7.1 Introduction

The world’s population is growing rapidly and has been predicted to exceed to even nine billion by the middle of this century (Rodriguez and Sanders 2015). Estimations indicate that the challenge to meet the ever-increasing demands of humankind will put a tremendous pressure on the global agriculture for almost doubling the food production. Unrestricted use of chemical pesticides and fertilizers for controlling plant pathogens and increasing food production has brought the world to the brink of an environmental catastrophe. According to the EU directive, in order to safeguard the human being and environmental health, and for the sustainable agriculture, it is of paramount importance to decrease the dependence of agrarian population on the use of agrochemicals for preventing the attack of harmful organisms and increasing crop production (EU Directive 2009/128/EC) (Berruti et al. 2016). Therefore, meeting the goal of forecasted agriculture production, it is imperative to implement alternative eco-friendly technologies, such as biocontrol agents, which is based on the sustainable utilization of natural resources. However, regardless of their massive potential, the use of these organisms has not been fully adopted by the farmers so far.

Amongst various biocontrol agents, arbuscular mycorrhizal fungi (AMF) appear to be most promising due to their well-established capability of increasing crop production by helping plants in combating various biotic and abiotic stresses. AMF belonging to the phylum Glomeromycota, develop mutual beneficial relationships with over 90% of terrestrial plants including agricultural and horticultural crops (Schüßler et al. 2001; Smith and Read 2008; Prasad et al. 2017). AM symbiotic association is believed to develop approximately 460 million years ago and perhaps played a major role in establishing the plants on land. In the plant root cortex, the fungal partner of this intimate association develops highly branched treelike structures termed as arbuscules (from Latin “arbusculum”, meaning bush or little tree), which are the functional sites of nutrient exchange, and balloon-like structures termed as vesicles, which are the storage organ of reserve food (Balestrini et al. 2015). AMF form two types of mycelium system, the intraradical and the extraradical in the plant root and soil, respectively. The extraradical hyphae emerge out from the root system and acquire nutrients from the soil (Miller et al. 1995). AMF extraradical hyphae explore a large volume of soil by extending several meters (extend beyond 100 m) away from the host plant’s roots; however, plant root hairs could extend one to 2 mm into the soil. The extensive extraradical mycelium formed by AMF connects many plant’s roots to the hyphal network of the fungi (Miller et al. 1995). Further, the fungal hyphae being much thinner than plant roots penetrate the smaller pores more efficiently (Allen 2011). Mycorrhizal fungi have been found to be one of the most abundant organisms of the rhizosphere and play a vital role in the terrestrial ecosystems as several plant species depend on them for the acquisition of mineral nutrients from the soil (Remy et al. 1994). They establish a physical link between plants and soil, provide the host plant with mineral nutrients and improve plant growth and productivity. In exchange, the heterotrophic AMF receive photosynthate from the host plant for the fungal growth, survival, and reproduction (asexual) (Smith and Read 1997, 2008; Goltapeh et al. 2008). Indeed, AMF protect their host from abiotic and biotic stresses (Evelin et al. 2009; Auge et al. 2014; Cameron et al. 2013; Schouteden et al. 2015; Nath et al. 2016), therefore becoming a growing choice as a biofertilizer and bioprotectant (Ijdo et al. 2011; Berruti et al. 2016).

Many studies have shown that AMF improve plant’s resistance that consequently reduce incidence as well as severity of plant diseases caused by a wide range of attackers including viruses, bacteria, nematodes and fungi. Although well-defined direct mechanisms are still unclear, several indirect mechanisms have been proposed by a number of researchers for increasing bioprotective ability of mycorrhizal plants. In the past decades, studied carried out to understand AMF-plant interactions in response to pathogen attack have proposed different mechanisms responsible for the increased tolerance to biotic stress in mycorrhizal plants (Cameron et al. 2013; Schouteden et al. 2015). The involvement of mycorrhizal fungi in the increased nutrient supply and altered rhizosphere microbial population, plant photosynthetic capacity, anatomy and architecture of the root system, root hydraulic conductivity, water use efficiency and antioxidants production seem to play a critical role in the AMF-mediated alleviation of biotic stresses. In this chapter, we have attempted to discuss the protective role of AMF towards different detrimental organisms belonging to fungi, bacteria, viruses and nematodes along with the possible mechanisms that may be employed in mycorrhizal plants with particular emphasis on the activation of defense mechanisms.

7.2 AMF Protection Against Plant Pathogens

Ample literature pertaining to the bioprotective role of AMF against various plant pathogens is available that has been reviewed time to time by various workers (Azcon-Aguilar and Barea 1996; Borowicz 2001; Akhtar and Siddiqui 2008; Veresoglou and Rillig 2012; Bagyaraj 2014; Pereira et al. 2016). Borowicz (2001) conducted a meta-analysis of data related to interactions between AM symbiosis and plant pathogens published between 1970 and early 1998, so that a general pattern, if possible, might be established. This analysis suggested the negative effect of AMF on the growth of pathogens and the nature of interaction between the two was influenced by the identity of the pathogen. AMF reduced pathogen growth in 50% of studies included in meta-analysis. AMF tended to decrease the harmful effects of fungal pathogens but to exacerbate the harmful effects of nematodes. Wherever, there was a negative effect on the growth of nematodes, the outcome depended upon mode of feeding of the nematode. AMF harmed sedentary endoparasitic nematodes but improved growth of migratory endoparasitic nematodes. In 16% of the total experiments included, both AMF and pathogens suffered reduced growth suggesting reciprocal suppression. Reciprocal suppression was more prominent when the pathogen was a fungus indicating that fungal pathogens in comparison to nematodes were more likely to compete with AMF. Another similar meta-analysis that included the wider data of period between 1978 and 2011 also provided unprecedentedly strong evidence of the ability of AMF to suppress plant pathogens. Additionally, the magnitude of the AM-induced decline in disease severity/nematode suppression ranged from 30 to 42% and 44–57% for fungal and nematode pathogens respectively, irrespective of pathogens’ identity or lifestyle suggesting that through AMF, plants possibly receive similar protection from all pathogens rendering AM formulations a potentially broadly effective biocontrol agent. Although there were no differences in AMF effectiveness with respect to the identity of the plant pathogen, the identity of the AMF isolate had a dramatic effect on the level of pathogen protection. AMF efficiency differences with respect to nematode pathogens were mainly limited to the number of AM isolates present; by contrast, modification of the ability to suppress fungal pathogens could occur even through changing the identity of the Glomeraceae isolate applied. N-fixing plants received more protection from fungal pathogens than non-N-fixing dicotyledons; this was attributed to the more intense AMF colonization in N-fixing plants (Veresoglou and Rillig 2012). Considering the bioprotective potential of AMF against pathogens variable results have been reported and the effectiveness of AMF varies with the identity of pathogen and host, and different abiotic factors. The effect of AMF has been studied against various biotic disease causing agents including fungi, bacteria, viruses and nematodes. Since, AMF colonize the roots of higher plants therefore assuming the localized bioprotection most of the studies undertaken are related to soil-borne pathogens and relatively few studies have been conducted on shoot affecting pathogens. On the basis of published reports, it seems that AMF reduce the incidence of disease occurrence in underground parts of plants but enhance the severity of disease in above ground parts in case of certain pathogens (Dehne 1982). AMF species from the family Glomeraceae are more effective at reducing pathogen abundance in contrast to species belonging to family Gigasporaceae (Maherali and Klironomos 2007; Sikes 2010). Further, for promotion and inhibition of plant growth and growth of pathogens, respectively, AMF are known to act synergistically with other microorganisms dwelling in the rhizosphere, which are often termed as plant growth-promoting microorganisms (PGPMs). Amongst PGPMs, plant growth-promoting rhizobacteria (PGPR) such as species belonging to genera, Pseudomonas, Paenibacillus, Rhizobium, Stenotrophomonas, Arthrobacter and Bacillus and fungi like Trichoderma sp., Gliocladium sp. and Aspergillus niger have been reported to help AMF in reducing the disease severity (Lioussanne 2010; Bharadwaj et al. 2012; Singh et al. 2013; Singh 2015; Prasad et al. 2017; Naglaa et al. 2016; Pereira et al. 2016; Sharma and Sharma 2016). On the basis of information available about mycorrhizal interactions with different pathogens, some of the general conclusions that can be drawn are: (1) AMF either alone or in combination with other microorganisms can reduce damage caused by different pathogens, soil-borne plant pathogens in particular, (2) the abilities of the AM symbioses to enhance resistance or tolerance in roots vary among different AMF tested, (3) the effectiveness of the protection varies from pathogen to pathogen, and (4) protection is influenced by soil and other environmental conditions (Pozo and Azcon-Aguilar 2007). Thus, it can be expected that these interactions will vary with the host plant and the culture system.

7.2.1 Protection Against Fungal Pathogens

The interactions between AMF and fungal plant pathogens have been studied most extensively and majority of these are related to fungal root pathogens (Whipps 2004). Consistent positive findings related to mycorrhizal plants and their root pathogens have been reported corroborating bioprotective effect of AMF against such pathogens; however, this consistency is missing against shoot pathogens and a lot of variability has been observed that varies with plant and pathogen involved (Ronsheim 2016). The majority of fungal pathogens that have been studied in relation to AMF belong to genera, Alternaria, Aphanomyces, Botrytis, Colletotrichum, Cylindrocladium, Erysiphe, Fusarium, Gaeumannomyces, Macrophomina, Oidium, Phytophthora, Pythium, Rhizoctonia, Sclerotium and Verticillium (Table 7.1).

Table 7.1 Effect of AMF on different pathogenic fungi in plants
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7.2.2 Protection Against Bacterial Pathogens

There are relatively very few studies where biocontrol effect of AMF has been reported against various bacterial pathogens and majority of these suggest protective role of AMF (Table 7.2). AMF identity appeared to be playing an important role in providing bioprotection against foliar pathogen, Pseudomonas syringae pv. glycinia on soybean. Amongst AMF, Entrophospora infrequens, Funneliformis mosseae, Claroideoglomus claroideum, and Racocetra fulgida, only E. infrequens reduced the colonization of pathogen in host plant (Malik et al. 2016).

Table 7.2 Effect of AMF against pathogenic bacteria in plants
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7.2.3 Protection Against Viral Pathogens

The impact of the AM symbiosis on infections caused by various viral pathogens is still largely uncertain and majority of studies conducted so far indicate negative impact where mycorrhizal colonization increases both multiplication of viruses and severity of the diseases (Dehne 1982; Miozzi et al. 2011), and AMF mediated protection against viral pathogens appeared to be a rare phenomenon (Maffei et al. 2014) (Table 7.3). Yellow mosaic virus infection in mycorrhizal mungbean had adverse effect on mycorrhizal colonization and reduced spore formation by AMF (Jayaram and Kumar 1995). Focusing on the disease symptoms, some of the viruses such as Tobacco mosaic virus (Jabaji-Hare and Stobbs 1984; Shaul et al. 1999), Potato virus Y (Sipahioglu et al. 2009), Citrus tristeza virus and Citrus leaf rurgose virus (Nemec and Myhre 1984), and Tomato spotted wilt virus (Miozzi et al. 2011) (TSWV) have been demonstrated to enhanced disease severity in the presence of mycorrhizal fungi (Table 7.3).

Table 7.3 Effect of AMF against plant viruses
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7.2.4 Protection Against Parasitic Nematodes

Nematodes are a diversified group of both free-living nematodes and parasitic nematodes of plants as well as animals that occur world over in various habitats. The plant-parasitic nematodes (PPN) are mostly root pests of a wide range of important agricultural crops and on the basis of feeding strategy, have been classified into different groups viz., ectoparasites, endoparasites, migratory endoparasites, and sedentary parasites (Perry and Moens 2011). Ectoparasitic nematode such as Xiphinema index remains in the rhizosphere during feeding and acquire food from the epidermal or outer cortical cells of the roots with the help of the stylet. Endoparasitic nematodes, in contrast, completely enter the root during feeding. Migratory endoparasitic nematodes (e.g., Radopholus spp. and Pratylenchus spp.) during feeding inside root migrate inter or intracellularly thus, causing damage to the plant along their migration path (Jones et al. 2013). Sedentary endoparasitic nematodes such as cyst and root-knot nematodes are considered to be the most damaging pests of agricultural crops worldwide (Jones et al. 2013; Bartlem et al. 2014) which become sedentary with the onset of feeding in the vascular cylinder (Gheysen and Mitchum 2011). This last group includes various species of genus Meloidogyne such as M. incognita and M. javanica which, are notorious for severe damages in tobacco, tomato, sunflower and pepper (Wesemael et al. 2011). The direct damage caused by PPN can be aggravated by secondary infections of the wounded plant tissues by other pathogens, moreover, some PPN, like the migratory ectoparasitic Xiphinema spp. can transmit plant viruses (Hao et al. 2012). Losses in crops yields caused by PPN are expected to rise due to climate change and cropping systems intensification (Nicol et al. 2011). Considering the limitations of currently used nematicides there is a need for alternative nematode management strategies; the use of AMF has been proposed as one of the environment-friendly strategies to manage PPN. PPN suppressive ability of AMF is well reported and has been previously reviewed (Pinochet et al. 1996; Hol and Cook 2005). In vitro, greenhouse as well as field experiments have indicated protective efficacy of AMF against PPN in crop plants like banana, coffee and tomato (Vos et al. 2013; Alban et al. 2013; Koffi et al. 2013). The bioprotective potential of AMF has been tested in different crop plants with highly variable results against various root-feeding nematodes belonging mainly to the genera Heterodera, Meloidogyne, Nacobbus, Pratylenchus, Radopholus, Rotylenchulus, Tylenchulus and Xiphinema (Table 7.4).

Table 7.4 Effect of AMF against different plant-parasitic nematodes
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7.3 Mechanisms of Mycorrhiza-Mediated Disease Control

Mycorrhizal symbiosis largely influences plant growth and development, and also plays a pivotal role in the biocontrol of plant diseases directly or indirectly (Singh et al. 2000; Azcon-Aguilar et al. 2002; Whipps 2004; Xavier and Boyetchko 2004; St-Arnaud and Vujanovic 2007). In addition to improved plant nutrition, several other mechanisms such as damage compensation, direct competition for colonization sites or photosynthate, alteration in the root morphology, changes in rhizosphere microbial populations, biochemical changes associated with plant defense mechanisms and the activation of plant defense mechanisms have also been found to be involved in AMF-induced biocontrol of plant pathogens (Whipps 2004; Jung et al. 2012) (Fig. 7.1).

Fig. 7.1
figure 1

An overview of the processes by which AMF can protect plants from pathogens. AMF facilitate host plant to acquire mineral nutrients (m) from soil and, in exchange, obtain carbon (c) from host plant. AM fungal hyphae enters plant root forming appressorium (ap) on the root surface and eventually vesicles (v) and arbuscules (a) in the root cortical cells by extending its hyphae. The fungus exerts a competition for photosynthate, infection sites and mineral nutrition with infectious organisms. AMF can control plant pathogens by increasing tolerance to pathogens, altering root morphology and rhizosphere interactions, and activating defense responses (ISR, MIR)

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7.3.1 Improved Nutrient Status

Although the soluble nutrients such as N and K can be accessed by nonmycorrhizal plants, the less soluble or immobile nutrients like P are more difficult to be attained by plants. This problem further exaggerates under nutrient deficient conditions. Indeed, the extensive thread-like extraradical hyphae of AMF act as an extension of the plant’s root system, extend several meters beyond the depletion zone, explore more soil volume and acquire both macro-and micro nutrients, therefore, improve nutrient status of their host plant. The nutritional aspect of plant-AMF interaction has been studied extensively from both physiological and molecular perspectives indicating that AMF considerably improve the acquisition of less soluble or immobile nutrients, mainly under stress conditions (Smith and Smith 2011). Nevertheless, mycorrhizal plants showed better survival and growth and increased resistance or tolerance to plant pathogens than that of the non-AMF plants, which could be ascribed to the increased nutrient status of mycorrhizal plants. However, it remains ambiguous whether the increased resistance against plant pathogens was a direct consequence of improved nutrient acquisition by mycorrhizal plants (Davis 1980; Declerck et al. 2002). Till the date, several reviews have been published advocating improved nutrients supply as one of the main mechanisms of AMF to control plant diseases (Azcon-Aguilar and Barea 1996; Xavier and Boyetchko 2004; Wehner et al. 2010; Schouteden et al. 2015), especially root-borne diseases (Bodker et al. 1998). On the other hand, there are a number of contradictory reports (Hooker et al. 1994; Linderman 1994). Davis (1980) provided an evidence of higher tolerance to citrus root rot disease induced by Thielaviopsis in AMF colonized than non-AMF citrus plants, conversely, non-AMF plants exhibited similar response to this pathogen when supplemented with additional dosage of phosphorus. Declerck et al. (2002) observed higher tolerance to Cylindrocladium spathiphylli in mycorrhizal as compared to non-mycorrhizal banana plants. The AMF isolates significantly improved growth and shoot P level of banana, and reduced root damage by C. spathiphylli, which may be correlated with the direct interaction between AMF and plant pathogen (Xavier and Boyetchko 2004). Caron et al. (1986) compared response between AMF and non-AMF tomato plants exposed to the Fusarium oxysporum Schlecht f. sp. radicis-lycopersici, a soil-borne pathogen, which can cause severe yield losses in tomato due to crown and root rot diseases. They observed a reduction in the Fusarium population and root rot incidences in the rhizosphere soil of AMF-colonized plants as compared to nonmycorrhizal control plants, and corroborated it with increased antagonistic activities in the mycorrhizosphere, an area influenced by AMF. They suggested that the disease suppression by AMF cannot be considered as a mere consequence of improved P nutrition; instead some other mechanisms may confer reduced disease incidences. A significant suppression in the symptoms of A. solani was observed in the mycorrhizal than non-mycorrhizal tomato plants by Fritz et al. (2006). Pettigrew et al. (2005) observed that plants with better nutrient status, growing in the cotton fields, which was infested with the sedentary semi-endoparasitic nematode Rotylenchulus reniformis were able to tolerate higher PPN population densities in their roots. Such findings indicate that the improved nutrition of the host plant could influence plant parasite nematode population densities either positively or negatively, however, no solid data are available to confirm a direct correlation between AMF-mediated increased nutrient status of host plant and the higher resistance against plant pathogens.

7.3.2 Changes in the Root System Morphology

The interaction between mycorrhizal fungi and host plant modulates the plant root system and influence microbial activities in the rhizosphere, especially plant-pathogen interaction (Atkinson et al. 1994; Scannerini et al. 2001; Hodge et al. 2009). Consequently, the total root length may increase or remain unchanged as has been reported in Vitis vinifera and Solanum lycopersicum respectively (Schellenbaum et al. 1991; Berta et al. 2005). The number and length of the roots vary according to the different AMF associations and in comparison to the main roots, modifications occur in the lateral roots more frequently. Pre-inoculation with mycorrhizal fungi increases formation of lateral branching as a result increasing suitable sites for root colonization, which confers to a high branched root system; however, changes in the root architecture as a consequence of AMF colonization could provide a fewer sites for pathogen infection (Norman et al. 1996; Fusconi et al. 1999; Harrison 2005). The strigolactones, a group of sesquiterpene lactones have also been found to play an important role in the modulation of shoot and root architecture. Together with auxins, strigolactones favor lateral root formation and facilitates the root to explore new areas in the soil. Strigolactones-induced changes in root architecture could alter the dynamics of some pathogen infections; however, further experimentation is required to establish this correlation (Jung et al. 2012).

Mukherjee and Ane (2011) observed that germinating fungal spores of Gigaspora margarita, G. rosea and Glomus intraradices could induce lateral roots formation and increase the total length of the root system in M. truncatula, indicating that diffusible signals released by mycorrhizal fungal spores trigger the lateral root developmental program. The important role of AM symbiosis in lateral root development has also been confirmed by Paszkowski and Boller (2002) and Olah et al. (2005). They revealed that branching in M. truncatula is directly induced by AMF germinating spores and their exudates. Increased root branching has also been recorded in the case of monocots and dicots (herbaceous and woody plants) with a significant difference in the order of the roots involved (Berta et al. 1995; Scannerini et al. 2001). However, the tap root plants appear to be more benefited than fibrous root plants in terms of the biomass production and acquirement of mineral nutrients (Yang et al. 2014). The increased root branching in AMF-colonized plants may directly be attributed to the production and action of AMF exudates; while the indirect reason of increasing root branching could be ascribed to the increased mineral nutrition and modulation of hormonal balance (Fusconi 2014). Vos et al. (2014) suggested that increased root branching in AMF-colonized plants could increase the implication for infection by a pathogen; however, a clear correlation did not establish (Vierheilig et al. 2008).

The higher nutrient uptake capacity of mycorrhizal plants attributes to the vigorous root growth, which indeed exhibits higher resistance to plant parasite infection. Elsen et al. (2003a) demonstrated that in banana, migratory endoparasitic nematodes-Radopholus similis and P. coffeae reduced root branching whereas, same increased by mycorrhizal fungus, Glomus mosseae. On the other hand, there is a probability that higher root branching negatively impacts host plant as it increases potential infection sites, depending on the parasite and host plant species. Primary roots are the preferential sites of colonization by migratory endoparasitic nematodes, like Radopholus similis, whereas the sedentary endoparasitic root-knot and cyst nematodes prefer to infect the root elongation zone and the sites of lateral root formation (Stoffelen et al. 2000; Wyss 2002; Elsen et al. 2003b; Curtis et al. 2009). Instead, the strawberry plant, bearing highly branched root system, is primarily infected through the root tips by the pathogenic fungus Phytophthora fragariae; however, the mycorrhizal roots of strawberry plants showed lower infection as compared to non-mycorrhizal roots, which was indeed higher in the case of highly-branched root system. By the way, it is difficult to explain a uniform impact of altered root morphology in the biocontrol of plant disease, therefore, substantiates the speculations of the involvement of other mechanisms in the mycorrhiza-induced biocontrol of plant diseases (Fusconi et al. 1999; Gamalero et al. 2010).

7.3.3 Changes in the Rhizosphere Interactions

Lorenz Hiltner (1904), a German agronomist and plant physiologist, who coined the term “rhizosphere” and described it as an area around the plant root, which is directly influenced by root secretions and associated population of soil microorganisms (Hiltner 1904). The plant root secretions/exudates comprising of sugars and organic acids (Hage-Ahmed et al. 2013), amino acids (Harrier and Watson 2004), phenolic compounds (McArthur and Knowles 1992), flavonoids (Steinkellner et al. 2007) and plant hormones such as strigolactones, Jasmonic acid, salicylic acid and ethylene (Lopez-Raez et al. 2010; Jung et al. 2012). These compounds play an important role in plant–microbe interactions in the rhizosphere. Some of them are crucial for the initial phase of plant-microbes interactions, while others are required at the later stages of interaction (Bais et al. 2006; Hage-Ahmed et al. 2013).

Alteration in the root exudation patterns directly impacts the microbial population in the mycorrhizosphere. Many studies suggested that AMF alter root exudates quality and quantity (Bansal and Mukerji 1994) and influence the rhizosphere microbial communities, which in turn reduce pathogen populations (Citernesi et al. 1996; Larsen et al. 2003). However, the quality and effectiveness of root exudation indeed depend on the plant and AMF species involved as well as on the degree of root colonization (Scheffknecht et al. 2006; Lioussanne et al. 2008; Badri and Vivanco 2009; Kobra et al. 2009). The findings of Pozo and Azcon-Aguilar (2007) demonstrate the degree of root colonization, which is typically characterized by the presence of arbuscules, as an important requirement for the control of plant pathogen. The root exudates collected from 4 months old AMF-colonized roots was attractive for the zoospores of Phytophthora nicotianae, whereas concentrated exudates obtained from 6 months old AMF colonized roots was repulsive for the zoospores of P. nicotianae, as compared to exudates harvested from nonmycorrhizal plant roots. This shows that a change in the root exudation pattern in mycorrhizal tomato plants negatively impacts the infection potential of zoospores of Phytophthora nicotianae, indicating an obvious involvement of root exudates in the plant-pathogen interactions (Lioussanne et al. 2008). Lioussanne et al. (2008) suggested that modification in the exudates composition of older roots due to AMF colonization could provoke the repulsion of P. nicotianae, and therefore reduce the degree of infection. Nevertheless, a differential pattern was also observed in the root exudates of mycorrhizal and non-mycorrhizal plants (Jones et al. 2004; Scheffknecht et al. 2006, 2007). Vos et al. (2013) investigated the influence of a mycorrhizal fungus, Glomus mosseae and mycorrhizal root exudates on the Meloidogyne incognita penetration of tomato roots. They found that exudates from mycorrhizal tomatoes generally minimize nematode penetration in mycorrhizal plants and transiently inhibited nematodes proliferation as compared to the root exudates obtained from nonmycorrhizal tomatoes. The study showed that nematode penetration of tomato roots decreases in mycorrhizal tomato roots. Moreover, mycorrhizal root exudates could partially affect the motility of nematode; therefore reduce the Meloidogyne incognita penetration and subsequent proliferation in tomato roots. The root exudates obtained from AMF-colonized plants root served as chemoattractants for plant-growth-promoting rhizobacteria, Azotobacter chroococcum and Pseudomonas fluorescens (Sood 2003). Siasou et al. (2009) found that rhizosphere fluorescent Pseudomonas strains produce increasing amounts of antibiotic 2,4-diacetylphloroglucinol in the presence of AMF, G. intraradices, which confers plant protection against Gaeumannomyces graminis var. tritici. This shows that mycorrhizal root exudates positively influence rhizosphere microbial communities and help in the biocontrol of plant pathogens. On the basis of results of many studies, it could be tempting to speculate that mycorrhizal fungi show a protective effect against infectious organisms, which is more obvious in the case of soil-borne diseases, in different plant systems.

7.3.4 Direct Competition with Other Microorganisms

The AMF-host relationship is fundamentally characterized by the development of arbuscules in root cortical cells (Dehne 1982), which die eventually due to their short lifespan. The AMF and pathogenic microbes most probably depend on common resources such as host photosynthate, nutrition, infection-site and space within the plant root for their survival and multiplication (Smith and Read 1997; Whipps 2004); hence competition can occur for these resources between pathogens and mycorrhizal fungi. Indeed, competition can be beneficial in the case of mycorrhiza-colonized cells for the physical exclusion of pathogens (Xavier and Boyetchko 2004). Graham (2001) observed that the competition between plant pathogens and AMF could arise if the availability of carbon is limited, which further corroborates the observations of Vos et al. (2014). The reduced locations for pathogen infection within AMF-colonized root system were also observed by Vigo et al. (2000), which make it plausible that AMF directly compete for colonization sites with other soil microorganisms (Vos et al. 2014). One of the well-studied examples in this connection is the study conducted by Cordier and colleagues on AMF, Glomus mosseae and pathogenic fungus, Phytophthora parasitica in tomato plants. The study showed that cortical cells of mycorrhizal root did not allow pathogen to penetrate roots that demonstrated to be a localized resistance response (Cordier et al. 1998). Mycorrhizal root system has shown complete exclusion of the Phytophthora parasitica from arbusculized cells in tomato roots (Cordier et al. 1996). Therefore, the competition occurring between AMF and pathogens for acquiring host photosynthate, root space or locations could be a potential strategy to control microbial infection in AMF-colonized plants; however, the potentiality of this mechanism to be used as a strategy for control of plant diseases has not received much attention as the results of various studies conducted are not consistent (Pozo et al. 1999; Vos 2012).

Since PPN also colonize plant root, therefore, the competition for space and infection loci appears to be involved in AMF-nematodes interactions. It becomes very difficult for migratory endo-parasitic nematodes to survive in the presence of mycorrhizal arbuscules, which largely develop in the root cortical cells, where these nematodes feeds upon (Jung et al. 2012; Schouteden et al. 2015). Moreover, the competition for the space between AMF and sedentary endo-parasitic nematodes becomes important if feeding cells extend into the host cortical cells. However, cyst nematodes are meagerly affected by AMF colonization as these nematodes are restricted to the endodermal cells only (Schouteden et al. 2015). Indeed, the formation of mycorrhizal fungi may also be affected by PPN infection as the competition for the nutrients and space arises between them as substantiated by Hol and Cook (2005) who reported reduced AMF colonization due to the attack of migratory and sedentary endoparasitic and ectoparasitic nematodes. Elsen et al. (2003b) observed that mycorrhizal inoculation of Musa with Glomus mosseae gives rise to a significantly higher plant growth even in the presence of nematodes under greenhouse conditions. Although nematodes decreased the root branching, the population densities of them drastically decreased in the presence of Glomus mosseae, and a decrease in root branching seems to be compensated by the AMF inoculation. A negative effect of burrowing nematode Radopholus similis and Pratylenchus coffeae infection was observed on the frequency of Glomus mosseae colonized Musa roots (Elsen et al. 2003a, b); however, such effect did not observe in the case of the intensity. In an in vitro experiment, carried out by Elsen et al. (2003c), the interaction between AMF and P. coffeae on transformed carrot roots in root organ culture did not influence the root colonization by mycorrhizal fungus Glomus intraradices (Elsen et al. 2003c), which substantiate the findings of recent study on in vitro mycorrhizal banana plantlets and R. similis (Koffi et al. 2013). Dos Anjos et al. (2010) observed that the establishment of mycorrhiza prior to the nematode infection could reduce both severity symptoms and reproduction of Meloidogyne incognita. Based on the findings, Alban et al. (2013) concluded that pre-inoculation of coffee plants with AMF could develop stronger and healthier plants, which resist Meloidogyne exigua infestation and subsequently reduce the rate of infestation. Lower nematode infestation in AMF colonized plants could be attributed to the lignifications of the plant cell wall cuticle, which is not easy to penetrate by nematodes to enter into plant roots. They highlighted that as compared to nematodes, AMF colonize plant root faster, giving them an advantage in their development inside the root, for that reason occupying more root space and eventually lower the nematode infestation rates.

7.4 The Activation of Defense Mechanisms in Response to AMF Formation

For the biological control of plant diseases, it is expected that arbuscular mycorrhizal fungi could apply more than one mechanism to restrain the adverse effects of the causal organisms. As above mentioned mechanisms do not elucidate satisfactorily the mycorrhiza-induced biocontrol of certain plant diseases, therefore, researchers have explored possibilities of other mechanism like the activation of plant defense compounds in response to AMF formation in plant roots. It has been observed that, in response to mycorrhizal colonization, though a weak or very local and transient, activation of specific plant defense compounds takes place which, elicits the specific defense reactions and makes the plants proactive against attackers/pathogens (Gianinazzi-Pearson et al. 1994; Koide and Schreiner 1992). The chemicals produced under plant defense mechanism are diversified groups of biochemicals which are synthesized mostly as secondary metabolites (Singh 2017). Some of such chemicals like, phytoalexins, chitinases, β-1,3-glucanases, pathogenesis-related proteins, callose, hydroxyproline-rich glycoproteins, phenolic compounds and enzymes of the phenylpropanoid pathway have been reported to be involved in the activation of plant defense as a result of AMF colonization (Gianinazzi-Pearson et al. 1994; Azcon-Aguilar and Barea 1996).

In the past decades, the changing host plant physiology (including plant nutrition) as a consequence of plant-AMF interactions and the plant signal transduction pathways controlling this intimate association have largely been the central point of research. Conversely, a little attention has been paid to understand the contribution of AMF for non-nutritional benefits, such as suppression of plant diseases or induction of plant resistance against plant diseases/attackers. It is well established that plant roots exude different chemical compounds (secondary metabolites), which usually signaling an array of soil microorganisms, predominantly occurring in the rhizosphere. The pioneer observations of Akiyama et al. (2005) and successive publications have established that strigolactones, a group of carotenoids-derived signaling molecules that are released by the host plant root promote AMF-hyphal branching and facilitate AMF establishment in the plant root. The production of strigolactones generally increases in the early phase of root colonization but, it decreases in a well-established mycorrhizal symbiosis (Jung et al. 2012). The root exudates released by AMF-colonized plants seems to prime microbial activities in the rhizosphere and thereby induce a ‘mycorrhizosphere effect’ (Linderman 1988; Giri et al. 2005).

Like certain other soil microbes, mycorrhizal fungi also exhibit the ability to reduce the impacts of plant pathogens through induced systemic resistance (Pozo and Azcon-Aguilar 2007). The induced systemic resistance (ISR) is typically a sustained induction of resistance in plants against pathogens, which is induced by the non-pathogenic rhizosphere microorganisms such as PGPR, mycorrhizal fungi or endophytes (Trotta et al. 1996; Cordier et al. 1998; Pineda et al. 2010). ISR protect plants from the infection of different plant pathogens including bacteria, fungi, viruses, nematodes and insects and is mediated by the priming of defense genes that demonstrate a higher expression systemically in the leaves only after the pathogen attack (van Wees et al. 2008; Pineda et al. 2010). ISR often exhibits increased plant-sensitivity towards the plant growth regulators such as jasmonic acid (JA) and ethylene (ET) (Pineda et al. 2010).

In the AMF-colonized plants, both localized and induced systemic resistance has been observed against detrimental organisms. Cordier et al. (1998), in split root experiment observed the protective role of AMF, Glomus mosseae against Phytophthora parasitica as it hindered the development and proliferation of causal organisms in tomato roots. They suggested that root cortical cells become immunized on AMF colonization resulting in a localized plant cell resistance, likely due to the formation of cell wall appositions supported by callose (adjacent to intercellular hyphae) and phenolic compounds, and plant cell defense responses. Induced systemic resistance in nonmycorrhizal root parts of the mycorrhizal plants could attribute to the host wall-thickenings containing non-esterified pectins and pathogenesis-related (PR)-1a protein and formation of callose rich jacket around the hyphae of P. parasitica (Cordier et al. 1998). Liu et al. (1995) found more than ten types of pathogenesis-related (PR) proteins in cotton plants, moreover, the content of PR proteins increased on AMF inoculation. The growth of hyphae and conidia of Verticillium dahlia were found to be hampered at certain concentrations in mycorrhizal plants, which subsequently helped in the reduction of disease incidences and index of verticillium wilt and in the promotion of seedling growth and yield of cotton seed. Indeed, the higher MIR response against V. dahlia could be an effect of the increased content of PR proteins in cotton plants on mycorrhization.

Mycorrhiza-induced resistance (MIR) against many plant pathogens has been demonstrated by researchers that seems to be based more on the priming of jasmonic acid-dependent defense (JADD) responses (Pozo and Azcon-Aguilar 2007) than accumulation of salicylic acid (Khaosaad et al. 2007) as there are reports suggesting negative impact of salicylic acid on mycorrhizal colonization (Hause et al. 2007; Jung et al. 2012; Miransari and Smith 2014). Priming can be explained as a pre-conditioning of plant tissues that allows the plant to activate defense responses faster and stronger against a broad range of plant pathogens/attackers. Such a pre-conditioning can be elicited by certain chemical compounds and different microorganisms (Pineda et al. 2010). Priming seems to be a plausible mechanism operating in MIR. The MIR-regulated bioprotection of crop plants has been reported in the case of Gaeumannomyces graminis var. tritici, which causes Take-all disease in barley (Khaosaad et al. 2007). Aberra et al. (1998) also observed similar results in the case of a sterile red fungus, which suppressed the infection of wheat roots by Gaeumannomyces graminis var. tritici. Benhamou et al. (1994) observed strong defense reactions at the sites challenged by Fusarium oxysporum f. sp. chrysanthemi in mycorrhizal transformed carrot roots. The protective ability of mycorrhizal fungi in grapevine roots against Meloidogyne incognita, has been found to be associated with primed expression of a chitinase gene (VCH3) (Li et al. 2006). Moreover, mycorrhiza-induced resistance against Fusarium oxysporum in mycorrhizal date palm trees and Colletotrichum in cucumber seem to be associated with the primed-accumulation of the phenolic compounds (Jaiti et al. 2008), and callose deposition (Lee et al. 2005), respectively.

Fritz et al. (2006) conducted an experiment to understand the influence of mycorrhizal fungi on the development of early blight in tomato, caused by a necrotrophic fungus, Alternaria solani. The mycorrhizal tomato plants showed a significant reduction in disease symptoms as compared to the non-mycorrhizal plants. Although the increased nutrient supply considerably influenced disease severity in mycorrhizal than non-mycorrhizal plants, the defensive role of AMF against causal organisms could be due to mycorrhiza-induced resistance. Recently, Cameron et al. (2013) presented a four-phase spatiotemporal model demonstrating MIR as a cumulative outcome of direct interactions between mycorrhizal fungi and plant, and responses to ISR-eliciting rhizobacteria present in the mycorrhizosphere. They highlighted that at the early stage of colonization, strigolactones present in the exudates of host plant roots, promote hyphal branching and AMF establishment. At the onset of mycorrhizal symbiosis, microbe-associated molecular patterns (MAMPs) from the fungus are recognized by the plant’s innate immune system that leads to a weak and transient MAMP-triggered immunity (MTI) response as well as the activation of long-distance signals in the xylem, which could prime the salicylic acid-dependent defense (SADD) responses. The AMF-regulated induction of the specific effector molecules suppresses MTI locally. Mycorrhizal symbiosis elicits the production of abscisic acid that systemically transports to the shoot tissues through xylem and can prime cell wall defense responses. With the development of arbuscules in the root cortical cells, the increased supply of sugar and mineral nutrition, particularly phosphorus modulates root metabolisms and thereby the chemical composition of root exudates. Such modifications in the root exudates chemical composition indeed influence mycorrhizosphere populations, which could allow the selection of growth-promoting rhizosphere microbes/bacteria that metabolize AMF root exudates and convey ISR-eliciting signals at the root surface and/or AMF hyphae, resulting in the long-distance signals, which could credit the priming of JA-dependent defense and ET-dependent defense responses and eventually triggers the ISR in mycorrhizal plants (Cameron et al. 2013). Although the well-defined roles of jasmonic acid in MIR against detrimental organisms are not well known, Pozo and Azcon-Aguilar (2007) proposed that the active suppression of components involved in the SA-dependent defense pathway could lead to the induction of MIR and the priming of JA-dependent defense responses (Pozo and Azcon-Aguilar 2007; Hause et al. 2007). Although salicylic acid has been proved to be a key regulator of plant defense against biotrophs (Glazebrook 2005), it could have negative impact on AMF formation in the host roots (García-Garrido and Ocampo 2002; Lopez-Raez et al. 2010). Therefore, it is possible that AMF suppress certain components of SA-dependent responses in the host plant in order to accomplish a compatible interaction. Dumas-Gaudot et al. (2000) also observed a delay in the accumulation of PR-1 proteins (common markers of SA-dependent responses) in mycorrhizal roots. Nevertheless, the beneficial microbes (PGPR)-induced systemic resistance, regulated by JA-dependent and ethylene-dependent signaling pathways, and associated with priming for enhanced defense against plant pathogens has been observed by van Wees et al. (2008). These findings tempting to consider that the JA is a key regulator in the AMF symbiosis (Hause et al. 2007; Hause and Schaarschmidt 2009). The higher levels of JA have been confirmed in mycorrhizal tomato roots (Lopez-Raez et al. 2010), which remains unchanged in the shoots (Pozo et al. 2010). Pozo et al. (2010) recorded rather low, but a significant increase in the expression of marker genes for JA responses and a strong induction of JA-regulated genes in Glomus mosseae-colonized tomato plants. Confirming a priming response in tomato plant they further validated the MIR response against Botrytis cinerea directly related to the priming of JA-dependent defense responses.

7.5 Conclusions and Outlook

Arbuscular mycorrhizal fungi have been found to protect several plant species against many pathogens including viruses, phytoplasmas, bacteria, fungi, and plant-parasite nematodes. The suppression of both necrotrophic and biotrophic pathogens and consequently reduction in the severity of disease symptoms either directly or indirectly has also been observed in majority of AMF-colonized plants. However, soil-borne root attackers appear to be affected more than shoot attackers. One of the reasons of such a generalization is availability of relatively few reports pertaining to air-borne pathogens. The protective action mechanism of AMF is not fully understood and based on the investigations done so far appears to be multi-targeted. The primary protection mechanism is increased resistance of crop plants as a result of AMF-mediated improved nutrient status. However, studies indicate the involvement of other mechanisms such as changes in the chemical composition of root exudates, modulation of rhizosphere microbial activities and the activation of plant defense responses in mycorrhiza-induced protection against different attackers. Indeed, the actual use of AMF as a bio-control agent remains to be popularized for agricultural practices.