrhizal fungi under different flooding regimes. Soil Biol Biochem 2019;129:169-77. https://doi.org/10.1016/j.soilbio.2018.11.020

96. Liang W, Ma X, Wan P, Liu L. Plant salt-tolerance mechanism: A review. Biochem Biophys Res Commun 2018;495:286-91. https://doi.org/10.1016/j.bbrc.2017.11.043

97. Fougnies L, Renciot S, Müller F, Plenchette C, Prin Y, De Faria SM, et al. Arbuscular mycorrhizal colonization and nodulation improve flooding tolerance in Pterocarpus officinalis Jacq. seedlings. Mycorrhiza 2007;17:159-66. https://doi.org/10.1007/s00572-006-0085-2

98. Wang Y, Qiu Q, Yang Z, Hu Z, Tam NF, Xin G. Arbuscular mycorrhizal fungi in two mangroves in South China. Plant Soil 2010;331:181-91. https://doi.org/10.1007/s11104-009-0244-2

99. Solís-Rodríguez UR, Ramos-Zapata JA, Hernández-Cuevas L, Salinas-Peba L, Guadarrama P. Arbuscular mycorrhizal fungi diversity and distribution in tropical low flooding forest in Mexico. Mycol Progress 2020;19:195-204. https://doi.org/10.1007/s11557-019-01550-x

100. Miller SP, Sharitz RR. Manipulation of flooding and arbuscular mycorrhiza formation influences growth and nutrition of two semiaquatic grass species. Funct Ecol 2000;14:738-48. https://doi.org/10.1046/j.1365-2435.2000.00481.x

101. Bauddh K, Singh RP. Growth: Tolerance efficiency and phytoremediation potential of Ricinus communis (L.) and Brassica juncea (L.) in salinity and drought affected cadmium contaminated soil. Ecotoxicol Environ Saf 2012;85:13-22. https://doi.org/10.1016/j.ecoenv.2012.08.019

102. Bárzana G, Aroca R, Ruiz-Lozano JM. Localized and nonlocalized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 2015;38:1613-27. https://doi.org/10.1111/pce.12507

103. Calvo-Polanco M, Sánchez-Romera B, Aroca R, Asins MJ, Declerck S, Dodd IC, et al. Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Environ Exp Bot 2016;131:47-57. https://doi.org/10.1016/j.envexpbot.2016.06.015

104. Yin N, Zhang Z, Wang L, Qian K. Variations in organic carbon, aggregation, and enzyme activities of gangue-fly ash-reconstructed soils with sludge and arbuscular mycorrhizal fungi during 6-year reclamation. Environ Sci Pollut Res Int 2016;23:17840-9. https://doi.org/10.1007/s11356-016-6941-5

105. Augé RM, Toler HD, Saxton AM. Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: A meta-analysis. Front Plant Sci 2014;5:562. https://doi.org/10.3389/fpls.2014.00562

106. Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC. Arbuscular mycorrhizal influence on zinc nutrition in crop plants: A meta-analysis. Soil Biol Biochem 2014;69:123-31. https://doi.org/10.1016/j.soilbio.2013.11.001

107. Lehmann A, Rillig MC. Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops a meta-analysis. Soil Biol Biochem 2015;81:147-58. https://doi.org/10.1016/j.soilbio.2014.11.013

108. Evelin H, Kapoor R, Giri B. Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Ann Bot 2009;104:1263-80. https://doi.org/10.1093/aob/mcp251

109. Zhang T, Hu Y, Zhang K, Tian C, Guo J. Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind Crops Prod 2018;117:13-9. https://doi.org/10.1016/j.indcrop.2018.02.087

110. Wilson GW, Rice CW, Rillig MC, Springer A, Hartnett DC. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: Results from long-term field experiments. Ecol Lett 2009;12:452-61. https://doi.org/10.1111/j.1461-0248.2009.01303.x

111. Nacoon S, Jogloy S, Riddech N, Mongkolthanaruk W, Kuyper TW, Boonlue S. Interaction between phosphate solubilizing bacteria and arbuscular mycorrhizal fungi on growth promotion and tuber inulin content of Helianthus tuberosus L. Sci Rep 2020;10:4916. https://doi.org/10.1038/s41598-020-61846-x

112. Mar Vázquez MM, César S, Azcón R, Barea JM. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 2000;15:261-72. https://doi.org/10.1016/S0929-1393(00)00075-5

113. Khan MS, Zaidi A. Synergistic effects of the inoculation with plant growth-promoting rhizobacteria and an arbuscular mycorrhizal fungus on the performance of wheat. Turk. J Agric 2007;31:355-62.

114. Diagne N, Baudoin E, Svistoonoff S, Ouattara C, Diouf D, Kane A, et al. Effect of native and allochthonous arbuscular mycorrhizal fungi on Casuarina equisetifolia growth and its root bacterial community. Arid Land Res Manag 2018;32:212-28. https://doi.org/10.1080/15324982.2017.1406413

115. Nanjundappa A, Bagyaraj DJ, Saxena AK, Kumar M, Chakdar H. Interaction between arbuscular mycorrhizal fungi and Bacillus spp. in soil enhancing growth of crop plants. Fungal Biol Biotechnol 2019;6:23. https://doi.org/10.1186/s40694-019-0086-5

116. Barea JM, Azcón R, Azcón-Aguilar C. Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Leeuwenhoek 2002;81:343-51. https://doi.org/10.1023/A:1020588701325

117. Tang T, Xie M, Chen S, Zhang S, Wu Q. Effects of arbuscular mycorrhizal fungi and rhizobia on physiological activities in white clover (Trifolium repens). Biotechnology 2019;18:49-54. https://doi.org/10.3923/biotech.2019.49.54

118. Bagyaraj DJ, Manjunath A, Patil RB. Interaction between a vesicular-arbuscular mycorrhiza and rhizobium and their effects on soybean in the field. New Phytol 1979;82:141-5. https://doi.org/10.1111/j.1469-8137.1979.tb07568.x

119. Larimer AL, Clay K, Bever JD. Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 2014;95:1045-54. https://doi.org/10.1890/13-0025.1

120. Xavier L. Response of lentil under controlled conditions to co-inoculation with arbuscular mycorrhizal fungi and rhizobia varying in efficacy. Soil Biol Biochem 2002;34:181-8. https://doi.org/10.1016/S0038-0717(01)00165-1

121. Xavier LJ, Germida JJ. Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol Fertil Soils 2003;37:261-7. https://doi.org/10.1007/s00374-003-0605-6

122. Jin L, Sun X, Wang X, Shen Y, Hou F, Chang S, et al. Synergistic interactions of arbuscular mycorrhizal fungi and rhizobia promoted the growth of Lathyrus sativus under sulphate salt stress. Symbiosis 2010;50:157-64. https://doi.org/10.1007/s13199-010-0058-2

123. Abd-Alla MH, El-Enany AW, Nafady NA, Khalaf DM, Morsy FM. Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 2014;169:49-58. https://doi.org/10.1016/j.micres.2013.07.007

124. Chatarpaul L, Chakravarty P, Subramaniam P. Studies in tetrapartite symbioses. Plant Soil 1989;118:145-50. https://doi.org/10.1007/BF02232800

125. Orfanoudakis MZ, Hooker JE, Wheeler-Jones CT. Early interactions between arbuscular mycorrhizal fungi and Frankia during colonisation and root nodulation of Alnus glutinosa. Symbiosis 2004;36:69-82.

126. Oliveira RS, Castro PM, Dodd JC, Vosátka M. Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 2005;60:1462-70. https://doi.org/10.1016/j.chemosphere.2005.01.038

127. Andrade DS, Leal AC, Ramos AL, De Goes KC. Growth of Casuarina cunninghamiana inoculated with arbuscular mycorrhizal fungi and Frankia actinomycetes. Symbiosis 2015;66:65-73. https://doi.org/10.1007/s13199-015-0335-1

128. Chonglu Z, Mingqin G, Yu C, Fengzhen W. Inoculation of Casuarina with ectomycorrhizal fungi, vesicular-arbuscular mycorrhizal fungi and Frankia. In: Mycorrhizas for Plantation Forestry in Asia ACIAR. Proceedings of the International Symposium and Workshop, Kaiping, China; November 7-11; 2014. p. 122.

129. Wheeler CT, Tilak M, Scrimgeour CM, Hooker JE, Handley LL. Effects of symbiosis with Frankia and arbuscular mycorrhizal fungus on the natural abundance of 15N in four species of Casuarina. J Exp Bot 2000;51:287-97. https://doi.org/10.1093/jexbot/51.343.287

130. Visser S, Danielson RM, Parkinson D. Field performance of Elaeagnus commutata and Shepherdia canadensis (Elaeagnaceae) inoculated with soil containing Frankia and vesicular arbuscular mycorrhizal fungi. Can J Bot 1991;69:1321-8. https://doi.org/10.1139/b91-171

131. Lesueur D, Duponnois R. Relations between rhizobial nodulation and root colonization of Acacia crassicarpa provenances by an arbuscular mycorrhizal fungus, Glomus intraradices Schenk and Smith or an ectomycorrhizal fungus, Pisolithus tinctorius Coker and Couch. Ann For Sci 2005;62:467-74. https://doi.org/10.1051/forest:2005043

132. Rajendran K, Devaraj P. Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with biofertilizers in farm land. Biomass Bioenergy 2004;26:235-49. https://doi.org/10.1016/j.biombioe.2003.07.001

133. Chilvers GA, Lapeyrie FF, Horan DP. Ectomycorrhizal vs endomycorrhizal fungi within the same root system. New Phytol 1987;107:441-8. https://doi.org/10.1111/j.1469-8137.1987.tb00195.x

134. Duponnois R, Diédhiou S, Chotte JL, Sy MO. Relative importance of the endomycorrhizal and (or) ectomycorrhizal associations in Allocasuarina and Casuarina genera. Can J Microbiol 2003;49:281-7. https://doi.org/10.1139/w03-038

135. Elumalai S, Raaman N. In vitro synthesis of Frankia and mycorrhiza with Casuarina equisetifolia and ultrastructure of root system. Indian J Exp Biol 2009;47:289-97.

136. Duponnois R. Mycorrhiza helper bacteria: Their ecological impact in mycorrhizal symbiosis. Handb Microb Biofertil 2006;117:231-50.

137. Frey-Klett P, Garbaye J, Tarkka M. The mycorrhiza helper bacteria revisited. New Phytol 2007;176:22-36. https://doi.org/10.1111/j.1469-8137.2007.02191.x

138. Rigamonte TA, Pylro VS, Duarte GF. The role of mycorrhization helper bacteria in the establishment and action of ectomycorrhizae associations. Braz J Microbiol 2010;41:832-40. https://doi.org/10.1590/S1517-83822010000400002

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