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Review ARTICLE

Front. Plant Sci., 19 September 2019 | https://doi.org/10.3389/fpls.2019.01068

Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance

Naheeda Begum1, Cheng Qin1, Muhammad Abass Ahanger1, Sajjad Raza2, Muhammad Ishfaq Khan3, Muhammad Ashraf4, Nadeem Ahmed1,5 and Lixin Zhang1*
  • 1College of Life Sciences, Northwest A&F University, Yangling, China
  • 2College of Natural Resources and Environment, Northwest A&F University, Yangling, China
  • 3Department of Weed Science, The University of Agriculture, Peshawar, Pakistan
  • 4University of Agriculture Faisalabad, Pakistan
  • 5Department of Botany, Mohi-Ud-Din Islamic University Azad Jammu and Kashmir, Pakistan

Abiotic stresses hamper plant growth and productivity. Climate change and agricultural malpractices like excessive use of fertilizers and pesticides have aggravated the effects of abiotic stresses on crop productivity and degraded the ecosystem. There is an urgent need for environment-friendly management techniques such as the use of arbuscular mycorrhizal fungi (AMF) for enhancing crop productivity. AMF are commonly known as bio-fertilizers. Moreover, it is widely believed that the inoculation of AMF provides tolerance to host plants against various stressful situations like heat, salinity, drought, metals, and extreme temperatures. AMF may both assist host plants in the up-regulation of tolerance mechanisms and prevent the down-regulation of key metabolic pathways. AMF, being natural root symbionts, provide essential plant inorganic nutrients to host plants, thereby improving growth and yield under unstressed and stressed regimes. The role of AMF as a bio-fertilizer can potentially strengthen plants’ adaptability to changing environment. Thus, further research focusing on the AMF-mediated promotion of crop quality and productivity is needed. The present review provides a comprehensive up-to-date knowledge on AMF and their influence on host plants at various growth stages, their advantages and applications, and consequently the importance of the relationships of different plant nutrients with AMF.

Introduction

Arbuscular mycorrhizal fungi (AMF) facilitate host plants to grow vigorously under stressful conditions by mediating a series of complex communication events between the plant and the fungus leading to enhanced photosynthetic rate and other gas exchange-related traits (Birhane et al., 2012), as well as increased water uptake. Numerous reports describe improved resistance to a variety of stresses including drought, salinity, herbivory, temperature, metals, and diseases due to fungal symbiosis (Rodriguez et al., 2008; Ahanger et al., 2014; Salam et al., 2017). Nearly 90% of plant species including flowering plants, bryophytes, and ferns can develop interdependent connections with AMF (Zhu et al., 2010a; Ahanger et al., 2014). AMF form vesicles, arbuscules, and hyphae in roots, and also spores and hyphae in the rhizosphere. Formation of hyphal network by the AMF with plant roots significantly enhances the access of roots to a large soil surface area, causing improvement in plant growth (Bowles et al., 2016). AMF improve plant nutrition by increasing the availability as well as translocation of various nutrients (Rouphael et al., 2015). AMF improve the quality of soil by influencing its structure and texture, and hence plant health (Zou et al., 2016; Thirkell et al., 2017). Fungal hyphae can expedite the decomposition process of soil organic matter (Paterson et al., 2016). Furthermore, mycorrhizal fungi may affect atmospheric CO2 fixation by host plants, by increasing “sink effect” and movement of photo-assimilates from the aerial parts to the roots. Keeping in view the importance of AMF and the research advancements related to their applications in agriculture, the present review focuses on the role of AMF as bio-fertilizers in the regulation of plant growth and development with improved nutrient uptake under stressful environments, and the level to which AMF can enhance plant growth under stressful environments.

Background of Arbuscular Mycorrhizal Fungi

AMF are soil-borne fungi that can significantly improve plant nutrient uptake and resistance to several abiotic stress factors (Sun et al., 2018). A majority of the species of AMF belong to the sub-phylum Glomeromycotina, of the phylum Mucoromycota (Spatafora et al., 2016). Four orders of AMF, namely, Glomerales, Archaeosporales, Paraglomerales, and Diversisporales, have been identified in this sub-phylum that also include 25 genera (Redecker et al., 2013). They are obligate biotrophs and ingest plant photosynthetic products (Bago et al., 2000) and lipids to accomplish their life cycle (Jiang et al., 2017). AMF-mediated growth promotion is not only by improving water and mineral nutrient uptake from the adjoining soil but also by safeguarding the plants from fungal pathogens (Smith and Read, 2008; Jung et al., 2012). Therefore, AMF are vital endosymbionts playing an effective role in plant productivity and the functioning of the ecosystem. They are of key importance for sustainable crop improvement (Gianinazzi et al., 2010).

Characteristics of AMF Symbiosis

The symbiosis of AMF with plants had been reported 400 million years ago (Selosse et al., 2015). Such types of links are established as a succession of biological processes, which lead to a variety of useful effects in both natural ecosystem and agricultural biotas (Van der Heijden et al., 2015). The symbiotic association of AMF is a classic example of mutualistic relationship, which can regulate the growth and development of plants. The mycelial network of fungi extends under the roots of the plant and promotes nutrient uptake that is otherwise not available. The fungal mycelium colonizes roots of many plants even if they belong to different species, resulting into a common mycorrhizal network (CMN). This CMN is considered as a primary component of the terrestrial ecosystem with its significant effects on different plant communities, particularly on invasive plants (Pringle et al., 2009) and the fungal-mediated transport of phosphorus (P) and nitrogen (N) to plants (Smith and Read, 2008). Moreover, communal nutrients also relocate from fungi to the plant, along with other related effects, which is probably why AMF improve plant tolerance to biotic and abiotic factors (Plassard and Dell, 2010). They have the ability to improve characteristics of soil and consequently encourage plant development in normal as well as in stressful circumstances (Navarro et al., 2014; Alqarawi et al., 2014a; Alqarawi et al., 2014b). AMF colonization improves tolerance of plants to stressful cues by bringing about several changes in their morpho-physiological traits (Alqarawi et al., 2014a; Alqarawi et al., 2014b; Hashem et al., 2015). AMF are considered as natural growth regulators of a majority of terrestrial flora. AMF are used as bio-inoculants, and researchers encourage their use as prominent bio-fertilizers in sustainable crop productivity (Barrow, 2012). Furthermore, AMF-inoculated soil forms more constant masses and significantly higher extra-radical hyphal mycelium than do the non-AMF-treated soils (Syamsiyah et al., 2018). Glomalin-related soil protein (GRSP) is believed to maintain water content in soils exposed to different abiotic stresses (Wu et al., 2014), which later on regulates water frequencies between soil and plants, automatically triggering plant development. Glomalin contains 30–40% C and its related compounds that safeguard soil from desiccation by enhancing the soil water holding capacity (Sharma et al., 2017). Growth-related functions, for example, stomatal conductance, leaf water potential, relative water content (RWC), PSII efficiency, and CO2 assimilation are affected by AMF inoculation (He et al., 2017; Chandrasekaran et al., 2019). AMF also help improve water stress tolerance by physiological alteration of the above-ground organs and tissues (Bárzana et al., 2012). Furthermore, inoculation of AMF improves the accumulation of dry matter and enhances water moisture uptake, consequently improving plant tolerance against stresses like drought and salinity. Exploitation of AMF for plant growth in various biological ecosystems can contribute greatly to organic culturing for growth promotion and yield maximization (Figure 1).

FIGURE 1
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Figure 1 A diagrammatic representation of mycorrhizal functions to regulate various processes in the ecosystem and plant growth promotion under abiotic stress condition.

AMF as a Bio-fertilizer

Bio-fertilizers are a mixture of naturally occurring substances that are used to improve soil fertility. These fertilizers are very useful for soil health as well as for plant growth and development (Sadhana, 2014). Different research studies conducted on AMF during the past two decades have highlighted their countless benefits on soil health and crop productivity. Therefore, it is widely believed that AMF could be considered as a replacement of inorganic fertilizers in the near future, because mycorrhizal application can effectively reduce the quantitative use of chemical fertilizer input especially of phosphorus (Ortas, 2012). Continuous use of inorganic fertilizers, herbicides, and fungicides has caused various problems to soil, plants, and human health, through their damaging impact on the quality of food products, soil health, and air and water systems (Yang et al., 2004). It is believed that AMF can possibly lower down the use of chemical fertilizers up to 50% for best agricultural production, but this estimate depends on the type of plant species and the prevalent stressful regimes (Table 1).

TABLE 1
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Table 1 Observed responses of plants to the inoculation application of AMF on host species exposed to various abiotic stress treatments.

AMF and Mineral Nutrition

Excessive land use may have a drastic impact on the overall biodiversity, which in turn may affect the ecosystem function as shown by several reports (Smith and Read, 1997; Balliu et al., 2015; Nouri et al., 2015; Wagg et al., 2015). A prominent role of such symbiotic relationship is to transfer nutrients, for example, organic carbon (C), in the form of lipids and sugars (Jiang et al., 2017; Luginbuehl et al., 2017). AMF colonization is widely believed to stimulate nutrient uptake in plants (Table 1). It is evident that inoculation of AMF can enhance the concentration of various macro-nutrients and micro-nutrients significantly, which leads to increased photosynthate production and hence increased biomass accumulation (Chen et al., 2017; Mitra et al., 2019). AMF have the capability to boost the uptake of inorganic nutrients in almost all plants, specifically of phosphate (Smith et al., 2003; Nell et al., 2010). AMF are also very effective in helping plants to take up nutrients from the nutrient-deficient soils (Kayama and Yamanaka, 2014). Apart from the macronutrients, AMF association has been reported to increase the phyto-availability of micronutrients like zinc and copper (Smith and Read, 1997). AMF improve the surface absorbing capability of host roots (Bisleski, 1973). Experimental trials on tomato plants inoculated with AMF have shown increased leaf area, and nitrogen, potassium, calcium, and phosphorus contents, reflecting enhanced plant growth (Balliu et al., 2015). AMF develop symbiosis with roots to obtain essential nutrients from the host plant and consequently provide mineral nutrients in return, for example, N, P, K, Ca, Zn, and S. Thus, AMF provide nutritional support to the plants even under inappropriate conditions inside the root cells. AMF produce fungal structures like arbuscules, which assist in exchange of inorganic minerals and the compounds of carbon and phosphorus, ultimately imparting a considerable vigor to host plants (Li et al., 2016b; Prasad et al., 2017). Therefore, they can significantly boost the phosphorus concentration in both root and shoot systems (Al-Hmoud and Al-Momany, 2017). Under phosphorus-limited conditions, mycorrhizal association improves phosphorus supply to the infected roots of host plants (Bucher, 2007). For example, Pi uptake rate was markedly improved in the AMF-colonized maize plants (Garcés-Ruiz, 2017). Increased photosynthetic activities and other leaf functions are directly related to improved growth frequency of AMF inoculation that is directly linked to the uptake of N, P, and carbon, which move towards roots and promote the development of tubers. It has been observed that AMF maintain P and N uptake ultimately helping in plant development at higher and lower P levels under different irrigation regimes (Liu et al., 2014; Liu et al., 2018). For example, mycorrhizal symbiosis positively increased the concentrations of N, P, and Fe in Pelargonium graveolens L. under drought stress (Amiri et al., 2017). Gomez-Bellot et al. (2015) reported improved levels of P, Ca, and K in Euonymus japonica under salinity stress due to instant fungus attachment. In another study, AMF-inoculated Pistachio plants exhibited high levels of P, K, Zn, and Mn under drought stress (Bagheri et al., 2012). In addition, AMF inoculation improved P and N contents in Chrysanthemum morifolium plant tissues (Wang et al., 2018) and increased seedling weight by improving water content and intercellular CO2, P, and N contents in Leymus chinensis (Jixiang et al., 2017).

It is believed that AMF improve the uptake of almost all essential nutrients and contrarily decrease the uptake of Na and Cl, leading to growth stimulation (Evelin et al., 2012). The extra-radical mycelium (ERM) can effectively improve nutrient uptake, thereby improving plant growth and development (Lehmann and Rillig, 2015). Nitrogen (N), being a main source of soil nutrition, is a well-known mineral fertilizer, even in those areas where there are enough livestock and farm-yard manure (FYM). Many scientists have reported the role of AMF in uptake of soil nutrients, especially of N and P, which can effectively promote the growth of host plants (Smith et al., 2011). In higher plants and some crops, N is a premier growth limiting factor. Several studies have explained that AMF have the ability to absorb and transfer N to the nearby plants or host plants (Hodge and Storer, 2015; Battini et al., 2017; Turrini et al., 2018). Zhang et al. (2018a) have demonstrated AMF mediated increased allocation of shoot biomass to panicles and grains through increased N and P redistribution to panicles particularly under low fertilizer levels. Translocation of N into seeds is enhanced from heading to maturity. AMF after establishing symbiosis produce extensive underground extra-radical mycelia ranging from the roots up to the surrounding rhizosphere, thereby helping in improving the uptake of nutrients specifically N (Battini et al., 2017). The interaction of salinity stress and AMF significantly affects the concentrations of P and N and the N:P ratio in plant shoots (Wang et al., 2018). Recently, it has been reported that native AMF treatments produce significant alterations in the N contents of crop plants (Turrini et al., 2018).

It has been widely accepted that fungi have the ability to take substantial amount of N from dead and decomposed material that later increases their fitness to grow and stay alive. Apart from this, large biomass and increased N requirements for AMF render them the main stakeholder of global N pool that is equivalent in scale to fine roots. Thus, they play a pivotal role in the N cycle (Hodge and Fitter, 2010). The AMF extra-radical hyphae can absorb and assimilate inorganic N (Jin et al., 2005). Several studies have shown that approximately 20–75% of the total N uptake of AM plants can be transferred by the AMF to their hosts (Tanaka and Yano, 2005; Govindarajulu et al., 2005; Ahanger et al., 2014; Hameed et al., 2014; Hashem et al., 2018). Increased N in AMF-colonized plants evidently results in higher chlorophyll contents, as chlorophyll molecules can effectively trap N (De Andrade et al., 2015). Other evidences favoring the AMF-mediated improvement in plant N nutrition can also be seen in the literature (Courty et al., 2015; Bucking and Kafle, 2015; Corrêa et al., 2015). AMF inoculation improves C and N accumulation and N assimilation under ambient and elevated CO2 concentrations (Zhu et al., 2016). For example, in olive plants, AMF were reported to improve growth, accumulation of micro-nutrients and macro-nutrients, and their allocation in the plantlets grown under increased levels of Mn (Bati et al., 2015).

Enhancement of plant nutrition and maintenance of Ca2+ and Na+ ratio are the significant dynamic attributes that help improve beneficial aspects of AMF colonization on overall plant performance (Evelin et al., 2012; Abdel Latef and Miransari, 2014). Improved growth and levels of protein, Fe, and Zn were found in mycorrhizal chickpea (Pellegrino and Bedini, 2014). Moreover, different reports have shown enhanced activity of a K+ transporter in the mycorrhizal roots of Lotus japonicus (Guether et al., 2009; Berruti et al., 2016). Moreover, two meta-analysis reports that appeared a few years ago showed the role of mycorrhizal symbiosis to various micro-nutrients in crops (Lehmann et al., 2014; Lehmann and Rillig, 2015; as reviewed by Berruti et al., 2016). Asrar et al. (2012) reported that the specified fungal association enhanced the contents of macronutrients such as N, P, K, Ca, and Mg of Antirrhinum majus under drought. AMF also proved to be effective in restricting the high accumulation of Na, Mn, Mg, and Fe in roots (Bati et al., 2015). Several studies conducted during the last few years have shown that AMF, such as Glomus mosseae and Rhizophagus irregularis exhibited improved heavy metal translocation in the shoot (Zaefarian et al., 2013; Ali et al., 2015). Micronutrients such as Zn and Cu being diffusion limited in soils are absorbed by plants with the help of mycorrhizal hyphae.

AMF and Plant Yield

Beneficial rhizosphere microorganisms not only can improve the nutrient status of crops, as described above, but also can enhance the quality of crops. For example, AMF-colonized strawberry exhibited increased levels of secondary metabolites resulting in improved antioxidant property (Castellanos-Morales et al., 2010). AMF can enhance the dietary quality of crops by affecting and production of carotenoids and certain volatile compounds (Hart et al., 2015). Bona et al. (2017) observed beneficial effects of AMF on the quality of tomatoes. In another study, Zeng et al. (2014) have reported increased contents of sugars, organic acids, vitamin C, flavonoids, and minerals due to Glomus versiforme resulting in enhanced citrus fruit quality. Mycorrhizal symbiosis induces enhanced accumulation of anthocyanins, chlorophyll, carotenoids, total soluble phenolics, tocopherols, and various mineral nutrients (Baslam et al., 2011). AMF have been employed in a large-scale field production of maize (Sabia et al., 2015), yam (Lu et al., 2015), and potato (Hijri, 2016), confirming that AMF possess a considerable potential for enhancing crop yield. AMF can also enhance the biosynthesis of valuable phytochemicals in edible plants and make them fit for healthy food production chain (Sbrana et al., 2014; Rouphael et al., 2015).

Rouphael et al. (2015) have reported that the abiotic stress mitigation by AMF could occur through maintenance of soil pH, thereby protecting its horticultural value. In addition, AMF can also play a critical role in improving the resistance of plants to stressful environments, as described below.

AMF and Abiotic Stresses

Drought

Drought stress affects plant life in many ways; for example, shortage of water to roots reduces rate of transpiration as well as induces oxidative stress (Impa et al., 2012; Hasanuzzaman et al., 2013). Drought stress imparts deleterious effects on plant growth by affecting enzyme activity, ion uptake, and nutrient assimilation (Ahanger and Agarwal, 2017; Ahanger et al., 2017a). However, there is a strong evidence of drought stress alleviation by AMF in different crops such as wheat, barley, maize, soybean, strawberry, and onion (Mena-Violante et al., 2006; Ruiz-Lozano et al., 2015; Yooyongwech et al., 2016; Moradtalab et al., 2019). Plant tolerance to drought could be primarily due to a large volume of soil explored by roots and the extra-radical hyphae of the fungi (Gianinazzi et al., 2010; Orfanoudakis et al., 2010; Gutjahr and Paszkowski, 2013; Zhang et al., 2016).

Such a symbiotic association is believed to regulate a variety of physio-biochemical processes in plants such as increased osmotic adjustment (Kubikova et al., 2001), stomatal regulation by controlling ABA metabolism (Duan et al., 1996), enhanced accumulation of proline (Ruiz-Sánchez et al., 2010; Yooyongwech et al., 2013), or increased glutathione level (Rani, 2016). Symbiotic relationship of various plants with AMF may ultimately improve root size and efficiency, leaf area index, and biomass under the instant conditions of drought (Al-Karaki et al., 2004; Gholamhoseini et al., 2013). Moreover, AMF and their interaction with the host plant are helpful in supporting plants against severe environmental conditions (Ruiz-Lozano, 2003; Table 1). The AMF symbiosis also results in enhanced gas exchange, leaf water relations, stomatal conductance, and transpiration rate (Morte et al., 2000; Mena-Violante et al., 2006). AMF can facilitate ABA responses that regulate stomatal conductance and other related physiological processes (Ludwig-Müller, 2010). Recently, Li et al. (2019) have demonstrated AMF-mediated enhancement in growth and photosynthesis in C3 (Leymus chinensis) and C4 (Hemarthria altissima) plant species through up-regulation of antioxidant system.

Salinity

It is widely known that the soil salinization is an increasing environmental problem posing a severe threat to global food security. Salinity stress is known to suppress growth of plants by affecting the vegetative development and net assimilation rate resulting in reduced yield productivity (Hasanuzzaman et al., 2013; Ahanger et al., 2017a). It also promotes the excessive generation of reactive oxygen species (Ahmad et al., 2010; Ahanger and Agarwal, 2017; Ahanger et al., 2017b; Ahanger et al., 2018). Attempts are being made to explore potential means of achieving enhanced crop production under salt affected soils. One such potential means is the judicious use of AMF for mitigating the salinity-induced adverse effects on plants (Santander et al., 2019). Several research studies have reported the efficiency of AMF to impart growth and yield enhancement in plants under salinity stress (Talaat and Shawky, 2014; Abdel Latef and Chaoxing, 2014; Table 1). El-Nashar (2017) reported that AMF enhanced growth rate, leaf water potential, and water use efficiency of the Antirrhinum majus plants. Recently, Ait-El-Mokhtar et al. (2019) have reported the beneficial effects of AMF symbiosis on physiological parameters such as photosynthetic rate, stomatal conductance, and leaf water relations under saline regimes. AMF significantly alleviated the deleterious effects on photosynthesis under salinity stress (Sheng et al., 2011). Mycorrhizal inoculation markedly improved photosynthetic rate, and other gas exchange traits, chlorophyll content, and water use efficiency in Ocimum basilicum L. under saline conditions (Elhindi et al., 2017). AMF-inoculated Allium sativum plants showed improved growth traits including leaf area index, and fresh and dry biomass under saline conditions (Borde et al., 2010). Recently, Wang et al. (2018) have reported considerable enhancement in fresh and dry weights, and N concentration of shoot and root due to mycorrhizal inoculation under moderate saline conditions.

Furthermore, plants possessing AMF show enhanced synthesis of jasmonic acid, salicylic acid, and several important inorganic nutrients. For example, concentrations of total P, Ca2+, N, Mg2+, and K+ were higher in the AMF-treated Cucumis sativus plants compared with those in the uninoculated plants under salt stress conditions (Hashem et al., 2018). Mycorrhizal inoculation to Capsicum annuum exhibited enhanced chlorophyll contents, and Mg2+ and N uptake coupled with reduced Na+ transport under saline conditions (Cekic et al., 2012). In addition, Santander et al. (2019) have shown with lettuce that the mycorrhizal plants had higher biomass production, increased synthesis of proline, increased N uptake, and noticeable changes in ionic relations, particularly reduced accumulation of Na+, than those in non-mycorrhizal plants under stress conditions. AMF inoculation can effectively regulate the levels of key growth regulators. For example, Hameed et al. (2014) and Talaat and Shawky (2014) have observed AMF-mediated improvement in cytokinin concentration resulting in a marked photosynthate translocation under salinity stress. In addition, AMF-mediated growth promotion under salinity stress was shown to be due to alteration in the polyamine pool (Kapoor et al., 2013). Furthermore, Aroca et al. (2013) showed that enhanced strigolactone in AMF-treated plants notably mitigated various salinity effects in lettuce plants. AMF-colonized plants have the ability to decrease oxidative stress by suppressing lipid membrane peroxidation under salinity stress (Abdel Latef and Chaoxing, 2014; Talaat and Shawky, 2014). Furthermore, inoculation of AMF was also observed to enhance the accumulation of various organic acids resulting in up-regulation of the osmoregulation process in plants grown under saline stress. For example, Sheng et al. (2011) observed an enhanced synthesis/accumulation of certain organic acids in maize plants growing in saline soil, and AMF induced increased production of betaine, confirming the indirect role of AMF in plant osmoregulation under salinity stress.

Heavy Metals

AMF are widely believed to support plant establishment in soils contaminated with heavy metals, because of their potential to strengthen defense system of the AMF mediated plants to promote growth and development. Heavy metals may accumulate in food crops, fruits, vegetables, and soils, causing various health hazards (Liu et al., 2013; Yousaf et al., 2016). AMF association with wheat positively increased nutrient uptake under aluminum stress (Aguilera et al., 2014). Plants grown on soils enriched with Cd and Zn exhibit considerable suppression in shoot and root growth, leaf chlorosis, and even death (Moghadam, 2016). There are many reports in the literature on uncovering the AMF-induced effects on the buildup of metals in plants (Souza et al., 2012; Table 1). Heavy metals can be immobilized in the fungal hyphae of internal and external origin (Ouziad et al., 2005) that have the ability to fix heavy metals in the cell wall and store them in the vacuole or may chelate with some other substances in the cytoplasm (Punamiya et al., 2010) and hence reduce metal toxicity in the plants. The strong effects of AMF on plant development and growth under severe stressful conditions are most often due to the ability of these fungi in increasing morphological and physiological processes that increase plant biomass and consequently uptake of important immovable nutrients like Cu, Zn, and P and thus reduced metal toxicity in the host plants (Kanwal et al., 2015; Miransari, 2017). It is also believed that enhanced growth or chelation in the rhizospheric soil can cause metal dilution in plant tissues (Kapoor et al., 2013; Audet, 2014). AMF reportedly bind Cd and Zn in the cell wall of mantle hyphae and cortical cells, thereby restricting their uptake and resulting in improved growth, yield, and nutrient status (Andrade and Silveira, 2008; Garg and Chandel, 2012).

Mycorrhizae can disturb the uptake of different metals into plants from the rhizosphere and their movement from the root zone to the aerial parts (Dong et al., 2008; Li et al., 2015). Mycelia of various AMF have a high cation-exchange capacity and absorption of metals (Takács and Vörös, 2003). Metal non-adapted AMF settle the polluted soils and reduce uptake and accumulation of heavy metals, as observed in perennial ryegrass (Lolium perenne) in artificially polluted soil with various elements like Cd, Ni, and Zn (Takács and Vörös, 2003). AMF are believed to regulate the uptake and accumulation of some key inorganic nutrients. For example, enhanced uptake of Si has been reported in mycorrhiza-inoculated plants like Glycine max (Yost and Fox, 1982) and Zea mays (Clark and Zeto, 2000). Hammer et al. (2011) also recorded considerable uptake of Si in spores and hyphae of Rhizophagus irregularis and its transfer to the host roots. It is pertinent that low Cd mobility and toxicity can also be addressed with AMF by increasing soil pH (Shen et al., 2006), restoring Cd in the extra-radical mycelium (Janouškova and Pavlíková, 2010), and binding Cd to glomalin, a glycoprotein. For example, in rice, AMF were very effective in lowering the levels of Cd in both the vacuoles and cell wall, which brought about Cd detoxification (Li et al., 2016a). Wang et al. (2012) observed that AMF-mediated improved Cd tolerance in alfalfa (Medicago sativa L.) had been possibly due to the modification of chemical forms of Cd in different plant tissues. Various processes that occur through the AMF are immobilization/restriction of metal compounds, precipitation of polyphosphate granules in the soil, adsorption to fungal cell wall chitin, and heavy metal chelation inside the fungus (Figure 1).

Temperature (High and Low)

As soil temperatures increase, plant community reactions may be dependent on AMF interactions for sustainable yield and production (Bunn et al., 2009). Heat stress significantly affects plant growth and development by imparting i) loss of plant vigor and inhibition of seed germination, ii) retarded growth rate, iii) decreased biomass production, iv) wilting and burning of leaves and reproductive organs, v) abscission and senescence of leaves, vi) damage as well as discoloration of fruit, vii) reduction in yield and cell death (Wahid et al., 2007; Hasanuzzaman et al., 2013), and viii) enhanced oxidative stress. Generally, AMF-inoculated plants show better growth under heat stress than do the non-AMF-inoculated ones (Gavito et al., 2005). Maya and Matsubara (2013) have reported the association of AMF Glomus fasciculatum with plant growth and development leading to positive changes in growth under the conditions of high temperature (Figure 2; Table 1).

FIGURE 2
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Figure 2 AMF inoculation alleviates temperature stress in plants.

AMF can increase plant tolerance to cold stress (Birhane et al., 2012; Chen et al., 2013; Liu et al., 2013). Moreover, a majority of reports state that various plants inoculated with AMF at low temperature grow better than non-AMF-inoculated plants (Zhu et al., 2010b; Abdel Latef and Chaoxing, 2011b; Chen et al., 2013; Liu et al., 2013). AMF support plants in combating cold stress and eventually improve plant development (Gamalero et al., 2009; Birhane et al., 2012). Moreover, AMF also can retain moisture in the host plant (Zhu et al., 2010a), increase plant secondary metabolites leading to strengthen plant immune system, and increase protein content for supporting the plants to combat cold stress conditions (Abdel Latef and Chaoxing, 2011b). For example, during cold stress, AMF-inoculated plants showed an enhanced water conservation capacity as well as its use efficiency (Zhu et al., 2010b). Symbiotic AMF relationship improves water and plant relationships and increases gas exchange potential and osmotic adjustment (Zhu et al., 2012). AMF improve the synthesis of chlorophyll leading to a significant improvement in the concentrations of various metabolites in plants subjected to cold stress conditions (Zhu et al., 2010a; Abdel Latef and Chaoxing, 2011b). The role of AMF during cold stress has also been reported to alter protein content in tomato and other vegetables (Abdel Latef and Chaoxing, 2011b).

AMF and Combined Abiotic Stresses

It is widely accepted that AMF could alleviate various stresses or combination of stresses that include, drought, salinity, temperature, nutrients, and heavy metals. For example, exposure of plants to a combination of drought and salinity causes an enhanced production of reactive oxygen species, which can be highly injurious to plants (Bauddh and Singh, 2012). Detoxification of reactive oxygen species (ROS) is done by the enzymes that include commonly superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), and glutathione reductase (GR) (Ahanger and Agarwal, 2017). In addition, combined application of drought and salinity to tomato plants inoculated with Scolecobasidium constrictum showed improved biomass production, leaf water relations, stomatal conductance, and Fv/Fm relative to those in non-inoculated plants (Duc et al., 2018). Thus, AMF are critical for improving plant growth and yield under stress (Abdel Latef, 2011; Abdel Latef and Chaoxing, 2011a; Abdel Latef and Chaoxing, 2011b; Abdel Latef and Chaoxing, 2014). Very rare research reports are available in the literature demonstrating the role of AMF in mitigation of combined effects of two or more stresses. AMF symbiosis protects plants against a variety of abiotic stresses using various processes such as improved photosynthetic rate, uptake and accumulation of mineral nutrients, accumulation of osmoprotectants, up-regulation of antioxidant enzyme activity, and change in the rhizosphere ecosystem (Bárzana et al., 2015; Calvo-Polanco et al., 2016; Yin et al., 2016). Several studies have shown improved nutritional status of AMF plants under osmotic stress conditions (Augé et al., 2014; Lehmann et al., 2014; Lehmann and Rillig, 2015) resulting from deficit irrigation or salinity. Similarities among the tolerance mechanisms may occur in response to AMF-mediated combined stress adaptations. It is proposed that AMF-mediated alterations in phytohormone profile, mineral uptake and assimilation, accumulation of compatible osmolytes and secondary metabolites, and up-regulation of antioxidant system can be the common mechanisms induced during different stresses. However, specific mechanisms like compartmentation and sequestration of toxic ions, production of phytochelatins, and protein expression can be specific and exhibit a significant change with stress type and the AMF species involved. Changes in root characteristics like hydraulic conductivities can improve the osmotic stress tolerance to considerable levels (Evelin et al., 2009). Zhang et al. (2018b) have shown that the AMF protected castor bean against saline stress by altering gas exchange traits and the levels of some key metabolites. The said characteristics of AMF may elevate nutraceutical quality of crops and could be of considerable agronomic importance for production and management of different potential crops. However, extensive studies are required to unravel the role of AMF in counteracting the effects of combined stresses.

Conclusion and Future Prospects

A few research reports have already documented the beneficial role of AMF in improving plant growth under stressful environments. Therefore, in this review, the existing information related to the role of AMF has been combined in a coherent way for understanding of AMF symbiotic relationship with a variety of plants under stress environments. Previously, the AMF have been mainly discussed as beneficial entities for nutrient uptake from soil; however, recently, it has been clearly depicted that plants inoculated with AMF can effectively combat various environmental cues, like salinity, drought, nutrient stress, alkali stress, cold stress, and extreme temperatures, and thus help increase per hectare yield of a large number of crops and vegetables. Encouragement of AMF usage is of immense importance for modern global agricultural systems for their consistent sustainability. Undoubtedly, exploitation of AMF for agricultural improvement can significantly reduce the use of synthetic fertilizers and other chemicals, thereby promoting the bio-healthy agriculture. AMF-mediated growth and productivity enhancement in crop plants can be beneficial to overcome the consumption requirement of increasing population across the globe. In addition, environment-friendly technologies shall be highly encouraged due to their widespread use. The primary focus of future research should be on the identification of genes and gene products controlling the AMF mediated growth and development regulation under stressful cues. Identification of both host as well as AMF specific protein factors regulating symbiotic association and the major cellular and metabolic pathways under different environmental stresses can be hot areas for future research in this field. Understanding the AMF induced modulations in the tolerance mechanisms and the crosstalk triggered to regulate plant performance can help improve crop productivity. Taken together, AMF must be explored at all levels to further investigate their role in nature as a bio-fertilizer for sustainable agricultural production.

Author Contributions

NB, CQ, MAA, SR, MIK, NA, and LZ contributed equally in preparation of this manuscript. MA helped considerably in writing of this manuscript and made final corrections.

Funding

This work was supported by the National Key Research and Development Program of China (2017YFE0114000), Sci-tec Project of China Tobacco Shaanxi Industrial Co. Ltd. (SXYC-2016-KJ-02) and Sci-tec Project of Shaanxi China Tobacco Industrial Co., Ltd. (JS-FW-2016-001).

Conflict of Interest Statement

All authors declare that there is no potential conflict of interest with any commercial or financial institution other than acknowledged in “Funding” section of this manuscript.

Acknowledgments

The authors thank Professor Rana Munns, CSIRO, Australia, for critical editing of the final draft of the manuscript and thankfully acknowledge the Northwest A&F University Shaanxi-China for providing the necessary facilities.

References

Abdel Latef, A. A. (2011). Influence of arbuscular mycorrhizal fungi and copper on growth, accumulation of osmolyte, mineral nutrition and antioxidant enzyme activity of pepper (Capsicum annuum L.). Mycorrhiza 21, 495–503. doi: 10.1007/s00572-010-0360-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Abdel Latef, A. A., Chaoxing, H. (2011a). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci. Hort. 127, 228–233. doi: 10.1016/j.scienta.2010.09.020

CrossRef Full Text | Google Scholar

Abdel Latef, A. A., Chaoxing, H. (2011b). Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol. Plant. 33, 1217–1225. doi: 10.1007/s11738-010-0650-3

CrossRef Full Text | Google Scholar

Abdel Latef, A. A., Chaoxing, H. J. (2014). Does the inoculation with Glomus mosseae improve salt tolerance in pepper plants? Plant Grow. Regul. 33, 644–653. doi: 10.1007/s00344-014-9414-4

CrossRef Full Text | Google Scholar

Abdel Latef, A. A., Miransari, M. (2014). The role of arbuscular mycorrhizal fungi in alleviation of salt stress. Use of microbes for the alleviation of soil stresses. New York, USA: Springer. Science+Business Media, 23–38. doi: 10.1007/978-1-4939-0721-2_2

CrossRef Full Text | Google Scholar

Abdelhameed, R. E., Rabab, A. M. (2019). Alleviation of cadmium stress by arbuscular mycorrhizal symbiosis. Int. J. Phytoremed. doi: 10.1080/15226514.2018.1556584

CrossRef Full Text | Google Scholar

Aguilera, P., Pablo, C., Fernando, B., Fritz, O. (2014). Diversity of arbuscular mycorrhizal fungi associated with Triticum aestivum L. plants growing in an andosol with high aluminum level. Agri. Eco. Environ. 186, 178–184. doi: 10.1016/j.agee.2014.01.029

CrossRef Full Text | Google Scholar

Ahanger, M. A., Alyemeni, M. N., Wijaya, L., Alamri, S. A., Alam, P., Ashraf, M., et al. (2018). Potential of exogenously sourced kinetin in protecting Solanum lycopersicum from NaCl-induced oxidative stress through up-regulation of the antioxidant system, ascorbate–glutathione cycle and glyoxalase system. PLoS One 13 (9), e0202–e0175. doi: 10.1371/journal.pone.0202175

CrossRef Full Text | Google Scholar

Ahanger, M. A., Agarwal, R. M. (2017). Potassium up-regulates antioxidant metabolism and alleviates growth inhibition under water and osmotic stress in wheat (Triticum aestivum L.). Protoplasma 254 (4), 1471–1486. doi: 10.1007/s00709-016-1037-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Ahanger, M. A., Tittal, M., Mir, R. A., Agarwal, R. M. (2017a). Alleviation of water and osmotic stress-induced changes in nitrogen metabolizing enzymes in Triticum aestivum L. cultivars by potassium. Protoplasma 254 (5), 1953–1963. doi: 10.1007/s00709-017-1086-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Ahanger, M. A., Tomar, N. S., Tittal, M., Argal, S., Agarwal, R. M. (2017b). Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol. Mol. Biol. Plants. 23 (4), 731–744. doi: 10.1007/s12298-017-0462-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Ahanger, M. A., Tyagi, S. R., Wani, M. R., Ahmad, P. (2014). “Drought tolerance: role of organic osmolytes, growth regulators, and mineral nutrients,” in Physiological mechanisms and adaptation strategies in plants under changing environment, vol. 1 . Eds. Ahmad, P., Wani, MR (New York, NY: Springer), 25–55. doi: 10.1007/978-1-4614-8591-9_2

CrossRef Full Text | Google Scholar

Ahmad, P., Jaleel, C. A., Salem, M. A., Nabi, G., Sharma, S. (2010). Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit. Rev. Biotechnol. 30, 161–175. doi: 10.3109/07388550903524243

PubMed Abstract | CrossRef Full Text | Google Scholar

Ait-El-Mokhtar, M., Laouane, R. B., Anli, M., Boutasknit, A., Wahbi, S., Meddich, A. (2019). Use of mycorrhizal fungi in improving tolerance of the date palm (Phoenix dactylifera L.) seedlings to salt stress. Sci. Hori. 253, 429–438. doi: 10.1016/j.scienta.2019.04.066

CrossRef Full Text | Google Scholar

Al-Hmoud, G., Al-Momany, A. (2017). Effect of four mycorrhizal products on squash plant growth and its effect on physiological plant elements. Adv. Crop. Sci. Tech. 5, 260. doi: 10.4172/2329-8863.1000260

CrossRef Full Text | Google Scholar

Ali, N., Masood, S., Mukhtar, T., Kamran, M. A., Rafique, M., Munis, M. F. H., et al. (2015). Differential effects of cadmium and chromium on growth, photosynthetic activity, and metal uptake of Linum usitatissimum in association with Glomus intraradices. Environ. Monitor. Assess. 187 (6), 311. doi: 10.1007/s10661-015-4557-8

CrossRef Full Text | Google Scholar

Al-Karaki, G., Mcmichael, B., Zak, J. (2004). Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mychorrhiza 14, 263–269. doi: 10.1007/s00572-003-0265-2

CrossRef Full Text | Google Scholar

Alqarawi, A. A., Abd-Allah, E. F., Hashem, A. (2014a). Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J. Plant. Interact. 9 (1), 802–810. doi: 10.1080/17429145.2014.949886

CrossRef Full Text | Google Scholar

Alqarawi, A. A., Hashem, A., Abd_Allah, E. F., Alshahrani, T. S., Huqail, A. A. (2014b). Effect of salinity on moisture content, pigment system, and lipid composition in Ephedra alata Decne. Acta Biol. Hung. 65 (1), 61–71. doi: 10.1556/ABiol.65.2014.1.6

PubMed Abstract | CrossRef Full Text | Google Scholar

Amiri, R., Ali, N., Nematollah, E., Mohammad, R. S. (2017). Nutritional status, essential oil changes and water-use efficiency of rose geranium in response to arbuscular mycorrhizal fungi and water deficiency stress. Symbiosis 73, 15–25. doi: 10.1007/s13199-016-0466-z

CrossRef Full Text | Google Scholar

Amiri, R., Nikbakht, A., Etemadi, N. (2015). Alleviation of drought stress on rose geranium Pelargonium graveolen L Herit. in terms of antioxidant activity and secondary metabolites by mycorrhizal inoculation. Sci. Hort. 197, 373–380. doi: 10.1016/j.scienta.2015.09.062

CrossRef Full Text | Google Scholar

Andrade, S. A. L., Silveira, A. P. D. (2008). Mycorrhiza influence on maize development under Cd stress and P supply. Braz. J. Plant Physiol. 20 (1), 39–50. doi: 10.1590/S1677-04202008000100005

CrossRef Full Text | Google Scholar

Aroca, R., Ruiz-Lozano, J. M., Zamarreño, A. M., Paz, J.A., García-Mina, J. M., Pozo, J. A., et al. (2013). Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 170, 47–55. doi: 10.1016/j.jplph.2012.08.020

PubMed Abstract | CrossRef Full Text | Google Scholar

Asrar, A. A., Abdel-Fattah, G. M., Elhindi, K. M. (2012). Improving growth, flower yield, and water relations of snapdragon Antirhinum majus L. plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica 50, 305–316. doi: 10.1007/s11099-012-0024-8

CrossRef Full Text | Google Scholar

Audet, P. (2014). “Arbuscular mycorrhizal fungi and metal phytoremediation: ecophysiological complementarity in relation to environmental stress,” in Emerging technologies and management of crop stress tolerance. Eds. Ahmad, P., Rasool, S. (San Diego: Academic Press), 133–160. doi: 10.1016/B978-0-12-800875-1.00006-5

CrossRef Full Text | Google Scholar

Augé, R. M., Toler, H. D., Saxton, A. M. (2014). Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front. Plant. Sci. 5, 562. doi: 10.3389/fpls.2014.00562

PubMed Abstract | CrossRef Full Text | Google Scholar

Bagheri, V., Shamshiri, M. H., Shirani, H., Roosta, H. (2012). Nutrient uptake and distribution in mycorrhizal pistachio seedlings under drought stress. J. Agric. Sci. Technol. 14, 1591–1604. doi: 10.5367/oa.2012.0109

CrossRef Full Text | Google Scholar

Bago, B., Pfeffer, P. E., Shachar-Hill, Y. (2000). Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 124, 949–958. doi: 10.1104/pp.124.3.949

PubMed Abstract | CrossRef Full Text | Google Scholar

Balliu, A., Sallaku, G., Rewald, B. (2015). AMF Inoculation enhances growth and improves the nutrient uptake rates of transplanted, salt-stressed tomato seedlings. Sustainability 7, 15967–15981. doi: 10.3390/su71215799

CrossRef Full Text | Google Scholar

Barrow, C. J. (2012). Biochar potential for countering land degradation and for improving agriculture. App. Geogr. 34, 21–28. doi: 10.1016/j.apgeog.2011.09.008

CrossRef Full Text | Google Scholar

Bárzana, G., Aroca, R., Paz, J. A., Chaumont, F., Martinez-Ballesta, M. C., Carvajal, M., et al. (2012). Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann. Bot. 109, 1009–1017. doi: 10.1093/aob/mcs007

PubMed Abstract | CrossRef Full Text | Google Scholar

Bárzana, G., Aroca, R., Ruiz-Lozano, J. M. (2015). 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. 38, 1613–1627. doi: 10.1111/pce.12507

PubMed Abstract | CrossRef Full Text | Google Scholar

Baslam, M., Garmendia, I., Goicoechea, N. (2011). Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse grown lettuce. J. Agric. Food Chem. 59, 5504–C5515. doi: 10.1021/jf200501c

PubMed Abstract | CrossRef Full Text | Google Scholar

Bati, C. B., Santilli, E., Lombardo, L. (2015). Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels. Mycorrhiza 25 (2), 97–108. doi: 10.1007/s00572-014-0589-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Battini, F., Grønlund, M., Agnolucci, M., Giovannetti, M., Jakobsen, I. (2017). Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Sci. Rep. 7, 4686. doi: 10.1038/s41598-017-04959-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Bauddh, K., Singh, R. P. (2012). 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. 85, 13–22. doi: 10.1016/j.ecoenv.2012.08.019

PubMed Abstract | CrossRef Full Text | Google Scholar

Bayani, R., Saateyi, A., Faghani, E. (2015). Influence of arbuscular mycorrhiza in phosphorus acquisition efficiency and drought-tolerance mechanisms in barley Hordeum vulgare L. Int. J. Biosci. 7, 86–94. doi: 10.12692/ijb/7.1.86-94

CrossRef Full Text | Google Scholar

Berruti, A., Lumini, E., Balestrini, R., Bianciotto, V. (2016). Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front. Microbiol. 6, 1559. doi: 10.3389/fmicb.2015.01559

PubMed Abstract | CrossRef Full Text | Google Scholar

Birhane, E., Sterck, F., Fetene, M., Bongers, F., Kuyper, T. (2012). Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169, 895–904. doi: 10.1007/s00442-012-2258-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Bisleski, R. L. (1973). Phosphate pools, phosphate transport, and phosphate availability. Annu. Rev. Plant Physiol. 24, 225–252. doi: 10.1146/annurev.pp.24.060173.001301

CrossRef Full Text | Google Scholar

Bona, E., Cantamessa, S., Massa, N., Manassero, P., Marsano, F., Copetta, A., et al. (2017). Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study. Mycorrhiza 27, 1–C11. doi: 10.1007/s00572-016-0727-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Borde, M., Dudhane, M., Jite, P. K. (2010). AM fungi influences the photosynthetic activity, growth and antioxidant enzymes in Allium sativum L. under salinity condition. Not. Sci. Biol. 2, 64–71. doi: 10.15835/nsb245434

CrossRef Full Text | Google Scholar

Bowles, T. M., Barrios-Masias, F. H., Carlisle, E. A., Cavagnaro, T. R., Jackson, L. E. (2016). Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci. Total Environ. 566, 1223–1234. doi: 10.1016/j.scitotenv.2016.05.178

PubMed Abstract | CrossRef Full Text | Google Scholar

Boyer, L. R., Brain, P., Xu, X. M., Jeffries, P. (2014). Inoculation of drought-stressed strawberry with a mixed inoculum of two arbuscular mycorrhizal fungi: effects on population dynamics of fungal species in roots and consequential plant tolerance to water. Mycorrhiza 25 (3), 215–227. doi: 10.1007/s00572-014-0603-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Bucher, M. (2007). Functional biology of plant phosphate uptake at root and mycorrhizae interfaces. New Phytol. 173, 11–26. doi: 10.1111/j.1469-8137.2006.01935.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Bucking, H., Kafle, A. (2015). Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5, 587–612. doi: 10.3390/agronomy5040587

CrossRef Full Text | Google Scholar

Bunn, R., Lekberg, Y., Zabinski, C. (2009). Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants. Ecology 90 (5), 1378–1388. doi: 10.1890/07-2080.1

PubMed Abstract | CrossRef Full Text | Google Scholar

Cabral, C., Sabine, R., Ivanka, T., Bernd, W. (2016). Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress. Plant Soil 408 (1–2), 385–399. doi: 10.1007/s11104-016-2942-x

CrossRef Full Text | Google Scholar

Calvo-Polanco, M., Sanchez-Romera, B., Aroca, R., Asins, M. J., Declerck, S., Dodd, I. C., et al. (2016). 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. 131, 47–57. doi: 10.1016/j.envexpbot.2016.06.015

CrossRef Full Text | Google Scholar

Castellanos-Morales, V., Villegas, J., Wendelin, S., Vierheiling, H., Eder, R., Cardenas-Navarro, R. (2010). Root colonization by the arbuscular mycorrhizal fungus Glomus intraradices alters the quality of strawberry fruit (Fragaria ananassa Duch.) at different nitrogen levels. J. Sci. Food Agric. 90, 1774–1782. doi: 10.1002/jsfa.3998

PubMed Abstract | CrossRef Full Text | Google Scholar

Cekic, F. O., Unyayar, S., Ortas, I. (2012). Effects of arbuscular mycorrhizal inoculation on biochemical parameters in capsicum annuum grown under long term salt stress. Turk. J. Bot. 36, 63–72. doi: 10.3906/bot-1008-32

CrossRef Full Text | Google Scholar

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

PubMed Abstract | CrossRef Full Text | Google Scholar

Chen, S., Jin, W., Liu, A., Zhang, S., Liu, D., Wang, F., et al. (2013). Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Sci. Hort. 160, 222–229. doi: 10.1016/j.scienta.2013.05.039

CrossRef Full Text | Google Scholar

Chen, S., Zhao, H., Zou, C., Li, Y., Chen, Y., Wang, Z., et al. (2017). Combined Inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front. Microbiol. 8, 25–16. doi: 10.3389/fmicb.2017.02516

PubMed Abstract | CrossRef Full Text | Google Scholar

Clark, R. B., Zeto, S. K. (2000). Mineral acquisition by arbuscular mycorrhizal plants. J. Plant Nutr. 23, 867–902. doi: 10.1080/01904160009382068

CrossRef Full Text | Google Scholar

Corrêa, A., Cruz, C., Ferrol, N. (2015). Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown. Mycorrhiza 25, 499–515. doi: 10.1007/s00572-015-0627-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Courty, P. E., Smith, P., Koegel, S., Redeckerm, D., Wipf, D. (2015). Inorganic nitrogen uptake and transport in beneficial plant root–microbe interactions. Crit. Rev. Plant Sci. 34, 4–16. doi: 10.1080/07352689.2014.897897

CrossRef Full Text | Google Scholar

De Andrade, S. A. L., Domingues, A. P., Mazzafera, P. (2015). Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere 134, 141–149. doi: 10.1016/j.chemosphere.2015.04.023

PubMed Abstract | CrossRef Full Text | Google Scholar

Dong, Y., Zhu, Y. G., Smith, F. A., Wang, Y., Chen, B. (2008). 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. 155, 174–181. doi: 10.1016/j.envpol.2007.10.023

PubMed Abstract | CrossRef Full Text | Google Scholar

Duan, X., Neuman, D. S., Reiber, J. M., Green, C. D., Arnold, M., Saxton, A. M., et al. (1996). Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J. Exp. Bot. 47 (303), 1541–1550. doi: 10.1093/jxb/47.10.1541

CrossRef Full Text | Google Scholar

Duc, N. H., Csintalan, Z., Posta, K. (2018). Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol. Biochem. 132, 297–307. doi: 10.1016/j.plaphy.2018.09.011

PubMed Abstract | CrossRef Full Text | Google Scholar

Elhindi, K. M., El-Din, S. A., Elgorban, A. M. (2017). The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L.). Saudi J. Biol. Sci. 24, 170–179. doi: 10.1016/j.sjbs.2016.02.010

PubMed Abstract | CrossRef Full Text | Google Scholar

EL-Nashar, Y. I. (2017). Response of snapdragon Antirrhinum majus L. to blended water irrigation and arbuscular mycorrhizal fungi inoculation: uptake of minerals and leaf water relations. Photosynthetica 55 (2), 201–209. doi: 10.1007/s11099-016-0650-7

CrossRef Full Text | Google Scholar

Evelin, H., Giri, B., Kapoor, R. (2012). Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22, 203–217. doi: 10.1007/s00572-011-0392-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Evelin, H., Kapoor, R., Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann. Bot. 104, 1263–1281. doi: 10.1093/aob/mcp251

PubMed Abstract | CrossRef Full Text | Google Scholar

Gamalero, E., Lingua, G., Berta, G., Glick, B. R. (2009). Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Can. J. Microbiol. 55, 501–514. 245. doi: 10.1139/W09-010

CrossRef Full Text | Google Scholar

Garcés-Ruiz, M., Calonne-Salmon, M., Plouznikoff, K., Misson, C., Navarrete-Mier, M., Cranenbrouck, S., et al. (2017). Dynamics of short-term phosphorus uptake by intact mycorrhizal and non-mycorrhizal maize plants grown in a circulatory semi-hydroponic cultivation system. Front. Plant Sci. 8, 1471. doi: 10.3389/fpls.2017.01471

PubMed Abstract | CrossRef Full Text | Google Scholar

Garg, N., Singh, S. (2017). Arbuscular mycorrhiza Rhizophagus irregularis, and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan, L. Millsp. (pigeon pea) genotypes under cadmium and zinc stress. J. Plant Growth Regul. 37, 1–18. doi: 10.1007/s00344-017-9708-4

CrossRef Full Text | Google Scholar

Garg, N., Chandel, S. (2012). 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. 31 (3), 292–308. doi: 10.1007/s00344-011-9239-3

CrossRef Full Text | Google Scholar

Gavito, M. E., Olsson, P. A., Rouhier, H., Medinapeñafiel, A., Jakobsen, I., Bago, A. (2005). Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi. New Phytol. 168, 179–188. doi: 10.1111/j.1469-8137.2005.01481.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Gholamhoseini, M., Ghalavand, A., Dolatabadian, A., Jamshidi, E., Khodaei-Joghan, A. (2013). Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric. Water Manag. 117, 106–114. doi: 10.1016/j.agwat.2012.11.007

CrossRef Full Text | Google Scholar

Gianinazzi, S., Golotte, A., Binet, M. N., Van Tuinen, D., Redecker, D., Wipf, D. (2010). Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20, 519–530. doi: 10.1007/s00572-010-0333-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Giri, B., Kapoor, R., Mukerji, K. G. (2007). 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. Microbiol. Ecol. 54, 753–760. doi: 10.1007/s00248-007-9239-9

CrossRef Full Text | Google Scholar

Goicoechea, N., Antol, M. C. (2017). Increased nutritional value in food crops. Microbiol. Biotechnol. 10, 1004–1007. doi: 10.1111/1751-7915.12764

CrossRef Full Text | Google Scholar

Goicoechea, N., Bettoni, M., Fuertes-Mendiza´bal, T., Gonzalez-Murua, C., Aranjuelo, I. (2016). Durum wheat quality traits affected by mycorrhizal inoculation, water availability and atmospheric CO2 concentration. Crop Past. Sci. 67, 147–155. doi: 10.1071/CP15212

CrossRef Full Text | Google Scholar

Gomez-Bellot, M. J., Ortuño, M. F., Nortes, P. A., Vicente-Sánchez, J., Bañón, S., Sánchez Blanco, M. J. (2015). Mycorrhizal euonymus plants and reclaimed water: biomass, water status and nutritional responses. Sci. Hort. 186, 61–69. doi: 10.1016/j.scienta.2015.02.022

CrossRef Full Text | Google Scholar

Govindarajulu, M., Pfeffer, P. E., Jin, H. R., Abubaker, J., Douds, D. D., Allen, J. W., et al. (2005). Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819–823. doi: 10.1038/nature03610

PubMed Abstract | CrossRef Full Text | Google Scholar

Grümberg, B. C., María, U. C., Shroeder, A., Vargas-Gil, S., Luna, C. M. (2015). The role of inoculum identity in drought stress mitigation by arbuscular mycorrhizal fungi in soybean. Biol. Fert. Soils 51, 1–10. doi: 10.1007/s00374-014-0942-7

CrossRef Full Text | Google Scholar

Guether, M., Neuhäuser, B., Balestrini, R. (2009). A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol. 150, 73–83. doi: 10.1104/pp.109.136390

PubMed Abstract | CrossRef Full Text | Google Scholar

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

PubMed Abstract | CrossRef Full Text | Google Scholar

Hajiboland, R., Aliasgharzadeh, N., Laiegh, S. F., Poschenrieder, C. (2010). Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato Solanum lycopersicum L. plants. Plant Soil. 331, 313–327. doi: 10.1007/s11104-009-0255-z

CrossRef Full Text | Google Scholar

Hajiboland, R., Dashtebani, F., Aliasgharzad, N. (2015). Physiological responses of halophytic C4 grass, Aeluropus littoralis to salinity and arbuscular mycorrhizal fungi colonization. Photosynthetica 53 (4), 572–584. doi: 10.1007/s11099-015-0131-4

CrossRef Full Text | Google Scholar

Hameed, A., Dilfuza, E., Abd-Allah, E. F., Hashem, A., Kumar, A., Ahmad, P. (2014). “Salinity stress and arbuscular mycorrhizal symbiosis in plants,” in Use of microbes for the alleviation of soil stresses, vol. 1. Ed. Miransari, M. (NY: Springer Science+Business Media), 139–159. doi: 10.1007/978-1-4614-9466-9_7

CrossRef Full Text | Google Scholar

Hammer, E. C., Nasr, H., Pallon, J., Olsson, P. A., Wallander, H. (2011). Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21 (2), 117–129. doi: 10.1007/s00572-010-0316-4

PubMed Abstract | CrossRef Full Text | Google Scholar

Hart, M., Ehret, D. L., Krumbein, A., Leung, C., Murch, S., Turi, C., et al. (2015). Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza 25, 359–376. doi: 10.1007/s00572-014-0617-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Hasanuzzaman, M., Gill, S. S., Fujita, M. (2013). “Physiological role of nitric oxide in plants grown under adverse environmental conditions,” in Plant acclimation to environmental stress. Eds. Tuteja, N., Gill, S. S. (NY: Springer Science+Business Media), 269–322. doi: 10.1007/978-1-4614-5001-6_11

CrossRef Full Text | Google Scholar

Hashem, A., Abd_Allah, E. F., Alqarawi, A. A., Aldubise, A., Egamberdieva, D. (2015). Arbuscular mycorrhizal fungi enhances salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. J. Plant Interact. 10 (1), 230–242. doi: 10.1080/17429145.2015.1052025

CrossRef Full Text | Google Scholar

Hashem, A., Alqarawi, A. A., Radhakrishnan, R., Al-Arjani, A. F., Aldehaish, H. A., Egamberdieva, D., et al. (2018). Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J. Biol. Sci. 25 (6), 1102–1114. doi: 10.1016/j.sjbs.2018.03.009

PubMed Abstract | CrossRef Full Text | Google Scholar

He, F., Sheng, M., Tang, M. (2017). Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought Stress. Front. Plant Sci. 8, 183. doi: 10.3389/fpls.2017.00183

PubMed Abstract | CrossRef Full Text | Google Scholar

Hijri, M. (2016). Analysis of a large dataset form field mycorrhizal inoculation trials on potato showed highly significant increase in yield. Mycorrhiza 2, 209–214. doi: 10.1007/s00572-015-0661-4

CrossRef Full Text | Google Scholar

Hodge, A., Fitter, H. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc. Natl. Acad. Sci. 107, 13754–13759. doi: 10.1073/pnas.1005874107

CrossRef Full Text | Google Scholar

Hodge, A., Storer, K. (2015). Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil. 386, 1–19. doi: 10.1007/s11104-014-2162-1

CrossRef Full Text | Google Scholar

Impa, S. M., Nadaradjan, S., Jagadish, S. V. K. (2012). “Drought stress induced reactive oxygen species and anti-oxidants in plants,” in Abiotic stress responses in plants: metabolism, productivity and sustainability. Eds. Ahmad, P., Prasad, M. N. V. (LLC: Springer Science+ Business Media), 131–147. doi: 10.1007/978-1-4614-0634-1_7

CrossRef Full Text | Google Scholar

Janouškova, M., Pavlíková, D. (2010). Cadmium immobilization in the rhizosphere of arbuscular mycorrhizal plants by the fungal extraradical mycelium. Plant Soil 332, 511–520. doi: 10.1007/s11104-010-0317-2

CrossRef Full Text | Google Scholar

Jiang, Y. N., Wang, W. X., Xie, Q. J., Liu, N., Liu, L. X., Wang, D. P., et al. (2017). Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356, 1172–1175. doi: 10.1126/science.aam9970

PubMed Abstract | CrossRef Full Text | Google Scholar

Jin, H., Pfeffer, P. E., Douds, D. D., Piotrowski, E., Lammers, P. J., Shachar-Hill, Y. (2005). The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol. 168, 687–696. doi: 10.1111/j.1469-8137.2005.01536.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Jixiang, L., Yingnan, W., Shengnan, S., Chunsheng, M., Xiufeng, Y. (2017). Effects of arbuscular mycorrhizal fungi on the growth, photosynthesis and photosynthetic pigments of Leymus chinensis seedlings under salt-alkali stress and nitrogen deposition. Sci. Total Environ. 576, 234–241. doi: 10.1016/j.scitotenv.2016.10.091

PubMed Abstract | CrossRef Full Text | Google Scholar

Jung, S. C., Martinez-Medina, A., Lopez-Raez, J. A., Pozo, M. J. (2012). Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 38, 651–664. doi: 10.1007/s10886-012-0134-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Kanwal, S., Bano, A., Malik, R. N. (2015). Effects of arbuscular mycorrhizal fungi on metals uptake, physiological and biochemical response of Medicago sativa L. with increasing Zn and Cd concentrations in soil. Am. J. Plant Sci. 6, 2906–2923. doi: 10.4236/ajps.2015.618287

CrossRef Full Text | Google Scholar

Kapoor, R., Evelin, H., Mathur, P., Giri, B. (2013). “Arbuscular mycorrhiza: approaches for abiotic stress tolerance in crop plants for sustainable agriculture,” in Plant acclimation to environmental stress. Eds. Tuteja, N., Gill, S. S. (LLC: Springer Science+Business Media), 359–401. doi: 10.1007/978-1-4614-5001-6_14

CrossRef Full Text | Google Scholar

Kayama, M., Yamanaka, T. (2014). Growth characteristics of ectomycorrhizal seedlings of Quercus glauca, Quercus salicina, and Castanopsis cuspidata planted on acidic soil. Trees 28, 569–583. doi: 10.1007/s00468-013-0973-y

CrossRef Full Text | Google Scholar

Khalloufi, M., Martínez-Andújar, C., Lachaâl, M., Karray-Bouraoui, N., Pérez-Alfocea, F., Albacete, A. (2017). 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. 214, 134–144. doi: 10.1016/j.jplph.2017.04.012

PubMed Abstract | CrossRef Full Text | Google Scholar

Kubikova, E., Moore, J. L., Ownlew, B. H., Mullen, M. D., Augé, R. M. (2001). Mycorrhizal impact on osmotic adjustment in Ocimum basilicum during a lethal drying episode. J. Plant Physiol. 158, 1227–1230. doi: 10.1078/0176-1617-00441

CrossRef Full Text | Google Scholar

Lehmann, A., Rillig, M. C. (2015). Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops—a meta-analysis. Soil Biol. Biochem. 81, 147–158. doi: 10.1016/j.soilbio.2014.11.013

CrossRef Full Text | Google Scholar

Lehmann, A., Veresoglou, S. D., Leifheit, E. F., Rillig, M. C. (2014). Arbuscular mycorrhizal influence on zinc nutrition in crop plants: a meta-analysis. Soil Biol. Biochem. 69, 123–131. doi: 10.1016/j.soilbio.2013.11.001

CrossRef Full Text | Google Scholar

Li, H., Chen, X. W., Wong, M. H. (2015). Arbuscular mycorrhizal fungi reduced the ratios of inorganic/organic arsenic in rice grains. Chemosphere 145, 224–230. doi: 10.1016/j.chemosphere.2015.10.067

PubMed Abstract | CrossRef Full Text | Google Scholar

Li, H., Luo, N., Zhang, L. J., Zhao, H. M., Li, Y. W., Cai, Q. Y., et al. (2016a). Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci. Total Environ. 571, 1183–1190. doi: 10.1016/j.scitotenv.2016.07.124

PubMed Abstract | CrossRef Full Text | Google Scholar

Li, J., Meng, B., Chai, H., Yang, X., Song, W., Li, S., et al. (2019). Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Front. Plant Sci. 10, 499. doi: 10.3389/fpls.2019.00499

PubMed Abstract | CrossRef Full Text | Google Scholar

Li, X., Zeng, R., Liao, H. (2016b). Improving crop nutrient efficiency through root architecture modifications. J. Integr. Plant Biol. 58, 193–202. doi: 10.1111/jipb.12434

PubMed Abstract | CrossRef Full Text | Google Scholar

Lin, A. J., Zhang, X. H., Wong, M. H., Ye, Z. H., Lou, L. Q., Wang, Y. S. (2007). Increase of multi-metal tolerance of three leguminous plants by arbuscular mycorrhizal fungi colonization. Environ. Geochem. Health 29, 473–481. doi: 10.1007/s10653-007-9116-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, C., Ravnskov, S., Liu, F., Rubæk, G. H., Andersen, M. N. (2018). Arbuscular mycorrhizal fungi alleviate abiotic stresses in potato plants caused by low phosphorus and deficit irrigation/partial root-zone drying. J. Agric. Sci. 156, 46–58. doi: 10.1017/S0021859618000023

CrossRef Full Text | Google Scholar

Liu, L. Z., Gong, Z. Q., Zhang, Y. L., Li, P. J. (2014). Growth, cadmium uptake and accumulation of maize Zea mays L. under the effects of arbuscular mycorrhizal fungi. Ecotoxicology 23, 1979–1986. doi: 10.1007/s10646-014-1331-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, X., Song, Q., Tang, Y., Li, W., Xu, J., Wu, J., et al. (2013). Human health risk assessment of heavy metals in soil–vegetable system: a multi-medium analysis. Sci. Total. Environ. 463–464, 530–540. doi: 10.1016/j.scitotenv.2013.06.064

PubMed Abstract | CrossRef Full Text | Google Scholar

Lu, F., Lee, C., Wang, C. (2015). The influence of arbuscular mycorrhizal fungi inoculation on yam (Dioscorea spp.) tuber weights and secondary metabolite content. Peer J. 3, 12–66. doi: 10.7717/peerj.1266

CrossRef Full Text | Google Scholar

Ludwig-Müller, J. (2010). “Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi,” in Arbuscular mycorrhizas: Physiology and function. Eds. Koltai, H., Kapulnik, Y. (Dordrecht: Springer), 169–190. doi: 10.1007/978-90-481-9489-6_8

CrossRef Full Text | Google Scholar

Luginbuehl, L. H., Menard, G. N., Kurup, S., Van Erp, H., Radhakrishnan, G. V., Breakspear, A., et al. (2017). Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356, 1175–1178. doi: 10.1126/science.aan0081

PubMed Abstract | CrossRef Full Text | Google Scholar

Mathur, S., Sharma, M. P., Jajoo, A. (2016). Improved photosynthetic efficacy of maize Zea mays plants with arbuscular mycorrhizal fungi (AMF) under high temperature stress. J. Photochem. Photobiol. B 180, 149–154. doi: 10.1016/j.jphotobiol.2018.02.002

CrossRef Full Text | Google Scholar

Maya, M. A., Matsubara, Y. (2013). Influence of arbuscular mycorrhiza on the growth and antioxidative activity in Cyclamen under heat stress. Mycorrhiza 23 (5), 381–390. doi: 10.1007/s00572-013-0477-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Mena-Violante, H. G., Ocampo-Jimenez, O., Dendooven, L., Martinez-Soto, G., Gonzalez-Castafeda, J., Davies, F. T., et al. (2006). Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho Capsicum annuum L. cv San Luis plants exposed to drought. Mycorrhiza 16, 261–267. doi: 10.1007/s00572-006-0043-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Miransari, M. (2017). “Arbuscular mycorrhizal fungi and heavy metal tolerance in plants,” in Arbuscular mycorrhizas and stress tolerance of plants. Ed. Wu, Q. S. (Singapore: Springer Nature), 174–161. doi: 10.1007/978-3-319-68867-1_4

CrossRef Full Text | Google Scholar

Mirshad, P. P., Puthur, J. T. (2016). Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass Saccharum arundinaceum, Retz. Environ. Monit. Assess. 188, 425. doi: 10.1007/s10661-016-5428-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Mitra, D., Navendra, U., Panneerselvam, U., Ansuman, S., Ganeshamurthy, A. N., Divya, J. (2019). Role of mycorrhiza and its associated bacteria on plant growth promotion and nutrient management in sustainable agriculture. Int. J. Life Sci. Appl. Sci. 1, 1–10.

Google Scholar

Moghadam, H. R. T. (2016). Application of super absorbent polymer and ascorbic acid to mitigate deleterious effects of cadmium in wheat. Pesqui. Agropecu. Trop. 6 (1), 9–18. doi: 10.1590/1983-40632016v4638946

CrossRef Full Text | Google Scholar

Moradtalab, N., Roghieh, H., Nasser, A., Tobias, E. H., Günter, N. (2019). Silicon and the association with an arbuscular-mycorrhizal fungus (Rhizophagus clarus) mitigate the adverse effects of drought stress on strawberry. Agronomy 9, 41. doi: 10.3390/agronomy9010041

CrossRef Full Text | Google Scholar

Morte, A., Lovisolo, C., Schubert, A. (2000). Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almerienseTerfezia claveryi. Mycorrhiza 10, 115–119. doi: 10.1007/s005720000066

CrossRef Full Text | Google Scholar

Navarro, J. M., Perez-Tornero, O., Morte, A. (2014). Alleviation of salt stress in citrus seedlings inoculated with arbuscular mycorrhizal fungi depends on the root stock salt tolerance. J. Plant Physiol. 171 (1), 76–85. doi: 10.1016/j.jplph.2013.06.006

CrossRef Full Text | Google Scholar

Nell, M., Wawrosch, C., Steinkellner, S., Vierheilig, H., Kopp, B., Lössl, A. (2010). Root colonization by symbiotic arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana officinalis L. Planta Med. 76, 393–398. doi: 10.1055/s-0029-1186180

PubMed Abstract | CrossRef Full Text | Google Scholar

Nouri, E., Breuillinsessoms, F., Feller, U., Reinhardt, D. (2015). Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrid. PLoS One 9, e90–841. doi: 10.1371/journal.pone.0127472

CrossRef Full Text | Google Scholar

Orfanoudakis, M., Wheeler, C. T., Hooker, J. E. (2010). Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 20, 117–126. doi: 10.1007/s00572-009-0271-0

PubMed Abstract | CrossRef Full Text | Google Scholar

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

CrossRef Full Text | Google Scholar

Ouziad, F., Hildebrandt, U., Schmelzer, E., Bothe, H. (2005). Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J. Plant Physiol. 162, 634–649. doi: 10.1016/j.jplph.2004.09.014

PubMed Abstract | CrossRef Full Text | Google Scholar

Pal, A., Pandey, S. (2016). Role of arbuscular mycorrhizal fungi on plant growth and reclamation of barren soil with wheat (Triticum aestivum L.) crop. Int. J. Soil Sci. 12, 25–31. doi: 10.3923/ijss.2017.25.31

CrossRef Full Text | Google Scholar

Paterson, E., Sim, A., Davidson, J., Daniell, T. J. (2016). Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralization. Plant Soil. 408, 243–C254. doi: 10.1007/s11104-016-2928-8

CrossRef Full Text | Google Scholar

Pavithra, D., Yapa, N. (2018). Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Ground Water Sust. Dev. 7, 490–494. doi: 10.1016/j.gsd.2018.03.005

CrossRef Full Text | Google Scholar

Pedranzani, H., RodrãGuez-Rivera, M., GutiaRrez, M., Porcel, R., Hause, B., Ruiz-Lozano, J. M. (2016). Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 26, 141–152. doi: 10.1007/s00572-015-0653-4

PubMed Abstract | CrossRef Full Text | Google Scholar

Pellegrino, E., Bedini, S. (2014). Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol. Biochem. 68, 429–439. doi: 10.1016/j.soilbio.2013.09.030

CrossRef Full Text | Google Scholar

Plassard, C., Dell, B. (2010). Phosphorus nutrition of mycorrhizal trees. Tree Physiol. 30, 1129–1139. doi: 10.1093/treephys/tpq063

PubMed Abstract | CrossRef Full Text | Google Scholar

Porcel, R., Redondogómez, S., Mateosnaranjo, E., Aroca, R., Garcia, R., Ruizlozano, J. M. (2015). Arbuscular mycorrhizal symbiosis ameliorates the optimum quantum yield of photosystem II and reduces non-photochemical quenching in rice plants subjected to salt stress. J. Plant Physiol. 185, 75–83. doi: 10.1016/j.jplph.2015.07.006

PubMed Abstract | CrossRef Full Text | Google Scholar

Prasad, R., Bhola, D., Akdi, K., Cruz, C., Sairam, K. V. S. S., Tuteja, N., et al. (2017). Introduction to mycorrhiza: historical development,” in Mycorrhiza. Eds. Varma, A., Prasad, R., Tuteja, N. (Cham: Springer), 1–7. doi: 10.1007/978-3-319-53064-2_1

CrossRef Full Text | Google Scholar

Pringle, A., Bever, J. D., Gardes, M., Parrent, J. L., Rillig, M. C., Klironomos, J. N. (2009). Mycorrhizal symbioses and plant invasions. Ann. Rev. Ecol. Evol. Syst. 40, 699–715. doi: 10.1146/annurev.ecolsys.39.110707.173454

CrossRef Full Text | Google Scholar

Punamiya, P., Datta, R., Sarkar, D., Barber, S., Patel, M., Da, P. (2010). Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass Chrysopogon zizanioides L. J. Hazard. Mater. 177, 465–474. doi: 10.1016/j.jhazmat.2009.12.056

PubMed Abstract | CrossRef Full Text | Google Scholar

Rani, B. (2016) Effect of arbuscular mycorrhiza fungi on biochemical parameters in wheat Triticum aestivum L. under drought conditions. Doctoral dissertation, CCSHAU, Hisar.

Google Scholar

Redecker, D., Schüssler, A., Stockinger, H., Stürmer, S. L., Morton, J. B., Walker, C. (2013). An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23 (7), 515–531. doi: 10.1007/s00572-013-0486-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Rodriguez, R. J., Henson, J., Van Volkenburgh, E., Hoy, M., Wright, L., Beckwith, F., et al. (2008). Stress tolerance in plants via habitat-adapted symbiosis. Int. Soc. Microb. Ecol. 2, 404–416. doi: 10.1038/ismej.2007.106

CrossRef Full Text | Google Scholar

Rouphael, Y., Franken, P., Schneider, C., Schwarz, D., Giovannetti, M., Agnolucci, M. (2015). Arbuscular mycorrhizal fungi act as bio-stimulants in horticultural crops. Sci. Hort. 196, 91–108. doi: 10.1016/j.scienta.2015.09.002

CrossRef Full Text | Google Scholar

Ruiz-Lozano, J. M. (2003). Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. Mycorrhiza 13, 309–317. doi: 10.1007/s00572-003-0237-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Ruiz-Lozano, J. M., Aroca, R., Zamarreño, Á.M., Molina, S., Andreo-Jiménez, B., Porcel, R., et al. (2015). Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ. 39 (2), 441–452. doi: 10.1111/pce.12631

PubMed Abstract | CrossRef Full Text | Google Scholar

Ruiz-Sánchez, M., Aroca, R., Muñoz, Y., Polón, R., Ruiz-Lozano, J. M. (2010). The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J. Plant Physiol. 167, 862–869. doi: 10.1016/j.jplph.2010.01.018

PubMed Abstract | CrossRef Full Text | Google Scholar

Sabia, E., Claps, S., Morone, G., Bruno, A., Sepe, L., Aleandri, R. (2015). Field inoculation of arbuscular mycorrhiza on maize (Zea mays L.) under low inputs: preliminary study on quantitative and qualitative aspects. Italian J. Agron. 10, 30–33. doi: 10.4081/ija.2015.607

CrossRef Full Text | Google Scholar

Sadhana, B. (2014). Arbuscular mycorrhizal fungi (AMF) as a biofertilizers—a review. Int. J. Curr. Microbiol. App. Sci. 3 (4), 384–400.

Google Scholar

Salam, E. A., Alatar, A., El-Sheikh, M. A. (2017). Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi J. Biol. Sci. 25 (8), 1772–1780. doi: 10.1016/j.sjbs.2017.10.015

PubMed Abstract | CrossRef Full Text | Google Scholar

Santander, C., Sanhueza, M., Olave, J., Borie, F., Valentine, C., Cornejo, P. (2019). Arbuscular mycorrhizal colonization promotes the tolerance to salt stress in lettuce plants through an efficient modification of ionic balance. J. Soil Sci. Plant Nutr. 19 (2), 321–331. doi: 10.1007/s42729-019-00032-z

CrossRef Full Text | Google Scholar

Sara, O., Ennajeh, M., Zrig, A., Gianinazzi, S., Khemira, H. (2018). Estimating the contribution of arbuscular mycorrhizal fungi to drought tolerance of potted olive trees (Olea europaea). Acta Physiol. Plant. 40, 1–81. doi: 10.1007/s11738-018-2656-1

CrossRef Full Text | Google Scholar

Sbrana, C., Avio, L., Giovannetti, M. (2014). Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35, 1535–1546. doi: 10.1002/elps.201300568

PubMed Abstract | CrossRef Full Text | Google Scholar

Selosse, M. A., Strullu-Derrien, C., Martin, F. M., Kamoun, S., Kenrick, P. (2015). Plants, fungi and oomycetes: a 400-million years affair that shapes the biosphere. New Phytol. 206, 501–506. doi: 10.1111/nph.13371

PubMed Abstract | CrossRef Full Text | Google Scholar

Sharma, S., Prasad, R., Varma, A., Sharma, A. K. (2017). Glycoprotein associated with Funneliformis coronatum, Gigaspora margarita and Acaulospora scrobiculata suppress the plant pathogens in vitro. Asian J. Plant Pathol. 11 (4), 192–202. doi: 10.3923/ajppaj.2017.199.202

CrossRef Full Text | Google Scholar

Shen, H., Christie, P., Li, X. (2006). Uptake of zinc, cadmium and phosphorus by arbuscular mycorrhizal maize (Zea mays, L.) from a low available phosphorus calcareous soil spiked with zinc and cadmium. Environ. Geochem. Health 28, 111. doi: 10.1007/s10653-005-9020-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Sheng, M., Tang, M., Zhang, F., Huang, Y. (2011). Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21, 423–430. doi: 10.1007/s00572-010-0353-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Smith, S. E., Read, D. J. (1997). Mycorrhizal symbiosis. San Diego: Academic Press, 607.

Google Scholar

Smith, S., Read, D. (2008). Mycorrhiza symbiosis, 3rd Ed. San Diego, CA: Academic Press.

Google Scholar

Smith, S. E., Jakobsen, I., Grnlund, M., Smith, F. A. (2011). Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156, 1050–1057. doi: 10.1104/pp.111.174581

PubMed Abstract | CrossRef Full Text | Google Scholar

Smith, S. E., Smith, F. A., Jakobsen, I. (2003). Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133, 16–20. doi: 10.1104/pp.103.024380

PubMed Abstract | CrossRef Full Text | Google Scholar

Souza, L. A., Andrade, S. A. L., Souza, S. C. R., Schiavinato, M. A. (2012). Evaluation of mycorrhizal influence on the development and phytoremediation potential of Canavalia gladiata in Pb contaminated soils. Int. J. Phytorem. 15, 465–476. doi: 10.1080/15226514.2012.716099

CrossRef Full Text | Google Scholar

Spatafora, J. W., Chang, Y., Benny, G. L., Lazarus, K., Smith, M. E., Berbee, M. L., et al. (2016). A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108, 1028–1046. doi: 10.3852/16-042

PubMed Abstract | CrossRef Full Text | Google Scholar

Sun, Z., Song, J., Xin, X., Xie, X., Zhao, B. (2018). Arbuscular mycorrhizal fungal proteins 14-3-3- are involved in arbuscule formation and responses to abiotic stresses during AM symbiosis. Front. Microbiol. 5, 9–19. doi: 10.3389/fmicb.2018.00091

CrossRef Full Text | Google Scholar

Syamsiyah, J., Herawati, A., Mujiyo (2018). The potential of arbuscular mycorrhizal fungi application on aggregrate stability in alfisol soil. IOP Conf. Series: Earth Environ. Sci. 142, 012045. doi: 10.1088/1755-1315/142/1/012045

CrossRef Full Text | Google Scholar

Takács, T., Vörös, I. (2003). Effect of metal non-adapted arbuscular mycorrhizal fungi on Cd, Ni and Zn uptake by ryegrass. Acta Agron. Hung. 51, 347–354.

Google Scholar

Talaat, N. B., Shawky, B. T. (2014). Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ. Exp. Bot. 98, 20–31. doi: 10.1016/j.envexpbot.2013.10.005

CrossRef Full Text | Google Scholar

Tanaka, Y., Yano, Y. (2005). Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ. 28, 1247–1254. doi: 10.1111/j.1365-3040.2005.01360.x

CrossRef Full Text | Google Scholar

Thirkell, T. J., Charters, M. D., Elliott, A. J., Sait, S. M., Field, K. J. (2017). Are mycorrhizal fungi our sustainable saviours considerations for achieving food security. J. Ecol. 105, 921–929. doi: 10.1111/1365-2745.12788

CrossRef Full Text | Google Scholar

Tsoata, E., Njock, S. R., Youmbi, E., Nwaga, D. (2015). Early effects of water stress on some biochemical and mineral parameters of mycorrhizal Vigna subterranea (L.) Verdc. (Fabaceae) cultivated in Cameroon. Int. J. Agron. Agric. Res. 7, 21–35.

Google Scholar

Turrini, A., Bedini, A., Loor, M. B., Santini, G., Sbrana, C., Giovannetti, M., et al. (2018). Local diversity of native arbuscular mycorrhizal symbionts differentially affects growth and nutrition of three crop plant species. Biol. Fertil. Soils 54, 203–217. doi: 10.1007/s00374-017-1254-5

CrossRef Full Text | Google Scholar

Van der Heijden, M. G., Martin, F. M., Selosse, M. A., Sanders, I. R. (2015). Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423. doi: 10.1111/nph.13288

PubMed Abstract | CrossRef Full Text | Google Scholar

Wagg, C., Barendregt, C., Jansa, J., Heijden, M. G. A. (2015). Complementarity in both plant and mycorrhizal fungal communities are not necessarily increased by diversity in the other. J. Ecol. 103, 1233–1244. doi: 10.1111/1365-2745.12452

CrossRef Full Text | Google Scholar

Wahid, A., Gelani, S., Ashraf, M., Foolad, M. R. (2007). Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199–223. doi: 10.1016/j.envexpbot.2007.05.011

CrossRef Full Text | Google Scholar

Wang, Y., Jing, H., Gao, Y. (2012). Arbuscular mycorrhizal colonization alters subcellular distribution and chemical forms of cadmium in Medicago sativa L. and resists cadmium toxicity. PLoS One 7, 3161–3164. doi: 10.1371/journal.pone.0048669

CrossRef Full Text | Google Scholar

Wang, Y., Wang, M., Li, Y., Wu, A., Huang, J. (2018). Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLoS One 13 (4), e0196408. doi: 10.1371/journal.pone.0196408

PubMed Abstract | CrossRef Full Text | Google Scholar

Wu, Z., McGrouther, K., Huang, J., Wu, P., Wu, W., Wang, H. (2014). Decomposition and the contribution of glomalin-related soil protein (GRSP) in heavy metal sequestration: field experiment. Soil Biol. Biochem. 68, 283–290. doi: 10.1029/2007JD008789

CrossRef Full Text | Google Scholar

Yang, S., Li, F., Malhi, S. S., Wang, P., Dongrang, S., Wang, J. (2004). Long term fertilization effects on crop yield and nitrate nitrogen accumulation in soil in Northwestern China. Agron. J. 96, 1039–1049. doi: 10.2134/agronj2004.1039

CrossRef Full Text | Google Scholar

Yang, Y., Tang, M., Sulpice, R., Chen, H., Tian, S., Ban, Y. (2014). Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia, L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. J. Plant Growth Regul. 33, 612–625. doi: 10.1007/s00344-013-9410-0

CrossRef Full Text | Google Scholar

Yin, N., Zhang, Z., Wang, L., Qian, K. (2016). Variations in organic carbon, aggregation, and enzyme activities of gangue-fly ash-reconstructed soils with sludge and arbuscular mycorrhizal fungi during 6-year reclamation. Envi. Sci. Pollut. Res. 23 (17), 17840–17849. doi: 10.1007/s11356-016-6941-5

CrossRef Full Text | Google Scholar

Yooyongwech, S., Phaukinsang, N., Cha-Um, S., Supaibulwatana, K. (2013). Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regul. 69, 285–293. doi: 10.1007/s10725-012-9771-6

CrossRef Full Text | Google Scholar

Yooyongwech, S., Samphumphuang, T., Tisarum, R., Theerawitaya, C., Chaum, S. (2016). Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hort. 198, 107–117. doi: 10.1016/j.scienta.2015.11.002

CrossRef Full Text | Google Scholar

Yost, R. S., Fox, R. L. (1982). Influence of mycorrhizae on the mineral contents of cowpea and soybean grown in an oxisol. Agron. J. 74 (3), 475–481. doi: 10.2134/agronj1982.00021962007400030018x

CrossRef Full Text | Google Scholar

Yousaf, B., Liu, G., Wang, R., Imtiaz, M., Zia-ur-Rehman, M., Munir, M. A. M., et al. (2016). Bioavailability evaluation, uptake of heavy metals and potential health risks via dietary exposure in urban-industrial areas. Environ. Sci. Pollut. Res. 23, 22443–22453. doi: 10.1007/s11356-016-7449-8

CrossRef Full Text | Google Scholar

Zaefarian, F., Rezvani, M., Ardakani, M. R., Rejali, F., Miransari, M. (2013). Impact of mycorrhizae formation on the phosphorus and heavy-metal uptake of Alfalfa. Comm. Soil Sci. Plant Anal. 44, 1340–1352. doi: 10.1080/00103624.2012.756505

CrossRef Full Text | Google Scholar

Zeng, L., JianFu, L., JianFu, L., MingYuan, W. (2014). Effects of arbuscular mycorrhizal (AM) fungi on citrus quality under nature conditions. Southwest China J. Agric. Sci. 27, 2101–2105. doi: 10.16213/j.cnki.scjas.2014.05.067

CrossRef Full Text | Google Scholar

Zhang, F., Jia-Dong, H. E., Qiu-Dan, N. I., Qiang-Sheng, W. U., Zou, Y. N. (2018a). Enhancement of drought tolerance in trifoliate orange by mycorrhiza: changes in root sucrose and proline metabolisms. Not. Bot. Horti. Agrobot. Cluj-Napoca 46, 270. doi: 10.15835/nbha46110983

CrossRef Full Text | Google Scholar

Zhang, T., Hub, Y., Zhang, K., Tian, C., Gu, J. (2018b). Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind. Crop. Prod. 117, 13–19. doi: 10.1016/j.indcrop.2018.02.087

CrossRef Full Text | Google Scholar

Zhang, X., Li, W., Fang, M., Jixian, Y., Meng, S. (2016). 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. 97, 2919–2925. doi: 10.1002/jsfa.8129

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhao, R., Guo, W., Bi, N., Guo, J., Wang, L., Zhao, J., et al. (2015). Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays, L.) grown in two types of coal mine spoils under drought stress. Appl. Soil Ecol. 88, 41–49. doi: 10.1016/j.apsoil.2014.11.016

CrossRef Full Text | Google Scholar

Zhu, X., Song, F., Liu, S., Liu, T., Zhou, X. (2012). Arbuscular mycorrhizae improve photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ. 58, 186–191. doi: 10.4161/psb.11498

CrossRef Full Text | Google Scholar

Zhu, X. C., Song, F. B., Xu, H. W. (2010a). Arbuscular mycorrhizae improve low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil. 331, 129–137. doi: 10.1007/s11104-009-0239-z

CrossRef Full Text | Google Scholar

Zhu, X. C., Song, F. B., Liu, S. Q., Liu, F. L. (2016). Arbuscular mycorrhiza improve growth, nitrogen uptake, and nitrogen use efficiency in wheat grown under elevated CO2. Mycorrhiza 26, 133–140. doi: 10.1007/s00572-015-0654-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhu, X. C., Song, F. B., Xu, H. W. (2010b). Effects of arbuscular mycorrhizal fungi on photosynthetic characteristics of maize under low temperature stress. Acta Ecol. Sin. 21, 470–475. doi: 10.1556/AAgr.51.2003.3.13

CrossRef Full Text | Google Scholar

Zhu, X. C., Song, F. B., Liu, S. Q., Liu, T. D., Zhou, X. (2012). Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ. 58, 186–191. doi: 10.1007/s11032-011-9671-x

CrossRef Full Text | Google Scholar

Zou, Y. N., Srivastava, A. K., Wu, Q. S. (2016). Glomalin: a potential soil conditioner for perennial fruits. Int. J. Agric. Biol. 18, 293–297. doi: 10.17957/IJAB/15.0085

CrossRef Full Text | Google Scholar

Keywords: arbuscular mycorrhizal fungi, plant growth, abiotic factors, stress tolerance, mineral nutrition

Citation: Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N and Zhang L (2019) Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance. Front. Plant Sci. 10:1068. doi: 10.3389/fpls.2019.01068

Received: 14 May 2019; Accepted: 07 August 2019;
Published: 19 September 2019.

Edited by:

Ricardo Aroca, Experimental Station of Zaidín (EEZ), Spain

Reviewed by:

Xiancan Zhu, Northeast Institute of Geography and Agroecology (CAS), China
Nieves Goicoechea, University of Navarra, Spain

Copyright © 2019 Begum, Qin, Ahanger, Raza, Khan, Ashraf, Ahmed and Zhang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Lixin Zhang, zhanglixin@nwsuaf.edu.cn