The Roles of Arbuscular Mycorrhizal Fungi in Influencing Plant Nutrients, Photosynthesis, and Metabolites of Cereal Crops—A Review

Abstract

Arbuscular mycorrhizal (AM) fungi are one of the important microbiota involved in a relationship with plant roots in which the plants and fungi both share and exchange nutrients and shelter. Cereal crops are the most essential sources of carbohydrates, dietary protein, and vitamin B for humans, and they supply the most fundamental diets. AM fungi are introduced as the optimal approach for real agricultural systems for increasing growth and productivity. According to a study from the previous decade, AM fungi were shown to promote crop growth and production, particularly in cereal crops. The AM fungi symbiosis provides a pleasant environment for microorganisms in the root and soil system, which promotes plant nutrition and water availability. AM fungi increase nutrient uptake and assimilation and also increase photosynthetic activity, which is directly associated with plant growth. Furthermore, AM fungi increase the primary and secondary metabolites, as well as soluble proteins and carbohydrates, in cereals crops. AM fungi have been shown to improve plant biomass, yield, and productivity in cereal crops. Additionally, the use of AM fungi enhances plants’ stress tolerance against various environmental stresses. In this review, we integrate the recent findings regarding the effects of AM fungi application on soil, root systems, nutrient availability and uptake, photosynthesis, metabolites, plant growth, and productivity. Furthermore, a large number of studies have been reviewed, and several limitations and research gaps have been identified that must be addressed in future studies.

1. Introduction

Arbuscular mycorrhizal (AM) fungi are one of the most significant microbiota, which are involved in a symbiotic relationship with the roots of plants [1]. Such symbiotic relationships have been reported in several cereal crops, including wheat (Triticum aestivum maize (Zea mays) and rice (Oryza sativa), and show very positive effects on the growth, yield, and productivity of the host plants [2,3,4,5]. However, the effect of AM fungi on plant growth is also dependent on the plant and AM fungi species, including the soil type and plant growth stage. To date, more than 255 AM fungi species have been identified, including Glomus etunicatum, Funneliformis mosseae, and Rhizophagus irregularis, and they are being used as a commercial AM inoculum for main crops in advanced agricultural systems [6,7,8,9]. Many of these are utilized for a variety of crops, including wheat, maize, and rice, and have either positive, neutral, or even negative effects during pot and field experiments. Nitrate (NO₃⁻) and ammonium (NH₄⁺) are used more often in order to produce foods with higher yields, and they alter the structure of the soil and the plant community while also disturbing the function of microorganisms [1,10]. AM fungi may provide some plants with a better environment and improve nutrient uptake even in soil with a low nutrient content [6]. Thus, AM fungi might be used for various plants, particularly cereals, to promote nutrient intake, enhance physiological characteristics, and increase plant growth and production. The present study evaluated the effects of AM fungi on cereal crop growth and yield production, and it also provides the most recent developments regarding the functions of AM fungi in enhancing plant nutrient uptake. Additionally, the impact of AM fungi on physiological functions, including photosynthesis, that are associated to plant growth, development, yield, and quality were examined. Furthermore, various fundamental mechanisms and processes involved in plant growth and the effect of AM fungi on primary and secondary metabolites were also reviewed.

1.1. The Effects of AM on Nutrient Uptake

Because of its enormous impacts on plant systems, the use of AM fungi has emerged as an intriguing strategy for environmentally responsible agriculture [10]. AM fungi are capable for maintaining about 90% of the plant’s P, 60% of its N, and 20% of its carbon [11]. AM fungi increase the concentrations of N, P, calcium (Ca), and other nutrients such as sulfur (S), K, iron (Fe), copper (Cu), manganese (Mn), and zinc (Zn) in various plants as reported by Khan et al. [1], Mei et al. [12], Mustafa et al. [13], Cao et al. [14], and Miransari, [15]. According to Frew et al. [16] and Smith and Smith [17], AM fungi may behave as parasites, extracting carbon while providing very little or no P to the host plant. Additionally, AM fungi may stimulate physiological and biochemical mechanisms in cereal plants at various stages, facilitating early plant growth and increasing stress tolerance as shown in (Table 1).

1.2. The Effects of AM Fungi on the Chlorophylls, Carotenoids, and Photosynthesis Rate

A higher photosynthetic rate could lead to higher metabolism in host plants, resulting in higher growth performance [18]. AM fungi were also reported as failing to enhance host nutrient uptake and failing to increase the rate of photosynthesis under low light conditions [19]. On the other hand, AM fungi facilitate enzymatic activity and increase the chlorophyll content and photosynthetic rate in cereal plants [20,21]. Additionally, under AM fungi inoculation, several enzymes including Phosphoenolpyruvate carboxylase (PEPC) and rubisco could be enhanced, resulting in a higher photosynthetic rate [22,23,24].

1.3. The Effects of AM Fungi on the Primary and Secondary Metabolites

Primary and secondary metabolites are important for plant growth and development. The primary metabolites are used in the fundamental processes of plants, while in regard to the secondary metabolites, many of their chemicals can be used against pathogens for plant protection. Numerous AM fungi, including G. etunicatum, R. irregularis, and Funneliformis mosseae, have been shown to increase primary and secondary metabolites, basic plant functions, and plant growth, as well as tolerance to biotic stress (bacteria and pathogens) and abiotic stress (drought, salt, and heavy metals) [25,26,27]. Moreover, higher metabolomics activities in cereal crops lead to higher growth, yield, and productivity of these crops [28,29]. However, the influence of AM fungi is still quite dynamic and depends on a wide range of factors, including the crop type, plant community, soil structure, and fertilizer management of the crops.

Table 1. The role of AM fungal spores in plant growth and development at different stages of cereal plants.

Plant	AMF Spore	Plant Stage	Function	Changes after AM Colonization	Environmental Conditions	References
Wheat	R. irregularis	Vegetative stage	Increased stress tolerance	Enhanced macro and micro nutrient concentration	Low- or high-temperature stress	[30]
Wheat	F. mosseae	Vegetative stage	Increased chlorophyll pigments	Increased the concentrations of P, N, K, and Mg	Saline soil condition	[31]
Wheat	F. geosporum	Seeding and vegetative stages	Maintenance of PSI and PSII	Upregulation of water and nutrient uptake	Salt, drought, and heavy metal conditions	[32]
Wheat	G. claroideum	Tillering stage	Increased photosynthesis	Enhanced total dry weight and leaf chlorophyll concentration	Drought stress condition	[33]
Wheat	R. intraradices, F. mosseae, F. geosporum	Tillering stage	Increased the activity of PSI and PSII	Increased relative water content (RWC)	Drought stress condition	[34]
Maize	F. mosseae	Pre-flowering stage	Increased stress tolerance	Increased N and P concentration	Under water deficit conditions	[35]
Maize	G. mosseae, G. clarum	Seedling stage	Improved plant growth	Increased P uptake by AM pathway	Under P-deficient conditions	[36]
Maize	G. etunicatum	Tillering stage	Increased plant biomass	Increased leaf water potential	Under P-deficient conditions	[36]
Maize	G. intraradices, G. intraradices	Vegetative stage	Increased water uptake and leaf water potential	Increased drought stress tolerance	Under sandy loam soil	[37]
Maize	R. irregularis	Seedling, tillering, and fruiting stages	Increased root length	Increased Cu tolerance	Under heavy metal condition	[38]
Rice	G. mosseae	Heading stage	Increased root and shoot growth	Increased N accumulation and protein content	Under greenhouse conditions	[39]
Rice	C. etunicatum	Heading and flowering stage	Improving nutrition status and plant growth	Increased net photosynthetic rate, stomatal conductance, and transpiration rate	Under salt stress conditions	[40]
Sorghum	R. irregularis	Fruiting stage	Improved their transpiration efficiency and drought tolerance	Increased uptake 15N	Under drought conditions	[41]
Sorghum	Glomus species	Flowering and fruiting stages	Increased root and shoot growth	Increased total dry matter yield	Under striga hermonthica conditions	[42]
Barley	G. mosseae	Flowering stage	Increased resistance against heavy metal conditions	Decreased Cd and Co uptake	Under heavy metal conditions	[43]
Barley	R. irregularis	Fruiting stage	Improved yield production	Improved Zn concentrations in grain	Under overexpression of HvZIP13 gene	[44]
Oat	Mix-AMF	Tillering and flowering stages	Increased nutrients and plant growth	Improved the P content in plants	Under fumigated soil	[45]
Oat	Mix-AMF with organic fertilizer	Early and late flowering stages	Increased photosynthesis and plant growth	Improved total N and P concentrations and dry weight of plant	Under organic farming conditions	[46]
Buckwheat	Mix-AMF	Fruiting stage	Increased growth and productivity	Improved the nutritional and functional quality	Under greenhouse conditions	[47]
Buckwheat	A. laevis	Fruiting stage	Increased plant growth	Increased plant height, leaf area, number of branches	Under organic conditions	[48]
Buckwheat	Glomus species	Harvesting stage	Plant biomass	Increased inorganic phosphorus uptake	Under organic garden conditions	[49]
Quinoa	G. mosseae	Fruiting stage	Plant growth	Decreased uptake of 137Cs	Under loamy sand conditions	[50]
Quinoa	G. mosseae	Fruiting stage	Shoot and root growth	Improved nutrient uptake	Under different nitrogen levels	[51]
Millet	G. mosseae	Harvesting stage	Plant height and dry weight of root	Improved P and N uptake	Under experimental pot conditions	[52]
Millet	R. fasciculatus	Fruiting stage and harvesting stage	Plant growth and grain yield	Increased the lengths and weights of shoots and roots	Under Benomyl conditions	[53]

Table 1. The role of AM fungal spores in plant growth and development at different stages of cereal plants.

Plant	AMF Spore	Plant Stage	Function	Changes after AM Colonization	Environmental Conditions	References
Wheat	R. irregularis	Vegetative stage	Increased stress tolerance	Enhanced macro and micro nutrient concentration	Low- or high-temperature stress	[30]
Wheat	F. mosseae	Vegetative stage	Increased chlorophyll pigments	Increased the concentrations of P, N, K, and Mg	Saline soil condition	[31]
Wheat	F. geosporum	Seeding and vegetative stages	Maintenance of PSI and PSII	Upregulation of water and nutrient uptake	Salt, drought, and heavy metal conditions	[32]
Wheat	G. claroideum	Tillering stage	Increased photosynthesis	Enhanced total dry weight and leaf chlorophyll concentration	Drought stress condition	[33]
Wheat	R. intraradices, F. mosseae, F. geosporum	Tillering stage	Increased the activity of PSI and PSII	Increased relative water content (RWC)	Drought stress condition	[34]
Maize	F. mosseae	Pre-flowering stage	Increased stress tolerance	Increased N and P concentration	Under water deficit conditions	[35]
Maize	G. mosseae, G. clarum	Seedling stage	Improved plant growth	Increased P uptake by AM pathway	Under P-deficient conditions	[36]
Maize	G. etunicatum	Tillering stage	Increased plant biomass	Increased leaf water potential	Under P-deficient conditions	[36]
Maize	G. intraradices, G. intraradices	Vegetative stage	Increased water uptake and leaf water potential	Increased drought stress tolerance	Under sandy loam soil	[37]
Maize	R. irregularis	Seedling, tillering, and fruiting stages	Increased root length	Increased Cu tolerance	Under heavy metal condition	[38]
Rice	G. mosseae	Heading stage	Increased root and shoot growth	Increased N accumulation and protein content	Under greenhouse conditions	[39]
Rice	C. etunicatum	Heading and flowering stage	Improving nutrition status and plant growth	Increased net photosynthetic rate, stomatal conductance, and transpiration rate	Under salt stress conditions	[40]
Sorghum	R. irregularis	Fruiting stage	Improved their transpiration efficiency and drought tolerance	Increased uptake 15N	Under drought conditions	[41]
Sorghum	Glomus species	Flowering and fruiting stages	Increased root and shoot growth	Increased total dry matter yield	Under striga hermonthica conditions	[42]
Barley	G. mosseae	Flowering stage	Increased resistance against heavy metal conditions	Decreased Cd and Co uptake	Under heavy metal conditions	[43]
Barley	R. irregularis	Fruiting stage	Improved yield production	Improved Zn concentrations in grain	Under overexpression of HvZIP13 gene	[44]
Oat	Mix-AMF	Tillering and flowering stages	Increased nutrients and plant growth	Improved the P content in plants	Under fumigated soil	[45]
Oat	Mix-AMF with organic fertilizer	Early and late flowering stages	Increased photosynthesis and plant growth	Improved total N and P concentrations and dry weight of plant	Under organic farming conditions	[46]
Buckwheat	Mix-AMF	Fruiting stage	Increased growth and productivity	Improved the nutritional and functional quality	Under greenhouse conditions	[47]
Buckwheat	A. laevis	Fruiting stage	Increased plant growth	Increased plant height, leaf area, number of branches	Under organic conditions	[48]
Buckwheat	Glomus species	Harvesting stage	Plant biomass	Increased inorganic phosphorus uptake	Under organic garden conditions	[49]
Quinoa	G. mosseae	Fruiting stage	Plant growth	Decreased uptake of 137Cs	Under loamy sand conditions	[50]
Quinoa	G. mosseae	Fruiting stage	Shoot and root growth	Improved nutrient uptake	Under different nitrogen levels	[51]
Millet	G. mosseae	Harvesting stage	Plant height and dry weight of root	Improved P and N uptake	Under experimental pot conditions	[52]
Millet	R. fasciculatus	Fruiting stage and harvesting stage	Plant growth and grain yield	Increased the lengths and weights of shoots and roots	Under Benomyl conditions	[53]

2. AM Fungi and Mineral Nutrition

AM fungi provide nutrient access to the host plants that are otherwise unavailable, resulting higher nutrient uptakes [54]. AM fungi provide higher nutrient availability and promote plant nutrient uptake to the host plant via the mycorrhizal uptake pathway, as shown in (Figure 1). The wheat plants inoculated with F. mosseae and R. intraradices showed a 2.5 times higher Zn uptake compared with non-inoculated plants (Table 2). Similarly, as reported by Pellegrino et al. [55] and Schweiger and Jakobsen [56], AM fungi considerably contributed to overall P uptake and soil fertility through the mycorrhizal uptake pathway in field-grown winter wheat. It is commonly acknowledged that the mycorrhizal uptake pathway is the one that allows plants to acquire phosphorus more quickly and effectively than the root uptake pathway. The N and P uptake in organic field wheat was increased by about 2.3 times by Glomus species as compared to the traditional system in the Canadian prairie [57]. However, it is also hypothesized that AM fungi could produce non-beneficial effects on wheat in the field depending on the P status in the soil, including the AM fungi status in the soil community [58]. Maize plants inoculated with R. irregularis had longer roots and higher P absorption under alkaline conditions; this is because AM fungi facilitate N and P uptake [38]. The AM fungus Glomus intraradices boosted the Zn and P content in the shoots of maize after 45 and 75 days after inoculation, respectively [59]. During the grain filling stage, the contents of N and P in maize roots and shoots in inoculated plants were considerably higher, which suggests that AM colonization mediates more translocation of N and P during the grain filling stage of host plants [60]. Inoculation of AM fungus with bacteria, i.e., G. mosseae and Rhizobium, increased maize N uptake by AM colonization and nodulation [61]. Thus, it is suggested that both AM fungi and bacteria can play a positive role in maize’s nutrient uptake and availability by mycorrhization and nodulation.

In rice, the mixed AM fungi increased N uptake in the roots and P concentration in the shoots, and resulted in higher growth and yield [62]. He and Dijkstra [63] reported that AM fungi significantly increased N and P concentrations in the roots of rice. In another study, the total ¹⁵N uptake of rice was higher in inoculated rice as compared to the control [64]. The AM fungus G. intraradices enhanced the P concentration of rice and increased grain yield and straw biomass by reducing the negative effect of heavy metals under arsenic (As) conditions [65]. Further, it is explained that this is because of the ‘dilution effect’ lowering the As concentrations in the grains due to the higher growth in AM-inoculated plants. In sorghum (sorghum bicolor), the AM fungus Glomus versiforme increased N, P, and K uptake, but there was no effect on carbon: nitrogen: phosphorus (C: N: P) stoichiometry [66]. In comparison to non-inoculated plants, sorghum plants inoculated with G. mosseae showed a higher ⁵⁹Fe content in shoots under low-nutritional soil conditions; this is due to C₄ crops being considered more responsive toward AM colonization than C₃ plants [67]. G. etunicatum considerably enhanced P, N, sulfur (S), and molybdenum (Mo) concentrations in the both roots and shoots of sorghum [68]. AM fungi R. irregularis inoculation reduces the growth of sorghum at an early stage, but increases P, Zn, and Fe concentrations in grains and the harvest indices in the mature stage [69]. It may be that AM fungi are more efficient and beneficial at the mature stage as compared to the seedling stage. In oat (Avena sativa) plants, the four mixed AM fungi, i.e., F. mosseae, Gigaspora spp., Claroideoglomus spp., and R. irregularis, were applied as seed coats under fungicides and increased Ca, B, and Cu contents in the roots, but had no significant effect on the P concentration of the host plant [70]. Mixed AM fungi increased P concentrations in shoots of oat plants and increased nutritional levels in sand beach soil [71]. Similarly, the inoculation of nine mixed-AM species increased the growth of oat plants by enhancing N and P uptake in a Mediterranean environment, suggesting that inoculation of AM fungi is a good option for oat crops in a Mediterranean climate to improve agro-ecosystem sustainability [72].

In barley (Hordeum vulgare), inoculation with the AM fungus G. mosseae decreased cadmium (Cd) and cobalt (Co) uptake under conditions of heavy metal (Cd, Co, and Pb)-polluted soil, demonstrating that AM colonization has an alleviating effect on barley under heavy metal conditions [43]. Another study found that R. irregularis boosted Zn uptake in barley plants as compared to non-inoculated plants [73] because AM fungi explore the soil volume beyond the nutrient depletion zone of the roots. AM fungi are in a better position to supply a plant with inorganic soil nutrients such as Zn²⁺ in higher amounts than found in the plants. Furthermore, another study indicates that the addition of humic acid may improve the performance of AM fungi, as a result, AM fungi may increase zinc absorption and improving plant zinc nutrition indirectly [74]. Under salinity conditions, the AM fungus G. intraradices promoted P, Fe, and Zn uptake in barley plants, while it inhibited the uptake of sodium (Na) in the host plants [75]. In buckwheat (Fagopyrum esculentum), the total N and P absorptions were positively affected by the mixed AM fungi under inorganic and organic P applications [49]. It has been stated that the mixed AM fungi might have a more positive impact on plants; such an example was found when millet (Pennisetum glaucum) plants were treated with mixed AM fungi, which led to higher P, K, Ca, Mg, and Zn absorptions in roots as compared to the controls [76]. Similarly, millet plants inoculated with Emericella rugulosa had higher nutrient levels, especially P in the roots and shoots, and this may be because E. rugulosa produces phosphatases and phytase, which mobilize P and enhance millet plants’ growth and productivity [77]. The application of three AM fungi, i.e., G. mosseae, G. fasciculatum, and G. decipiens, enhanced millet plants’ growth and glomalin-related soil protein (GRSP) under barren soil conditions [78], suggesting that AM fungi contribute to heavy metal sequestration in polluted soils and sediments in semi-arid environments.

Table 2. The role of AM fungal spores in nutrient uptake in different plant stages of cereal plants.

Plant	AM Fungi Spore	Plant Stage	Nutrient Uptake	Environmental Conditions	References
Wheat	Glomus species	Tillering stage, heading stage	Nitrogen	Under ozone stress conditions	[79]
Wheat	R. tenuis	Vegetative stage, fruiting stage	Phosphate	In a semi-arid field environment	[80]
Wheat	R. fasciculatus, F. mosseae	Fruiting stage	Zinc	Under drought stress conditions	[55]
Wheat	R. Intraradices	Tillering stage	Zinc	Under P application conditions	[81]
Maize	G. mosseae, G. etunicatum	Tillering stage	Nitrogen	Under zinc-deficient soil conditions	[82]
Maize	G. mosseae	Vegetative stage	Nitrogen	Under field conditions	[61]
Maize	R. irregularis	Fruiting stage	Phosphorus	Compartmented pots with radioactive P tracer conditions	[10]
Maize	G. clarum	Fruiting stage	Phosphorus	Under P deficient conditions	[36]
Rice	R. intraradices	Tillering and maturity stages	Nitrogen, phosphorus, and carbon	Under experimental greenhouse conditions	[39]
Rice	Glomus species	Early tillering stage	Nitrogen and phosphorus	Under wetland conditions	[83]
Rice	G. mosseae	Fruiting stage	Arsenic	Under As soil conditions	[84]
Rice	G. geosporum, G. mosseae	Fruiting stage	Phosphorus	Under As soil conditions	[84]
Barley	G. mosseae	Seedling, flowering, and fruiting stages	Zinc	Under Cd conditions	[85]
Barley	G. intraradices	Fruiting stage	Zinc	Under drought and seat stress conditions	[86]
Sorghum	A. scrobiculata	Harvesting stage	Nitrogen	Under greenhouse conditions	[87]
Sorghum	Glomus species	Harvesting stage	Phosphorus	Under greenhouse conditions	[87]
Sorghum	R. irregularis	Fruiting stage	Phosphorus	Under low-phosphorus soil conditions	[69]
Sorghum	G. etunicatum and G. intraradices	Fruiting stage	Zinc, magnesium, and iron	Under micronutrient-deficient conditions	[88]
Oat	G. mosseae	Fruiting stage	Nitrogen and phosphorus	Under nutrient deficient condition	[89]
Oat	R. irregularis	Fruiting stage	Mineral nutrition content	Under conditions of different levels of P	[13]
Buckwheat	Glomus species	Harvesting stage	Phosphorus	Under low to medium soil pH conditions	[49]
Buckwheat	Glomus species	Harvesting stage	Nitrogen	Under low to medium soil pH conditions	[49]
Quinoa	G. mosseae	Fruiting stage	Cesium	Under loamy sand conditions	[50]
Quinoa	G. mosseae	Fruiting stage	Nitrogen	Under conditions of different nitrogen levels	[51]
Millet	G. mosseae	Fruiting stage	Nitrogen	Under experimental pot conditions	[52]
Millet	G. mosseae	Fruiting stage	Phosphorus	Under experimental pot conditions	[52]
Millet	G. mosseae	Fruiting stage	N, P, and K	Under cow dung (CD) or poultry manure (PM) conditions	[90]

Table 2. The role of AM fungal spores in nutrient uptake in different plant stages of cereal plants.

Plant	AM Fungi Spore	Plant Stage	Nutrient Uptake	Environmental Conditions	References
Wheat	Glomus species	Tillering stage, heading stage	Nitrogen	Under ozone stress conditions	[79]
Wheat	R. tenuis	Vegetative stage, fruiting stage	Phosphate	In a semi-arid field environment	[80]
Wheat	R. fasciculatus, F. mosseae	Fruiting stage	Zinc	Under drought stress conditions	[55]
Wheat	R. Intraradices	Tillering stage	Zinc	Under P application conditions	[81]
Maize	G. mosseae, G. etunicatum	Tillering stage	Nitrogen	Under zinc-deficient soil conditions	[82]
Maize	G. mosseae	Vegetative stage	Nitrogen	Under field conditions	[61]
Maize	R. irregularis	Fruiting stage	Phosphorus	Compartmented pots with radioactive P tracer conditions	[10]
Maize	G. clarum	Fruiting stage	Phosphorus	Under P deficient conditions	[36]
Rice	R. intraradices	Tillering and maturity stages	Nitrogen, phosphorus, and carbon	Under experimental greenhouse conditions	[39]
Rice	Glomus species	Early tillering stage	Nitrogen and phosphorus	Under wetland conditions	[83]
Rice	G. mosseae	Fruiting stage	Arsenic	Under As soil conditions	[84]
Rice	G. geosporum, G. mosseae	Fruiting stage	Phosphorus	Under As soil conditions	[84]
Barley	G. mosseae	Seedling, flowering, and fruiting stages	Zinc	Under Cd conditions	[85]
Barley	G. intraradices	Fruiting stage	Zinc	Under drought and seat stress conditions	[86]
Sorghum	A. scrobiculata	Harvesting stage	Nitrogen	Under greenhouse conditions	[87]
Sorghum	Glomus species	Harvesting stage	Phosphorus	Under greenhouse conditions	[87]
Sorghum	R. irregularis	Fruiting stage	Phosphorus	Under low-phosphorus soil conditions	[69]
Sorghum	G. etunicatum and G. intraradices	Fruiting stage	Zinc, magnesium, and iron	Under micronutrient-deficient conditions	[88]
Oat	G. mosseae	Fruiting stage	Nitrogen and phosphorus	Under nutrient deficient condition	[89]
Oat	R. irregularis	Fruiting stage	Mineral nutrition content	Under conditions of different levels of P	[13]
Buckwheat	Glomus species	Harvesting stage	Phosphorus	Under low to medium soil pH conditions	[49]
Buckwheat	Glomus species	Harvesting stage	Nitrogen	Under low to medium soil pH conditions	[49]
Quinoa	G. mosseae	Fruiting stage	Cesium	Under loamy sand conditions	[50]
Quinoa	G. mosseae	Fruiting stage	Nitrogen	Under conditions of different nitrogen levels	[51]
Millet	G. mosseae	Fruiting stage	Nitrogen	Under experimental pot conditions	[52]
Millet	G. mosseae	Fruiting stage	Phosphorus	Under experimental pot conditions	[52]
Millet	G. mosseae	Fruiting stage	N, P, and K	Under cow dung (CD) or poultry manure (PM) conditions	[90]

3. AM Fungi and Photosynthetic Activity of Cereal Crops

AM fungi inoculation has been reported to influence photosynthetic parameters, i.e., chlorophyll-a (Chl-a), chlorophyll-b (Chl-b), carotenoids (Caro), and the SPAD value. AM fungi increase photosynthetic activity, regulate stomatal conductivity, and enhance tolerance against various stress conditions, resulting in increased plant growth (Figure 2). AM fungi were reported to increase the photosynthesis rate in wheat, maize, and rice by facilitating the uptake of N and P from the soil. Beltrano and Ronco [33] and Peterson et al. [91] reported that wheat inoculated with AM fungi showed higher chlorophyll contents as compared to non-inoculated plants under drought stress conditions. Further, the AM fungus F. mosseae increased photosynthetic activity and mitigated the negative effects of environmental stressors on wheat growing in salty soil [31]. AM fungi were reported to protect the water splitting complex followed by enhancing the primary photochemistry of photosystem-II (PSII) under high temperatures. The leaf area and photosynthetic rate (Pn) of maize plants were positively influenced by two AM fungi species, G. mosseae and G. intraradices [37]. Compared to non-inoculated plants, G. etunicatum improved maize chlorophyll content and Pn by up to 29% [36]. This is because AM fungi positively influence the P content of maize, which, in turn, influences a variety of physiological processes, including photosynthesis. Similarly, the AM fungus Glomus tortuosum improved physiological metabolisms by increasing the chlorophyll content, light energy utilization efficiency, gas exchange, and rubisco activity of maize under salinity stress conditions [92]. This suggest that AM fungi could mitigate the growth limitations caused by salinity stress and hence play a very important role in promoting the photosynthetic capacity of maize under salt stress.

AM fungi inoculation increased photosynthesis as well as soluble carbohydrates in rice plants; this is because AM fungi improved the efficiency of PSII photochemistry as compared to the non-inoculated plants [93]. AM fungi were observed to enhance photosynthetic activities in barley plants [94]. According to Achatz et al. [95], enhanced AM colonization leads to early plant development and higher phosphate supply, resulting in a very positive influence on the photosynthesis and stomatal conductivity of barley plants. An additional study found that AM fungi had a favorable influence on rubisco and PSII in barley, and thus improved its tolerance against salt and drought stress [96,97]. AM fungi favorably interact with plants and other microorganism to increase plants’ N uptake, resulting in increased photosynthesis rates and growth in various plants including sorghum [98]. Under drought stress conditions, AM fungi boosted agro-physiological characteristics, including photosynthesis and grain production, in sorghum plants by supplying more water and increasing water use efficiency [99]. This might be because AM fungi improved the roots’ capacity to absorb soil moisture, which kept the stomata open in the leaves and increased dry matter production. Water conductivity improvement may also be due to an increase in root surface area for water and P absorption, as well as improved osmoregulation provided by AM fungi and rhizobacteria in the soil. In the context of quinoa plants inoculated with AM fungi (G. mosseae and Glomus tortuosum), the results showed a considerable increase in chlorophyll content, as well as PSII photochemical efficiency [100]. AM fungi assisted N uptake in quinoa, which is associated with high enzymatic activity leading to a higher chlorophyll content and photosynthetic activity [100]. When millet plants were inoculated with Glomus fasciculatum under salt conditions, the total chlorophyll content and plant growth were significantly increased due to positive changes in antioxidant enzymatic activities [101]. Additionally, the role of AM fungi in cereal crops regarding photosynthesis has been thoroughly researched; in the context of AM fungi, some plants, such as buckwheat, quinoa, and millet, required further exploration. Nonetheless, a thorough study and understanding of the deep mechanisms of photosynthesis are require further investigation.

4. AM Fungi with Primary and Secondary Metabolites

AM fungi are essential for the beneficial enhancement of primary and secondary metabolites, which are required for plant development, enzymatic activities, and other processes, including stress tolerance (Figure 3). AM fungi increase water and nutrient absorption, recalibrate the metabolic pathways of plants, and affect the concentration of primary and secondary metabolites [1]. The studies by Pepe et al. [20] and Ryan et al. [21] showed that some essential phytochemicals (phenolic acids, flavones, and phytic acid) belonging to secondary metabolites were higher in cereal plants under AM fungi inoculation. The concentrations of phytochemicals such as alkaloids, terpenoids, flavonoids, and organic compounds were also reported to be higher in AM-inoculated plants [22,23,24]. AM fungi also increase the photosynthetic rate by activating the primary and secondary metabolomic biosynthesis pathways via changes in phytohormonal concentrations and creating signaling molecules [60]. According to Bowles et al. [102], AM fungi improved nutrient uptake, especially of N and P, which is associated with increased enzymatic activity, leading to increased synthesis of primary and secondary metabolites. Talaat and Shawky [103] reported that AM fungi had a significant impact on the Membrane Stability Index (MSI), photochemical reactions during photosynthesis, carbohydrates, and soluble protein in two wheat cultivars (cv. Sids 1 and cv. Giza 168). Another study found that AM fungi increased proline biosynthesis and 9-cis-epoxycarotenoid dioxygenase (nced) activity in wheat, increased protein synthesis, and sped up the metabolic processes of the plants, resulting in higher anti-oxidative reactions and immune responses, which lead to increased tolerance against abiotic stresses in plants [104]. These results suggested that AM fungi may potentially have a role in the synthesis of essential plant hormones such as abscisic acid. The AM fungus F. mosseae alleviated the negative effect of heavy metals, promoted lipid production, and increased carbohydrate concentrations in wheat, which showed higher Performance Index (PI) values under Cd conditions [105,106]. By enhancing the amino acid biosynthesis pathway, AM fungi in combination with plant growth-promoting rhizobacteria (PGPR) improved sugar, starch, and galactose metabolism in wheat and barley plants [72]. Similarly, AM fungi improved soil fertility and increased tolerance against different environmental stresses, which have positive effects on both the quantity and quality of the secondary metabolites [16]. G. intraradices promoted the concentration of glucose and glyceraldehyde 3-phosphate, while G. mosseae, G. intraradices, and G. rosea increased the levels of cyclohexanone and its derivatives, which lead to higher secondary metabolites (Table 3). Higher AM colonization was reported to increase flavonoid, iso-flavonoid, phenolic, triterpenoid, cinnamic acid amide, and Apo-carotenoid accumulation in the roots and shoots of barley [107].

AM fungi were reported to mediate the production of organic acids such as oxalic, malonic, fumaric, malic, citric, and T-aconitic in maize roots through the seed coating [108]. AM fungi significantly increased antioxidant enzymes and antioxidant activity in oat leaves, and increased tolerance against abiotic stress conditions [109]. In another study, AM fungi colonization effectively counteracted sulfur dioxide (SO₂)-induced alterations, increased the photosynthetic rate, maintained Superoxide dismutase (SOD) activity, and increased catalase (CAT) activity in oats under salt stress condition [110]. Plants cultivated in Arabian medium crude oil (ACO) with the AM fungus, i.e., Glomus intraradices, had a considerably improved degradation of ACO, but there were no variations in proline, total phenolic, nitrate reductase levels, or plant–gas exchange [111].

AM fungi stimulated plant metabolism and homeostasis by increasing dehydrogenase (DH) activity in oat, which is involved in the synthesis of nicotinamide adenine dinucleotide phosphate (NADPH) and nicotinamide adenine dinucleotide (NADH); both are involved in plant homeostasis against different stresses [112]. When sorghum plants were exposed to varying levels of chromium (Cr) stress, the plant tolerance increased due to higher antioxidant enzyme activity and primary metabolites under AM fungi inoculation [113]. Similarly, in another study, AM fungi were discovered to protect plants from oxidative stress by boosting antioxidant enzymatic activity in sorghum [114]. Furthermore, under Fe deficiency, AM fungi improved the enzymatic pathways that inhibit oxidation and enhanced secondary metabolites in sorghum [115,116]. Two AM fungi, i.e., G. mosseae and G. tortuosum, increased soluble sugar and proline content, as well as enzymatic activity, in quinoa, but decreased these when high N was applied. It is suggested that AM fungi could perform better under medium-N application [51]. In quinoa plants, the concentrations of natural lipid fatty acids (NLFAs) and phospholipid fatty acids (PLFAs) were higher than in wheat, millet, and sorghum in bulk soil under AM inoculation [117]. The soluble sugar, proline, and flavonoid contents were found to be higher with the AM fungus R. intraradices in millet plants [118]. In another experiment, it was shown that F. mosseae increased the primary metabolomics, including fatty acids and enzymatic activities, of millet plants in contrast to non-inoculated plants [119]. In the same report, another AM fungus, R. intraradices, was shown to increase the concentration of benzenoids, phenols, and flavonoids in millet, suggesting that AM fungi facilitate the production of secondary metabolites. In most cases, AM symbioses promote the accumulation of primary and secondary metabolites in many plants, including cereals, which have a positive effect on plant growth and development. To expand understanding in this area, studies with many other plants should be conducted; in the case of cereal, the use of nitrogen-fixing bacteria in combination with AM fungi aiming to optimize the synthesis of bioactive chemicals should also be investigated.

Table 3. The role of AM fungal spores in improving primary and secondary metabolites in different cereal plants.

Plant	AM Fungi Spore	Primary Metabolites	Secondary Metabolites	Environmental Conditions	References
Wheat	Glomus species	Proline and glycinebetaine	_	Under salt stress conditions	[105]
Wheat	Mix-AMF	γ-amino butyric acid	_	Under rainfed field conditions	[72]
Wheat	F. mosseae	Amino acid (3-phospho-hydroxypyruvate) and carbohydrates (mannosylfructose-phosphate)	Flavonoids, terpenoids, and staurosporine (alkaloids)	Under water stress conditions	[120]
Wheat	F. Mosseae, C. claroideum	_	Production of phenolic compounds	Under drought stress conditions	[121]
Maize	R. intraradices, F. mosseae, F. geosporum	Carbohydrates and photosynthates	_	Under high-temperature stress conditions	[122]
Maize	G. albida, C. etunicatum, A. longula	Total proteins	Phenols and tannins	Under experimental greenhouse conditions	[123]
Maize	Glomus species	Carbohydrate, leaf soluble sugar, and proline content	_	Under different temperature stress conditions	[30]
Maize	Mix-AMF	Protein levels	_	Under field conditions	[124]
Rice	G. etunicatum, G. geosporum, G. mosseae	Cyanidin-3-glucoside and peonidin-3-glucoside	_	Under salt stress conditions	[125]
Rice	Glomus species	Fatty acids, amino acids, and carotenoids	Terpenoids	Under Cd soil conditions	[126]
Barley	G. intraradices	Glucose and glyceraldehyde 3-phosphate	_	Under feeding experimental conditions	[127]
Barley	G. mosseae, G. intraradices, G. rosea	_	Cyclohexenone and its derivatives	Pot greenhouse experimental conditions	[128]
Barley	G. intraradices	_	Hydroxycinnamic acid amides, yclohexenone derivatives, and blumenin	Under defined nutritional medium conditions	[129]
Sorghum	G. mosseae, G. intraradices	Octadecane, pentaethylene glycol, acetic acid, and pentaethylene glycol	_	Under volatile organic compound (VOC) conditions	[130]
Sorghum	Mix-AMF	_	Anthocyanin, polyphenols, and flavonoids	Under drought stress conditions	[131]
Sorghum	Glomus species	Glucose, fatty acids, and methionine	Ferulic acid and phenolic compounds, 3,4-dihydroxycinnamic acid	Under marginal soil conditions	[132]
Oat	R. irregularis	Ascorbic acid and glutathione content	_	Under sulfur dioxide (SO2) exposure conditions	[111]
Oat	G. intraradices	_	Terpenoid glycoside and phenolic compounds	Under defined nutritional medium condition	[133]
Oat	G. intraradices	_	Sesquiterpenoid cyclohexenone derivatives	Under defined nutritional medium conditions	[134]
Oat	G. intraradices	Free amino acids and proteins	_	Under N application conditions	[135]
Buckwheat	Glomus species	_	Flavonoid content	Under UV-B radiation conditions	[136]
Buckwheat	Mix-AMF	Carbohydrates	_	Under greenhouse conditions	[47]
Buckwheat	Mix-AMF	Fatty acids	_	Under temperate agricultural soil conditions	[119]
Quinoa	G. mosseae	Soluble sugar	_	Under conditions of different nitrogen levels	[51]
Quinoa	Mix-AMF	Natural lipids	_	Under temperate agricultural soil conditions	[119]
Quinoa	Mix-AMF	_	Polyphenol compounds	Under salt stress conditions	[137]
Millet	R. intraradices	_	Benzenoid, phenol, and flavonoid content	Under sandy loam soil conditions	[121]
Millet	F. mosseae	Fatty acids	_	Under sandy clay loam conditions	[121]
Millet	R. intraradices	Proline and soluble sugar content	Phenol and flavonoid content	Under drought stress conditions	[120]

_ indicates that no result is available in the study.

Table 3. The role of AM fungal spores in improving primary and secondary metabolites in different cereal plants.

Plant	AM Fungi Spore	Primary Metabolites	Secondary Metabolites	Environmental Conditions	References
Wheat	Glomus species	Proline and glycinebetaine	_	Under salt stress conditions	[105]
Wheat	Mix-AMF	γ-amino butyric acid	_	Under rainfed field conditions	[72]
Wheat	F. mosseae	Amino acid (3-phospho-hydroxypyruvate) and carbohydrates (mannosylfructose-phosphate)	Flavonoids, terpenoids, and staurosporine (alkaloids)	Under water stress conditions	[120]
Wheat	F. Mosseae, C. claroideum	_	Production of phenolic compounds	Under drought stress conditions	[121]
Maize	R. intraradices, F. mosseae, F. geosporum	Carbohydrates and photosynthates	_	Under high-temperature stress conditions	[122]
Maize	G. albida, C. etunicatum, A. longula	Total proteins	Phenols and tannins	Under experimental greenhouse conditions	[123]
Maize	Glomus species	Carbohydrate, leaf soluble sugar, and proline content	_	Under different temperature stress conditions	[30]
Maize	Mix-AMF	Protein levels	_	Under field conditions	[124]
Rice	G. etunicatum, G. geosporum, G. mosseae	Cyanidin-3-glucoside and peonidin-3-glucoside	_	Under salt stress conditions	[125]
Rice	Glomus species	Fatty acids, amino acids, and carotenoids	Terpenoids	Under Cd soil conditions	[126]
Barley	G. intraradices	Glucose and glyceraldehyde 3-phosphate	_	Under feeding experimental conditions	[127]
Barley	G. mosseae, G. intraradices, G. rosea	_	Cyclohexenone and its derivatives	Pot greenhouse experimental conditions	[128]
Barley	G. intraradices	_	Hydroxycinnamic acid amides, yclohexenone derivatives, and blumenin	Under defined nutritional medium conditions	[129]
Sorghum	G. mosseae, G. intraradices	Octadecane, pentaethylene glycol, acetic acid, and pentaethylene glycol	_	Under volatile organic compound (VOC) conditions	[130]
Sorghum	Mix-AMF	_	Anthocyanin, polyphenols, and flavonoids	Under drought stress conditions	[131]
Sorghum	Glomus species	Glucose, fatty acids, and methionine	Ferulic acid and phenolic compounds, 3,4-dihydroxycinnamic acid	Under marginal soil conditions	[132]
Oat	R. irregularis	Ascorbic acid and glutathione content	_	Under sulfur dioxide (SO2) exposure conditions	[111]
Oat	G. intraradices	_	Terpenoid glycoside and phenolic compounds	Under defined nutritional medium condition	[133]
Oat	G. intraradices	_	Sesquiterpenoid cyclohexenone derivatives	Under defined nutritional medium conditions	[134]
Oat	G. intraradices	Free amino acids and proteins	_	Under N application conditions	[135]
Buckwheat	Glomus species	_	Flavonoid content	Under UV-B radiation conditions	[136]
Buckwheat	Mix-AMF	Carbohydrates	_	Under greenhouse conditions	[47]
Buckwheat	Mix-AMF	Fatty acids	_	Under temperate agricultural soil conditions	[119]
Quinoa	G. mosseae	Soluble sugar	_	Under conditions of different nitrogen levels	[51]
Quinoa	Mix-AMF	Natural lipids	_	Under temperate agricultural soil conditions	[119]
Quinoa	Mix-AMF	_	Polyphenol compounds	Under salt stress conditions	[137]
Millet	R. intraradices	_	Benzenoid, phenol, and flavonoid content	Under sandy loam soil conditions	[121]
Millet	F. mosseae	Fatty acids	_	Under sandy clay loam conditions	[121]
Millet	R. intraradices	Proline and soluble sugar content	Phenol and flavonoid content	Under drought stress conditions	[120]

_ indicates that no result is available in the study.

5. The Roles of AM Fungi in Grain Yield and the Quality of Cereal Crops

AM fungi G. intraradices and G. mosseae with Trichoderma atroviride improved wheat grain productivity by 32.1 and 8.3%, respectively. AM fungi alter micronutrient availability and absorption of N, P, and other micronutrients at grain filling stage, resulting higher protein concentration and enhanced cereal crop quality and quantity [138]. In two wheat cultivars, i.e., Brookton and Krichauf, AM plants produced a lower grain yield per plant without the addition of P, while the addition of P positively affected grain yield, and the cultivar Brookton was more efficient in the case of grain weight as compared to Krichauf in highly calcareous soil [139]. Generally, it is concluded that AM fungal colonization increases P absorption by the AM pathway, which improves resource accumulation and promotes flowering initiation [140]. This influence may, in turn, contribute to increased reproductive success since early flowering leads to a higher number of flowers (and therefore grain) [74]. In maize, G. intraradices increased the silage yield, as well as the green and dry matter yield, under both irrigated and non-irrigated conditions; AM fungi strengthen the plants’ ability to increase their tolerance to biotic and abiotic stress conditions under high- and low-humidity conditions [141]. Similarly, AM fungi and Azotobacter chrocoocum facilitated N and P uptake during the fruiting stage and enhanced the cob weight, length, grain weight, and starch content of maize [142]. Rice plants treated with F. mosseae, Acaulospora laevis, and Gigaspora margarita improved spikelet fertility (%), and rice productivity by 125% and 143%, respectively, under salt treatments [143]. At the mature stage, the inoculated rice allocated more nutrients to reproductive parts as compared to the non-inoculated plants and had 18.4% increase in grain weight. However, AM fungi inoculation had no significant effect on the contribution of C or N translocation to seeds, which may be the result of the simultaneous increase in sink potential under inoculation. Furthermore, the 100-seed weight was also reduced by 4.0%, while the panicle number was increased by 26.1%; as a result, the grain yield was increased by 28.2% in rice compared to the control treatment [39]. Barley plants treated with R. irregularis had improved grain yields and biochemical characteristics of seeds due to the boosting of Zn concentrations and starch content in two cultivars [29]. Similarly, the use of five AM fungi, Pacispora franciscana, F. mosseae, F. geosporum, R. irregularis, and Glomus tenebrosum, boosted barley kernel weight and grain production by 90% and 68%, respectively. The levels of K, Cu, Fe, Zn, and Ca in grain were likewise significantly greater in inoculated plants, whereas the Na content in grain was lower [144]. The sorghum cultivars (Ajabsido-MNO9-7018, Macia-PRO9110-4319, and Sureno (Latin American; PRO9110-4317)) produced 285 % more grain/plants under AM inoculation since it has been observed that AM colonization allocates available nutrients to grain rather than vegetative biomass (harvest index) [145]. Furthermore, G. mosseae increased the grain yield by 27% and significantly improved the agronomic characteristics of sorghum plants under drought stress condition [101]. AM fungus R. irregularis was applied to sorghum plants resulting in the accumulation of higher amounts of P, Zn, and Fe in the grain, which resulted in higher yield and harvest indices as compared to non-inoculated plants [73]. The plant growth and yield of oat plants increased when barley and rye (Secale cereal) crops were recycled with AM fungi in the cropping system, suggesting that a low-input cropping system with the application of AM fungi could increase oat yield and productivity [146]. In another study, after 45 days of treatment with mixed-AM fungi, oat plant ‘variety Pepita’ performed better than oat ‘variety Supernova’ in terms of growth and yield production in a field experiment held in Southern Chile [147]. In combination with Azotobacter chroococcum and Trichoderma harzianum, the AM fungus Acaulophora laevis showed 95% higher colonization and increased herbage yield of Buckwheat plants, demonstrating that AM fungi are environmentally friendly with other microorganisms and facilitate higher yields and productivity [48]. In the same study, large flower clusters, herbage yields, the number of seeds per cyme, the maximum harvest index, and seed yields were higher in buckwheat under AM fungi application. In quinoa, the addition of organic compost inoculated with mixed-AM fungi led to increases in dry weight, grain production, and nutritional quality under drought stress [148]. Furthermore, quinoa treated with G. mosseae had increased plant shoot growth, but it had no significant effect on yield [51]. Two AM fungi, i.e., Rhizophagus fasciculatus and Ambispora leptoticha, in combination with PGPR bacteria (Pseudomonas) increased grain yields more effectively than single inoculation, suggesting that the application of AM fungi and PGPR bacteria together could boost millet plant growth and productivity [149]. When mixed commercial AM fungi were treated with SWSC (solid waste-based soil conditioner), AM colonization rates rose up to 81%, resulting in higher millet growth and yield compared to the control [150]. Moreover, the hyphae of the AM fungus C. etunicatum extended throughout a 12 cm soil layer, absorbing more nutrients and resulting in higher growth, revealing that the AM fungus has the potential to boost millet yield and productivity [151]. The majority of the research has claimed that AM fungi have good impacts on grain yield and quality, while only few studies have shown that AM fungi have a detrimental effect on grain yield and quality. In addition, the roles of many AM fungus spores are unknown; as a result, this is an opportunity for researchers to learn more about the impact of various and distinct AM fungal spores on cereal crops.

6. Conclusions

Arbuscular mycorrhizal (AM) fungi have many roles in various developmental processes in plants, especially in cereals. AM fungi have an effect on nutrient availability and uptake, increase the photosynthetic rate, improve antioxidant activities, and increase tolerance against environmental stress. Moreover, AM fungi have a positive impact on both the primary and secondary metabolites and also increase growth, yield, and productivity. AM fungi are utilized in greenhouses and on a smaller scale in agricultural systems, but it is possible that they may also be used on a larger scale. However, there are a higher number of AM fungi spores and the function of each group or each spore in different crops is still unknown. More studies are required to investigate the role and function of AM fungi spores in numerous plants, particularly cereal crops. In addition, the molecular processes and genetic aspects of each species should be researched in order to have a better understanding of the distinctions in the functions that are present in different AM fungi species. Plants such as oat and barley plants should be more thoroughly investigated under AM conditions to provide more knowledge about the effects of AM fungi on these plants since there has not been much study on these plants in relation to AM symbiosis.