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Loo, W.T.;  Chua, K.;  Mazumdar, P.;  Cheng, A.;  Osman, N.;  Harikrishna, J.A. Arbuscular Mycorrhizal Symbiosis and Climate Change Stress Alleviation. Encyclopedia. Available online: https://encyclopedia.pub/entry/34237 (accessed on 21 May 2024).
Loo WT,  Chua K,  Mazumdar P,  Cheng A,  Osman N,  Harikrishna JA. Arbuscular Mycorrhizal Symbiosis and Climate Change Stress Alleviation. Encyclopedia. Available at: https://encyclopedia.pub/entry/34237. Accessed May 21, 2024.
Loo, Wan Teng, Kah-Ooi Chua, Purabi Mazumdar, Acga Cheng, Normaniza Osman, Jennifer Ann Harikrishna. "Arbuscular Mycorrhizal Symbiosis and Climate Change Stress Alleviation" Encyclopedia, https://encyclopedia.pub/entry/34237 (accessed May 21, 2024).
Loo, W.T.,  Chua, K.,  Mazumdar, P.,  Cheng, A.,  Osman, N., & Harikrishna, J.A. (2022, November 13). Arbuscular Mycorrhizal Symbiosis and Climate Change Stress Alleviation. In Encyclopedia. https://encyclopedia.pub/entry/34237
Loo, Wan Teng, et al. "Arbuscular Mycorrhizal Symbiosis and Climate Change Stress Alleviation." Encyclopedia. Web. 13 November, 2022.
Arbuscular Mycorrhizal Symbiosis and Climate Change Stress Alleviation
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Climate change is likely to have severe impacts on food security in the topics as these regions of the world have both the highest human populations and narrower climatic niches, which reduce the diversity of suitable crops. Legume crops are of particular importance to food security, supplying dietary protein for humans both directly and in their use for feed and forage. Other than the rhizobia associated with legumes, soil microbes, in particular arbuscular mycorrhizal fungi (AMF), can mitigate the effects of biotic and abiotic stresses, offering an important complementary measure to protect crop yields. 

abiotic stress arbuscular mycorrhizae biotic stress

1. Alleviation of Abiotic Stress

Numerous studies report that climate change-related abiotic stresses including heat, drought, salinity, and waterlogging impair the uptake of soil nutrients and water balance [1][2][3]. These phenomena cause crop yield to reduce significantly, resulting in increased pressure for food production. Although the use of chemical fertilizers can increase soil fertility and crop productivity, excessive use of agro-chemicals reduces the soil organic matter and quality, and the residues contribute to pollution of adjacent water bodies [4]. To circumvent these problems, farming communities are considering soil microorganism such as AMF for sustainable agricultural practice.

1.1. Heat Stress

Extreme heat stress affects legume growth and metabolism. Under heat stress, heat-sensitive enzymes involved in physiological processes are inhibited, causing a disruption in the cellular homeostasis; this is associated with the accumulation of harmful reactive oxygen species (ROS) [5]. This was reflected in elevated electrolyte leakage, proline, malondialdehyde (MDA), and hydrogen peroxide (H2O2) contents in heat-stressed faba bean [6] and mung bean (Vigna radiata) [7] plants. Heat stress also affects the reproductive stages and yield of legumes. Heat-stressed green bean (Phaseolus vulgaris) plants showed delayed flowering and decreased pollen viability and pod and seed yields as compared to non-stressed plants [8]. Similarly, a 10-day exposure to 35/16 °C (day/night) during the flowering and pod development stage resulted in decreased pod yield in chickpea (Cicer arietinum) plants [9].
Studies have shown that AMF help in alleviating the negative effects of heat stress in many plants, although relevant information on AMF–legume interaction is limited. Under heat stress, the ability of plant roots to absorb water and nutrients reduces. AMF improve plant tolerance to heat mainly through enhancement of water and nutrient uptake, which in turn improves plant growth and yield under heat stress [10]. This is evident from higher water use efficiency, water holding capacity, and relative water content in AMF-inoculated maize (Zea mays) grown at 40 °C [11]. Meanwhile, AMF-inoculated asparagus (Asparagus officinalis) accumulated more of the macronutrients nitrogen (N), phosphorous (P), and potassium (K), and micronutrients such as calcium (Ca), magnesium (Mg), and iron (Fe) than non-AMF plants under heat stress [12]. In the model legume plant M. truncatula, a night temperature elevated by 1.53 °C negatively affected growth. Inoculation with the AMF Rhizophagus irregularis mitigated the effects of heat stress and enhanced M. truncatula growth in terms of biomass, flower and seed number, leaf sugar, shoot zinc, and root phosphorus contents [13]. While the mechanisms have not been reported for any legume species, AMF have been associated with improved photosynthetic capacity, stomatal conductance, and transpiration rate in heat-stressed maize inoculated with a mixed AMF culture of R. irregularis, Funneliformis mosseae, and F. geosporum [14]. The improved photosynthesis in AMF-inoculated plants could be attributed to protective effects from the symbiotic fungi against oxidative damage caused by high temperature. Under heat stress, mycorrhizal plants often exhibit enhanced activities of various antioxidant enzymes [12][15]. AMF Septoglomus deserticola and S. constrictum ameliorated heat stress-associated oxidative damage in tomato (Solanaceae lycopersicum) by reducing the levels of lipid peroxidation and H2O2, while elevating the antioxidant enzyme activities in root and leaves [16].

1.2. Drought Stress

The impacts of drought on legume growth and yield involve a series of complex processes. Legumes respond directly to drought stress by triggering stomatal closure to prevent water loss through transpiration. This is evident from studies on soybean and green bean that reported a decrease in stomatal conductance and transpiration rate during a drought stress treatment [17][18]. Stomatal closure limits the CO2 intake and subsequently inhibits photosynthesis. In a drought treatment, a drought-sensitive soybean cultivar Anta82 experienced reduced photosynthesis rate after 3 days [17]
Studies have shown that AMF symbiosis aids in physiological regulation of legumes, which enhances their tolerance to drought. AMF colonize plant roots and develop an extensive network of extraradical hyphae in the soil surrounding the root, which help to absorb water from the soil [19] and enhance water uptake under drought conditions. Higher stomatal conductance, transpiration, and photosynthesis rates occurred in AMF-associated legumes such as soybean and green bean [17][18]. AMF treatment on legumes is also beneficial for the uptake of nutrients: When administrated with 45% to 75% water holding capacity, mycorrhizal green bean plants had increased macro- and micronutrients including N, P, K, Mg, Fe, zinc (Zn), manganese (Mn), and copper (Cu) [20]. AMF treatment also improved the green bean yield under drought stress as seeds with higher nutrient contents including N, K, Mg, Ca, vitamin B1, folic acid, crude fiber, and protein were produced compared to non-mycorrhizal plants [18].
Under long term water deficit, stomatal closure and low CO2 supply alter the cellular homeostasis and disrupt the electron transport and carbon-reduction cycle [21]. Low intercellular CO2 leads to over-reduction of electron transport components and subsequent leakage of electron to oxygen molecules which generates ROS. A high ROS accumulation causes oxidative damage to the nucleic acids, proteins, and lipids [22]. Drought stress resulted in high superoxide radical (O2), H2O2, and MDA accumulation in black locust which was ameliorated by AMF treatment. Mycorrhizal black locust exhibited higher activities of the antioxidant enzymes superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR) [23]. The ROS generated during drought stress also damage the photosynthetic apparatus of plants and this was evident from the reduced photosynthetic chlorophyll pigments in chickpea under water stress. This condition was ameliorated in mycorrhizal chickpea plants reflected by enhanced chlorophylls and carotenoid content [24].
Several studies have shown that interaction with AMF altered gene expression in the host legumes in response to drought stress. To combat the ROS generated during a drought treatment, mycorrhizal black locust plants exhibited higher gene expression for antioxidant enzymes such as Cu/Zn-superoxide dismutase (Cu/Zn-SOD), ascorbate peroxidase (APX), and glutathione reductase (GR) in the roots, stems, and leaves or at least one of the organs [23]. This shows that AMF–legume interaction provides protection against drought by inducing the expression of genes responsible for antioxidant enzyme activities. Aroca, et al. [25] reported that AMF treatment enhanced the tolerance of green bean plants to drought through regulation of various aquaporin genes that were found to be differentially expressed in the presence of AMF. A transcriptome analysis also revealed up- and downregulation of aquaporin-related genes in the leaves and roots of drought-stressed mycorrhizal green bean plants, together with altered transcription levels in pathways for osmoregulation, DNA repair, and response to oxidative stress during drought stress [26].

1.3. Salinity Stress

Salinity impedes the growth and decreases the yield of many legume species. Salinity tests (ranging from 50 to 250 mM NaCl) resulted in lower plant height and shoot and root biomass in green bean [27], soybean [28], pigeon pea [29], cowpea [30], and chickpea [31]. Salt stress also decreased pod yield and dry weight in faba bean and green bean [27][32]. These negative impacts are attributed to the osmotic, ionic and oxidative stresses that are induced under high salinity [33]. Studies have shown that AMF symbiosis reduces the negative impacts of salt stress in legumes. AMF-inoculated pea [34] and green bean [27] plants exhibited greater plant height, root length, and shoot and root biomass under salinity treatment, while mycorrhizal faba bean plants had higher numbers of pods per plant and higher pod dry weight [27][34]. Other than model AMF species such as Glomus irradicans [27], R. irregularis [29], and F. mosseae [35], the use of native AMF inoculum from saline soil also improved the growth and development of pigeon pea (Cajanus cajan) plants under salt stress [29][36].
High salinity levels induce osmotic stress that impairs the root system by reducing the water availability for plant metabolic processes [37]. AMF root colonization and extension of the fungal extraradical hyphae into the soil significantly enhance the water uptake in various legumes. This was reported for legume species such as cowpea, green bean, and fenugreek, where the AMF-inoculated plants exhibited significantly higher relative water content in their leaves when compared to non-inoculated plants [27][30][38].
Salinity also causes an ionic stress attributed to sodium (Na+) and chloride (Cl) ion build-up in the plant cytosol, which is toxic to the plants [39]. At the same time, other mineral ions such as K, Ca, P, and Mg are lower in legume plant cells [27][30][32][34], which can result in reduced photosynthetic pigments [27][38]. Mycorrhization of legumes alleviates the deleterious effects of salinity-induced ionic stress by reducing uptake of toxic Na+ and Cl, which is crucial in maintaining the ionic homeostasis in legume plant cells. As a result of AMF-inoculation, faba bean [32] and pea [34] plants retained higher P, K, Mg, and Ca contents and showed improved growth compared to non-mycorrhizal plants under high salinity. Mycorrhizal legumes also retained higher pigment contents compared to non-mycorrhizal legumes in a salinity condition, indicating the role of AMF in modulating plant ion contents such as Mg, an essential component of photosynthetic pigment [28][32][36].
Salinity also causes oxidative stress attributed to the build-up of ROS such as H2O2 and O2 which damage cellular lipid, proteins, and nucleic acids [40]. In response to salt stress, legumes produce antioxidant enzymes or antioxidant molecules to scavenge the aggressive ROS [29][41] and increase levels of proline that could reduce the oxidation of lipid [42]. AMF inoculation can enhance the salt tolerance of legumes such as green bean [27], faba bean [32], and pigeon pea [29] by elevating antioxidant enzyme levels. Compared to non-inoculated plants, these mycorrhizal legumes showed higher levels of SOD, CAT, GR, and POD. Mycorrhization of fenugreek and grass pea plants was also associated with enhanced proline content [38][43] although levels were reduced in mycorrhizal pea plants [34]. In addition, MDA, an end-product of lipid peroxidation, was reduced in various mycorrhizal legumes such as peanut [44], pigeon pea [29], and soybean [28] .
The complexity of AMF-induced salt tolerance in legumes has been alluded to from transcriptome studies: Transcriptome analysis identified differentially expressed genes (DEGs) that were responsible for regulation of biological processes pertinent to oxidation and reduction, oxidative stress response, cell wall, and cellular component organization in the roots of mycorrhizal peanut plants that were salt-stressed, as compared to non-mycorrhizal plants. The study also reported higher expression of peroxidase and glutathione S-transferase genes in mycorrhizal peanut plants [44]. In another study, AMF-mediated salt tolerance in Sesbania cannabina was associated with DEGs related to oxidation-reduction processes, photosynthesis, and several transcription factor groups. Elevated expression of genes related to SOD, CAT, POD, and GR was also observed in mycorrhizal S. cannabina plants, indicating the AMF role in enhancing the plant ROS-scavenging capability under salinity stress [45].
A majority of legume species form symbioses with rhizobia, which are beneficial for growth and productivity. However, the number of root nodules, nodule biomass, and leghemoglobin content in various legume plants decreases under high salinity [32][36][37][46]. This indicates reduced nitrogen fixation as leghemoglobin is responsible for supplying oxygen to nitrogen-fixing bacteria and protecting nitrogenase against oxygen damage in the nodules [47]. AMF inoculation alleviated these salt stress impacts in the legumes faba bean and soybean, which demonstrated enhanced nodulation and higher nitrogenase activity in their nodules [28][32][36]. Mycorrhization also led to higher accumulation of trehalose that can act as osmoprotectant in the nodules of salt-stressed pigeon pea [36] plants. Nonetheless, high salinization reduces AMF root colonization and spore counts in the rhizosphere, as reported in faba bean [32], grass pea [43], and pigeon pea [48] plants.

1.4. Waterlogging Stress

Legumes are very susceptible to waterlogging stress and do not thrive under inundated conditions. Under waterlogged conditions, soybean [49], cowpea [50], faba bean, grass pea, and lupins [51] suffered significant growth reduction and yield loss. Waterlogging causes air in the soil to escape and available oxygen is greatly reduced, resulting in a hypoxic condition in the rhizosphere that inhibits plant root respiration. Although plants can maintain energy production through anaerobic respiration, the process also accumulates toxic metabolites such as lactic acid, ethanol, aldehydes, and various ROS species [52][53]. High ROS levels cause oxidative damage to the cell membrane [54] and photosynthetic apparatus [50]. This is evident from the high cell membrane injury in green bean plants waterlogged for 7 days, and the significant decrease in stomatal conductance, chlorophyll contents, transpiration, and photosynthesis rates, as well as final seed yield in waterlogged mung bean [55] and cowpea [50]. Waterlogging also prevents root uptake of essential nutrients from the soil such as nitrogen and minerals. This leads to a nutrition imbalance which also contributes to reduced growth and yield loss in legumes. Although faba bean plants survived a 20-day waterlogging treatment, the plants showed severe reduction in total nitrogen uptake, in addition to decreased seed and biomass production [56].
Studies have shown AMF symbiosis to help plants to survive waterlogging stress. However, waterlogged soil creates an anaerobic condition which is unfavorable for AMF which are obligate aerobes [57] and decreases root colonization in various plants [57][58]. Nonetheless, some AMF such as Gigaspora species in rice ecosystems were found better adapted to semi-aerobic and anaerobic soils [59]. These AMF were shown to provide protective effects and enhance the growth of various plants under waterlogging stress. Although there is limited study on the role of AMF in enhancing legume growth and survival in waterlogged conditions, it was shown that the AMF root colonization of green bean plants was not affected by repeated short term flooding [60]. When AMF-colonized green bean plants were treated with short term flooding, they exhibited enhanced growth in terms of root dry weight [60]. This indicates the potential of AMF in alleviating the negative effects of waterlogging in legumes. As climate change is associated with more extremes in weather, including flooding, as well as predicted rises in sea levels in the tropical regions, it will be valuable to explore AMF that are able to mitigate waterlogging stress in tropical legumes.

2. Alleviation of Biotic Stress

The role of AMF in the alleviation of biotic stresses in tropical legumes has received much less attention compared to abiotic stresses [61]. The following are examples of pests and diseases that affect legumes and for which AMF have been reported to relieve symptoms. From the limited number of available reports, it can be suggested that much further research is needed in this area.

2.1. Bacterial Pathogens of Legumes

AMF colonization triggers mycorrhizal-induced resistance (MIR) in host plants, and activates immune responses such as callose deposition, cell wall thickening, and production of ethylene, ROS, and antimicrobial compounds [62]. Studies have shown that AMF colonization reduces disease symptoms of several bacterial pathogens in tropical legumes. Pseudomonas syringae pv. Glycinea (Psg) is a pathovar that causes bacterial blight in soybean plants, producing effector proteins that suppress the host plant’s immunity and resulting in leaf chlorosis and necrosis, lesions on soybean pods, and discoloration of the stem [63]. Inoculation of soybean with AMF species Entrophospora infrequens reduced Psg colonization of plants seven-fold compared to non-AMF plants [64]. The higher uptake and transfer of N and enhanced biomass production induced by E. infrequens was suggested to have an important role in improving the immunity of soybean plants. Another bacterial pathogen of legumes, Xanthomonas campestris pv alfalfae, is a pathovar that is responsible for leaf spots in several legume plants, including alfalfa and M. truncatula [65]. Inoculations of AMF species Glomus intraradices (reclassified as R. intraradices), Glomus versiforme (reclassified as Diversispora versiformis), and Gigaspora gigantea in M. truncatula infected with X. campestris reduced disease symptoms in the leaves and upregulated defense-related genes compared to non-AMF plants [66].

2.2. Fungal Pathogens of Legumes

Soil-borne fungal pathogens compete with AMF for infection sites and the presence of arbuscules in plant host cells can prevent invasion by hyphae of fungal pathogens [67]. Charcoal root rot is a soilborne disease caused by the broad-range fungus Macrophomina phaseolina. This pathogen infects the roots and lower stem of over 500 plant species including legumes such as peanut, soybean, and chickpea [68]. Multiple AMF species have shown to reduce the symptoms caused by M. phaseolina in legumes. In chickpea plants, inoculation with individual AMF species Glomus fasciculatum (reclassified as Rhizophagus fasciculatus), Glomus constrictum (reclassified as S. constrictum), G. intraradices (reclassified as R. intraradices), Gigaspora margarita, or Acaulospora sp. were able to reduce root-rot severity and increase plant growth, chlorophyll content, and the number of pods compared to non-AMF plants [69][70]. AMF species R. irregularis has been reported to upregulate pathogenesis/disease-resistant genes and increase lignin production in soybean plants under M. phaseolina infection compared to non-AMF plants [71]. This response reduces disease incidence and severity, leading to an improvement in plant growth and yield [72]. Various wilt diseases in legumes are caused by fungi, including Fusarium wilt in pigeon pea due to infection with Fusarium udum. Symptoms of infected plants include chlorosis, leaf and stem drooping, and wilting [73]. Inoculation of pigeon pea with AMF species G. fasciculatum (reclassified as R. fasciculatus) was able to significantly reduce wilting severity, and increased plant height, shoot dry weight, and phosphorous content compared to non-AMF plants [74]. Another wilt infection of pea that also leads to severe root rot and seedling damping off is caused by Aphanomyces euteiches [75]. This pathogen also affects a large range of other legume plants. Inoculation of pea with AMF species G. fasciculatum (reclassified as R. fasciculatus) and G. intraradices (reclassified as R. intraradices) significantly reduced spore production and root-rot severity compared to non-AMF plants [75][76][77]. Inoculation with G. intraradices (reclassified as R. intraradices) in pea also delayed and reduced the activity of A. euteiches enzymes such as glucose-6-phosphate dehydrogenase, phosphoglucomutase, and peptidase, which are essential for pathogenesis of A. euteiches [78][79]. Phytophthora sojae is a host-specific pathogen and only infects soybean. The disease causes damping off in seedlings, and root rot and stem lesions in mature plants [80]. Inoculation of AMF species G. intraradices (reclassified as R. intraradices) reduced oxidative damage in soybean plants infected with P. sojae by decreasing H2O2 content and increasing jasmonic acid content, glutathione reductase activity, and the metabolism of nitrogen and carbon compared to non-inoculated controls [81].

2.3. Nematode Infections of Legumes

AMF colonization leads to altered composition of exudates from the roots of host plants, which may affect nematode motility and infection [82]. The effect of root exudates on nematodes is species-dependent, so the degree of protection will be variable [83]. Heterodera cajani is a nematode species that mainly infects pigeon pea but it is also able to infect other legumes such as cowpea and mung bean, causing root galling, stunting, and leaf chlorosis [84]. Inoculation with AMF species F. mosseae reduced the H. cajani population by over 40% in infected pigeon pea plants and increased plant length, shoot dry weight, and phosphorous content compared to non-inoculated plants [74]. Another nematode species that can infect more than 3000 plant species including legumes such as cowpea and chickpea is Meloidogyne incognita. Found in tropical and subtropical regions, M. incognita causes root galling, reduced growth and leaf chlorosis [85]. Inoculation with individual species of AMF species G. fasciculatum (reclassified as R. fasciculatus), G. constrictum (reclassified as S. constrictum), G. intraradices (reclassified as R. intraradices), G. margarita or Acaulospora sp. in chickpea infected with M. incognita increased plant height, fresh and dry weight, yield, and chlorophyll content together with a reduced nematode population and less root galling than non-AMF plants [69][70].

2.4. Insect Pests of Legumes

In addition to bacterial, fungal, and nematode pathogens, inoculation of some legume plants with AMF species has been shown to reduce damage caused by insects. Well established AMF colonization increases biosynthesis of jasmonates in host plants [86]. Jasmonates regulate production and emission of volatile organic compounds such as terpenoids which repel pests or attract predators of pests [87]. Inoculation of M. truncatula with AMF species R. irregularis reduced phloem ingestion by the pea aphid Acyrthosiphon pisum, resulting in higher carbon content in the plants compared to non-inoculated plants [76]. Another example is inoculation with AMF species G. intraradices (reclassified as R. intraradices) in Vigna mungo (black gram) exposed to tobacco cutworm (Spodoptera litura). AMF-inoculated plants showed higher lignin content and plant biomass compared to non-inoculated plants [88].

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