Nath, d and meena, v s 2018 mycorrhizae a potential microorganism and its implication in agriculture

Chapter 10

Mycorrhizae: A Potential Microorganism and Its Implication in Agriculture Debabrata Nath and Vijay Singh Meena

Abstract Mycorrhiza is a symbiotic mutualistic relationship between special soil fungi and fine plant root system. Mycorrhizal fungi are a heterogeneous group of diverse fungal taxa, associated with the roots of over 90% of all plant species. They play a crucial role in plant nutrient uptake, water relations, ecosystem establishment, plant diversity and the productivity of plants. Scientific research involves multidisciplinary approaches to understand the adaptation of mycorrhizae to the rhizosphere, mechanism of root colonization, effect on plant physiology and growth, biofertilization, plant resistance and biocontrol of plant pathogens, reclamation of heavy metals and contribution in soil aggregation. Mycorrhizae are an essential belowground component in the establishment and sustainability of plant communities, but thorough knowledge is required to achieve maximum benefits from these microorganisms and their associations.

Keywords Mycorrhiza · Glomalin · Ectomycorrhiza · Endomycorrhiza

10.1 Introduction Mycorrhizal fungi have existed since the first plants appeared on dry land more than 450 million years ago. They form a close symbiotic relationship with plant roots.

They are called mycorrhizae from the Greek “mycos”, meaning fungus, and “rhiza”, meaning roots. The word mycorrhiza was first used by German researcher A.B. Frank in 1885. Mycorrhiza is a symbiotic mutualistic relationship between D. Nath (*) Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, India ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India V. S. Meena ICAR-Vivekananda Institute of Hill Agriculture, Almora, Uttarakhand, India Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India © Springer Nature Singapore Pte Ltd. 2018 V. S. Meena (ed.), Role of Rhizospheric Microbes in Soil, https://doi.org/10.1007/978-981-10-8402-7_10

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special soil fungi and fine plant roots; it is neither the fungus nor the root but rather the structure formed from these two partners. Since the association is mutualistic, both organisms benefit from the association (Meena et al. 2013a, 2016a; Bahadur et al. 2014; Maurya et al. 2014; Jat et al. 2015; Kumar et al. 2015, 2016b; Ahmad et al. 2016; Parewa et al. 2014; Prakash and Verma 2016). The fungus receives carbohydrates (sugars) and growth factors from the plant, which in turn receives many benefits, including increased nutrient absorption. In this association, the fungus takes over the role of the plant’s root hairs and acts as an extension of the root system (Muchovej 2001).

Mycorrhizae form a network of filaments that associate with plant roots and draw nutrients from the soil that the root system would not be able to access otherwise. This fungus-plant alliance stimulates plant growth and accelerates root development. It also makes the plant less susceptible to soil-borne pathogens and to other environmental stresses such as drought and salinity. In return the plant provides carbohydrates and other nutrients to the fungi. They utilize these carbohydrates for their growth and to synthesize and excrete molecules like glomalin (glycoprotein).

The release of glomalin in the soil environment results in better soil structure and higher organic matter content (Rillig 2004). However, in soil that has been disturbed by human activity, the quantity of mycorrhizae decreases drastically so that there are not enough of them to produce a significant benefit on plant growth and soil health (Meena et al. 2015a, 2016b; Priyadharsini and Muthukumar 2016; Kumar et al. 2016a, 2017; Raghavendra et al. 2016; Zahedi 2016).

10.2 Mycorrhizal Types There are two major groups of mycorrhizal fungi: ectomycorrhizal and endomycorrhizal fungi. Members of the former group develop exclusively on the exterior of root cells, whereas those of the latter penetrate the plant cells where direct metabolic exchanges can occur. Ectomycorrhizae are essentially found on trees and form visible structures, whereas endomycorrhizal fungi colonize trees as well as shrubs and most herbaceous plants and do not form visible structures.

10.2.1 Ectomycorrhizae Ectomycorrhizal fungi are also found in natural environments, mainly in forest ecosystems. These fungi can form visible reproductive structures (mushrooms) at the feet of trees they colonize. Ectomycorrhizal fungi grow between root cells without penetrating them. Their hyphae grow externally, forming dense growth known as a fungal mantle. These fungi form symbiotic relationships with most pines, spruces and some hardwood trees including beech, birch, oak and willow.

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10.2.2 Endomycorrhizae Among the types of endomycorrhizal fungi, arbuscular mycorrhizal (AM) fungi are the most prevalent in soils. Their name is derived from structures they form within the plant root cell arbuscules. Arbuscules are finely branched structures that form within a cell and serve as a major metabolic exchange site between the plant and the fungus. Vesicles are found in some species of AM fungi; they are saclike structures, emerging from hyphae, which serve as a storage organ for lipids. Endomycorrhizae are further divided into orchid, ericoid and arbuscular mycorrhizae (AMs).

10.3 Mechanism of Symbiosis Trees in the families Pinaceae, Fagaceae, Dipterocarpaceae and Caesalpinoidaceae found in many forests all interact with hundreds of ectomycorrhizal species of Basidiomycetes and Ascomycetes, so that these fungi can be said to have shaped the present forests. The ectomycorrhizal fungi colonize the lateral roots of these trees with sheathing mycorrhizae, in which a fungal mantle covers the root tip, and a socalled Hartig net of intercellular hyphae surrounds the epidermal and outer cortical cells (Figs. 10.1 and 10.2).

The ectomycorrhizal fungus surrounds the root tip with a thick mantle of closely appressed hyphae, whereas the Hartig net develops around the epidermal cells

Ectomycorrhizae

Endomycorrhizae chlamydospore

xylem epidermis cortex Hartig net

epidermis arbuscule endodermis vesicle

root hair fungal sheath

100 µm cortex

Fig. 10.1 Schematic diagram on ecto- and endomycorrhizae

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Arbuscular mycorrhiza

* Hyphopodium Mycellium

Mantle #

Arbuscule

Hartig net

Fig. 10.2 Illustration of root colonization structures in ectomycorrhizal (blue) and arbuscular mycorrhizal (pink) interactions

(green). In the case of arbuscular mycorrhizae, the root tip is usually not colonized.

Hyphae develop from a spore and produce a hyphopodium on the root epidermis.

Intraradical colonization proceeds both intra- and intercellularly and culminates with the formation of arbuscules, little fungal trees, inside inner cortical cells (brown).

Arbuscule Highly branched structure produced by arbuscular mycorrhizal fungi inside the cell lumen of their host. Arbuscules are considered to be the key element of the symbiotic nutrient exchanges between the plant and the fungus.

Hyphopodium Specialized hypha of an arbuscular mycorrhizal fungus, often branched and swollen, which adheres to the root epidermis before intracellular fungal penetration (Fig. 10.3).

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Fig. 10.3 The transition from the free-living status of an EM fungus to the symbiotic phase.

(Adapted from Bonfante and Genre 2010)

A growing hypha from the mycelium of T. melanosporum as observed in fluorescence microscopy is shown in (a) (Courtesy: R. Balestrini). Hyphal morphology changes in the mantle, in which the repeated branching, characterized by incomplete transversal walls (arrowheads), originates a pseudoparenchymatous structure, are evident in the electron micrograph shown in (b). In both images, the fungal wall is falsely coloured in blue and nuclei in red. The transverse section of a mycorrhizal root tip stained with Trypan blue is presented in (c), showing the organization of hyphae in the mycelium, mantle and Hartig net.

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Fig. 10.4 Scheme summarizing the main nutrient exchange processes in EM and AM symbiosis

10.4 Nutrient and Signal Exchange in Ectomycorrhiza Mycorrhizal fungi, similar to other plant-interacting fungi, base their life cycle on the uptake of organic carbon from a living plant (Fig. 10.4).

Emphasis is placed on the translocation of phosphorus (P), nitrogen (N) and carbon (C) at the soil-fungus and fungus-plant interface. Inorganic P and mineral or organic forms of N, such as NH4+, NO3− and amino acids (AA), are taken up by specialized transporters located on the fungal membrane in the extraradical mycelium. NH3/NH4+ and Pi (the latter originated in AM fungi from the hydrolysis of polyphosphate) are imported from the symbiotic interface to the plant cells through selective transporters. Hexose transporters import plant-derived carbon to the fungus, whereas transporter proteins involved in the export of nutrients from either the plant or fungus have not been identified yet (Meena et al. 2015b, f, 2016c; Rawat et al. 2016; Yasin et al. 2016; Saha et al. 2016a; Yadav and Sidhu 2016; Dotaniya et al. 2016; Jaiswal et al. 2016; Jha and Subramanian 2016).

10.5 Finding the Host Root The dissection of plant responses illustrates how the mechanisms operating to accommodate the AM fungus inside the plant cell lumen are shared by diverse plants and have been conserved during evolution (Fig. 10.5); root colonization is vital to AM fungi.

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Fig. 10.5 Schematic summary of the root colonization process by AM fungi under soil-plant system

The germination of a resting spore is followed by the production of a short explorative mycelium. The perception of plant exudates, released by the host root, induces recursive hyphal branching, increasing the probability of a direct contact between the symbionts. In the meantime, fungal exudates are perceived by the root, where they trigger calcium spiking. Signal transduction leads to the activation of cellular and transcriptional responses (green cells and nuclei). The contact between the plant and fungus is followed by the adhesion of a hyphopodium to the root surface (Meena et al. 2014a, 2015e, 2016d; Saha et al. 2016b; Verma et al. 2014, 2015b; Sharma et al. 2016; Bahadur et al. 2016b; Das and Pradhan 2016; Dominguez-­ Nunez et al. 2016). This triggers the assembly of a broad aggregation of cytoplasm (yellow), named the prepenetration apparatus (PPA), in the contacted epidermal cell and underlying outer cortical cell. Subsequent intracellular fungal colonization strictly follows the route of PPAs from the epidermis to the inner cortex. Here, intercellular hyphae can develop along the root axis. The PPA mechanism is then replicated in the contacted inner cortical cells, both before fungal entry and—on a smaller scale—branching. Eventually, a highly branched arbuscule occupies most of the cell volume, forming an extensive surface for nutrient exchange (Verma et al.

2015a; Meena et al. 2013b, 2015c; Shrivastava et al. 2016; Velazquez et al. 2016; Teotia et al. 2016).

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10.6 Beneficial Effects of AM Beneficial effects of AM result from one or several of these mechanisms: (i) Increased overall absorption capacity of roots due to morphological and physiological changes in the plant. There is increased absorption surface area, greater soil area explored (since the fungus acts as an extension of the root), greater longevity of absorbing roots, better utilization of low-availability nutrients and better retention/storage of soluble nutrients, thus reducing reaction with soil colloids or leaching losses (Fig. 10.6). (ii) Increased mobilization and transfer of nutrients (P, N, S, micronutrients Cu and Zn) from the soil to the plant. Mycorrhizal fungi have been estimated to “substitute” up to 500 lb/a of P for citrus and 170 lb/a for soybeans in tropical areas. (iii) AM aids plant in foraging for unevenly distributed nutrients by increasing the soil volume that is explored for P and also facilitating mineral weathering of apatite. (iv) Arbuscular mycorrhizal fungi can be a useful tool of integrated weed management (Li et al. 2016). (v) Modification of plant-pathogen relations: Mycorrhizae influence the colonization of roots by other microorganisms and reduce the susceptibility (or increase the tolerance) of roots to soil-borne pathogens such as nematodes or phytopathogenic fungi such as Fusarium oxysporum and F. solani. Development of

Fig. 10.6 Schematic view of possible interactions among different components of the mycorrhizosphere. (Adapted from Johansson et al. 2004)

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basal stem rot (BSR) disease in oil palm (Elaeis guineensis) caused by Ganoderma boninense is reduced by combination effect of arbuscular mycorrhizal fungi (AMF) with with endophytic bacteria (EB) (Sundram et al. 2015). (vi) Effects of AM fungi on fungal pathogens: AM fungi may also interact with other root-associated microorganisms, such as pathogenic fungi. In a study by Filion et al. (1999), the differential effects in vitro of a crude extract from the growth medium of the AM fungus Glomus intraradices on the sporulation of two pathogenic fungi and on the growth of two bacterial species were investigated. Conidial germination of the mycoparasitic fungus T. harzianum and the growth of P. chlororaphis were stimulated, whereas conidial germination of the plant root pathogen F. oxysporum was reduced, and the growth of Clavibacter michiganensis was unaffected. The measured effects were correlated with extract concentration, and no significant influence of pH on growth or germination was detected (Filion et al.

1999; Sindhu et al. 2016; Meena et al. 2014b, 2015d, 2016e; Singh et al. 2016).

The authors concluded that the release of unspecified substances by the AM fungus into the growth medium was the main factor explaining the differential growth of the tested microorganisms. In field experiments, Newsham et al. (1995) found Glomus sp. inoculated and uninoculated seedlings of the annual grass Vulpia ciliata into a natural population and that AM inoculation did not affect P concentrations in the plants. However, mycorrhiza protected the plants from the deleterious effects of F. oxysporum infection on shoot and root growth.

Apparently, the AM suppressed pathogen development in the roots. Following transplantation, comparison of root-infecting mycofloras of AM and non-AM plants revealed that AM plants had fewer naturally occurring infections of F. oxysporum and Embellisia chlamydospora. It was proposed that the main benefit supplied by AM fungi to V. ciliata is the protection from pathogenic fungi, rather than improved P uptake (Filion et al. 1999; Meena et al. 2017) and increased production of plant growth hormones such as cytokinins and gibberellins; (vii) Modification of soil-plant-water relations, promoting better adaptation of plant to adverse environment conditions (drought, metals). At elevated heavy metal concentrations in soils, mycorrhizal fungi have been shown to detoxify the environment for plant growth. (viii) Arbuscular mycorrhizal fungi responded to differences in host community and resource availability, suggesting that mycorrhizal functions, such as carbon sequestration and soil stability, will be affected by global change (Antoninka et al. 2011; Singh et al. 2015; Meena et al. 2013c; Bahadur et al.

2016a; Masood and Bano 2016). (ix) Arbuscular mycorrhizae enhance plant interception of leached nutrients (Asghari and Cavagnaro 2011). (x) Effects of AM fungi on plant and soil function and interaction: An increase in water-soluble aggregates in mycorrhizal soybean (Glycine max), which were dependent on the mycorrhizal fungal species, was found. Differences in the bacterial communities were also found among the fungal species, suggesting that AM species may influence both water-soluble aggregates and bacterial composition (Schreiner et al. 1997).

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Ectomycorrhizal inoculum is easily produced for application in forest nurseries, but the necessity of AM inoculum production via a host plant is still an obstacle to ample utilization of AM fungi in agricultural crops. Nevertheless, progress is being made in this area, and some commercial inoculum is currently marketed. Some of the important practical applications of mycorrhizae are (a) in soil that are constantly fumigated or receiving high rates of fungicides to eliminate/reduce soil-borne pathogens (importance of mycorrhizae for agricultural crops such as in horticultural crops and fruits), (b) in revegetation of eroded or mined areas (extreme pH, metal toxicity, low organic matter content, natural AM inoculum and overall fertility) and (c) in arid and semi-arid regions. With increasing concerns about excessive nutrient application to the environment, the use of mycorrhizal symbioses to promote plant growth while reducing the inputs of fertilizer and pesticides may have great potential for citrus and vegetable crops, which respond very well to inoculation (Mukhovej 2001) (Fig. 10.7).

Mycorrhizae are the rule in nature, not the exception. Most plants (more than 90% of all known species) present at least one type of mycorrhiza. Among the

Fig. 10.7  An overview of mycorrhizal root and non-mycorrhizal root function

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Fig. 10.8 The boxes represent the four phases of formation of the plant-fungus association in the AM symbiosis; (a) plant roots exude strigolactones and induce hyphal branching; (b) the AM fungus contacts the root surface and forms hyphopodia; (c) epidermal plant cells produce a prepenetration apparatus; the AM fungus starts to grow inside the plant and reaches the cortex; (d) the AM fungal hypha branches inside the cortex cells and forms the arbuscules. (Adapted from Marco et al. 2015)

important plants that associate with mycorrhizal fungi are corn, carrots, leek, potatoes, beans, soybeans, other legumes, tomatoes, peppers, onions, garlic, sunflower, strawberries, citrus, apples, peaches, grapes, cotton, coffee, tea, cocoa, sugarcane, forest species, wild plants and even weeds. Cabbage, Cruciferae in general, and some aquatic plants are usually non-mycorrhizal (Mukhovej 2001) (Fig. 10.8).

10.6.1 Effects of Mycorrhizosphere Bacteria on AM Fungi Mycorrhizosphere bacteria may affect AM fungi and their plant hosts through a variety of mechanisms (Fig. 10.6). Some of these have been more fully studied in ectomycorrhizal fungi by Garbaye (1994), but possibilities include (i) effects on the receptivity of the root, (ii) effects on the root-fungus recognition, (iii) effects on the fungal growth, (iv) modification of the chemistry of the rhizospheric soil and (v) effects on the germination of the fungal propagules.

The germination was also enhanced following addition of kaolin or activated charcoal, indicating that the spores contained self-inhibitors, which were possibly inactivated by soil bacteria or were immobilized by substances with a high ion

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exchange capacity. Carpenter-Boggs et al. (1995) tested the stimulatory effects of actinomycetes and Streptomyces orientalis on Gigaspora margarita spore germination and found that amounts of volatile compounds produced by the isolates correlated well with AM spore germination. Conversely, other studies using pasteurization, fumigation or sterilization of soils have demonstrated that the presence of some soil bacteria may also inhibit spore germination (Tommerup 1985; Ross 1980; and Wilson et al. 1988).

10.6.2 Arbuscular Mycorrhizal Fungi Act As a Biocontrol Microbial inoculants can be used as an alternative means for controlling pests and disease in agricultural cropping systems, permitting the reduced use of pesticides that could otherwise pose threats to human health and nontargeted organisms. The biocontrol organisms may affect AM fungi, or be affected themselves by AM fungi, in similar ways to the interactions already described above. Biocontrol agents against pathogenic fungi may in particular have negative effects on “nontarget” AM fungi. The mechanisms of antagonistic interactions resulting in biocontrol may involve competition for colonization sites or nutrients and production of fungistatic compounds. Although the literature concerning biocontrol is extensive, few studies have explicitly considered interactions involving AM fungi. The main conclusions that can be drawn are as follows: (1) AM associations can reduce damage caused by soil-borne plant pathogens, (2) the abilities of the AM symbioses to enhance resistance or tolerance in roots are not equal for the different AM fungi so far tested, (3) protection is not effective for all pathogens, and (4) protection is modulated by soil and other environmental conditions. Some positive effects of rhizobacteria on AM fungal colonization of roots may be due to antagonistic effects of competing pathogens (Azcon et al. 1996) but also direct synergistic effects on mycorrhizal colonization itself (Budi et al. 1999); however AM-induced suppression of root pathogens and stimulation of plant growth-promoting microorganisms may also be important (Kapoor and Mukerji 1998).

10.6.2.1 M echanisms by Which an AM Association Could Control Root Pathogens (i) Improved nutrient status of the host plant: Increased nutrient uptake made possible by the AM symbiosis results in more vigorous plant, and the plant itself may thus be more resistant and tolerant to pathogen attack. It has been suggested that AM fungi increase host tolerance of pathogen attack by compensating for the loss of root biomass or function caused by pathogens (Linderman 1994).

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(ii) Competition for host photosynthates: It has been proposed that the growth of both the AM fungi and root pathogens depends on host photosynthates and that they compete for the carbon compounds reaching the root (Smith 1987; Linderman 1994). When AM fungi have primary access to photosynthates, the higher carbon demand may inhibit pathogen growth. (iii) Anatomical and morphological changes in the root system: It has been demonstrated that AM colonization induces remarkable changes in root system morphology, as well as in the meristematic and nuclear activities of root cells (Atkinson et al. 1994). (iv) Activation of plant defence mechanisms: The activation of specific plant defence mechanisms as a response to AM colonization is an obvious basis for the protective capacity of AM fungi (Gianinazzi-Pearson et al. 1994).

Endotrophic mycorrhizal fungus Glomus fasciculatus causes an increase in Luffa cylindrica L. plant resistance to nematode infection and development. Inoculation of plants with fungus before nematode infestation seemed necessary to allow the fungal symbiont to become established and colonize extensively the cortical cells of Luffa transplant and seedling (Nangyal et al. 2016).

10.6.3 C ontribution of Mycorrhiza in Glomalin Production, Soil Aggregation and Soil Quality The formation of a biomolecule such as glomalin would have served as an evolutionary advantage to the fungus. Glomalin is a glycoprotein produced on the hyphae of mycorrhiza in the soil. The indirect or “secondary” impacts of glomalin on the formation and stabilization of soil aggregates further improved the efficiency of the symbiotic relationship and the growth environment (Rillig and Mummey 2006).

Glomalin rich soil protein released by AMF enhances soil aggregation. There is increasing circumstantial evidence accumulating from decomposition studies that GRSP is of AMF origin (Fig. 10.9). When AMF growth is eliminated, e.g. by incubating soil without host plants, we have observed that GRSP concentrations decline, along with AMF hyphae (Steinberg and Rillig 2003).

Tillage results in destroying soil structure and also hyphae of mycorrhizae. So due to tillage, efficiency of mycorrhizae and also carbon requirement for glomalin production subsequently reduced. No-tillage (NT) practices along with continuous cropping systems (by eliminating fallow periods and/or growing cover crops), using mycorrhizal host crops, and reducing synthetic inputs (especially P), enhance the plant-mycorrhizal symbiotic relationship (Nichols and Wright 2004; Preger et al.

2007; Roldan et al. 2007; Rillig 2004; Rillig et al. 2007).

AMF, as a factor of soil quality, can perhaps be viewed to be important via three main mechanisms: influences on plant physiology, soil ecological interactions and

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Immunoreactivity monoclonal antibody

GPRS is (at least partly of AMF origin Decomposition evidence

In-vitro culture evedence

Fig. 10.9 Various lines of evidence suggest that GRSP in soil is of arbuscular mycorrhizal fungal origin, although conclusive evidence can only come from additional detection tools

soil engineering (Fig. 10.10). These mirror the importance of the symbiosis at the individual plant level, in community ecology and in influencing processes at the ecosystem scale, respectively (Fig. 10.11).

Glomalin is present in large amounts in soils which is indeed a distinct component of soil organic matter. This is a glycoprotein from Glomales which is the taxonomic genera to which AMF belong (Wright and Upadhyaya 1996). The main detection tool is a monoclonal antibody (MAb32B11), raised originally against crushed AMF spores (Wright and Upadhyaya 1996). The extraction of glomalin from plant hyphae and soils is extremely drastic.

In fact, it is the severity of the extraction conditions that clearly demonstrates its uncommonly high stability. Glomalin is very difficult to solubilize, and it is resistant to most chemical used in routine and characterization methods (Wright and Upadhyaya 1996). Table 10.1 shows the various fractions of soil proteins and glomalin and the correlation coefficients for EEG and TG on soil aggregation according to Wright and Upadhyaya (1998) (Table 10.2).

10 Mycorrhizae: A Potential Microorganism and Its Implication in Agriculture Strength of available evidence

Ecosystem and soil ecology

GRSP correlation with WSA Responses to treatments Persistence, distribution

Fungal community ecology

Differences in GRSP production

Fungal physiology (organism)

Functions in AMF biology • Habitat engineering • others

Cell/hyphal biology

Glomalin secretion Presence in hyphal wall

Biochemistry/ Molecular biology

Biochemical characterization of putative gene product

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Fig. 10.10 Reflecting the origins of research on GRSP in soil sciences, there is currently a strong gradient of knowledge available from the ecosystem level to the biochemistry level Habitat engineering capability

Soil ecological interactions

Soil Quality: Sustained capacity to produce

Plant physiology influences

Fig. 10.11 Arbuscular mycorrhizal fungi as a component of soil quality, more than just plant nutrition Table 10.1 Proposal for a new terminology describing various fractions of soil proteins and glomalin Current usage TG (total glomalin) EEG (easily extractable glomalin) Glomalin

Identity Bradford-reactive soil protein (after autoclave/citrate extraction) Bradford-reactive soil protein (easily extracted autoclave/ citrate extraction) Gene product and protein

Proposed new name/usage BRSP (Bradford-­ reactive soil protein) EE-BSRP (easily extractable)

Justification Bradford assay is non-specific for a particular protein Bradford assay is non-specific for a particular protein GRSP (glomalin-­ It is a very complex related soil protein) compound

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Table 10.2 Correlation coefficients for fractions of glomalin, %C in soil aggregates and aggregate stability (Wright and Upadhyaya 1998) %C 0.49** 0.61*** 0.65***

EEG TG Aggregate stability

EEG

TG

0.94*** 0.69***

0.70***

** and *** denote significance at p < 0.1 and p < 0.01, respectively 0.7 0.6

weight (gm)

0.5

a

a

0.4 0.3

Mycorrhiza

0.2

Non Mycorrhiza

0.1

b

b

0 Fresh Weight

Dry Weight Parameters

Fig. 10.12 Effects of mycorrhizal inoculation on the growth of Ipomoea aquatica. Error bars indicate standard deviations (SDs). Mean values followed by the different letters are significantly different (P < 0.05) and same letters are not significantly different (P < 0.05)

10.6.4 E ffect of Arbuscular Mycorrhizal Fungi Inoculation on Growth and Uptake of Mineral Nutrition 10.6.4.1 Increase in Ipomoea aquatica Weight After Mycorrhizal Inoculation The fresh weight of mycorrhiza-inoculated plants was higher than that of uninoculated (control) plants (Fig. 10.12). The average fresh weight of mycorrhiza treatment plants was 0.48 ± 0.l6 gm, whereas the fresh weight of control plants was 0.45 ± 0.09 g. Similarly to the fresh weight, the dry weight of treatment plants (0.034 ± 0.005) was similar to the control plants (0.032 ± 0.018 gm). There were no significant (p < 0.05) differences between the plant weight of mycorrhiza-inoculated plants and non-mycorrhizal-infected plants. Tabassum et al. (2011) showed that the AM fungi significantly increase the growth of cowpea plants compared to noninfected plants.

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10.6.4.2 Effects of AMF Infection on Macronutrient Uptake Among the measured macronutrients, K uptake was highest compared to other macronutrient uptake followed by Na and Mg for both the cases of mycorrhiza-­treated and mycorrhiza-nontreated plants. Least amount of P uptake was observed (treated with mycorrhiza as 0.01 mg/plant and untreated as 0.007 mg per plant). In mycorrhiza-inoculated plants, Na and Mg uptake was 0.015 mg/plant and 0.014 mg/plant higher than control plants as 0.013 mg/plant and 0.01 mg/plant, respectively. These findings are supported by the work of Tabassum Yaseen et al. (2011) who showed that nutrient uptake of AMF-infected plants is higher compared to non-­AMF-­ infected plants.

10.6.4.3 Effects of AMF Infection on Micronutrient Uptake All determined micronutrient uptakes in AMF-treated plants were higher than control plants (without AMF). The uptake of micronutrients like Fe, Mn and Zn was 0.24, 0.07 and 0.23 mg/plant in case of mycorrhiza infection, but for noninfected plant the uptake was 0.16, 0.02 and 0.09 mg/plant, respectively. AMF have been also shown for betterment of immobile soil nutrient uptake such as P, Zn and Cu (Jiang et al. 2013; Liu et al. 2002).

10.6.5 A rbuscular Mycorrhizal Fungi: Implications for Integrated Weed Management (i) Mycorrhizal growth responses (MGRs) in different environmental conditions will help identify situations that favour AMF in IWM (Li et al. 2016). Depending upon the conditions and weed communities of a particular agroecosystem, it may be feasible for producers to use different levels of tillage intensity, vegetation management and soil fertility inputs to manage AMF-weed-crop interactions and thereby enhance IWM (Table 10.3).

AMF did not differentiate in their impacts on strong host crops and strong host weeds. However, AMF may differentially benefit high-mycorrhizal growth response crops compared to low-mycorrhizal growth response host weeds, enhancing indirect weed suppression by crop competition, as proposed in Fig. 10.13.

10.6.6 Reclamation of Heavy Metals by Mycorrhiza Extraradical mycelium (ERM) of mycorrhiza from polluted soils accumulated Cu in the mucilaginous outer hyphal wall zone, cell wall and inside the hyphal cytoplasm.

The accumulated Cu was mainly associated with Fe in the mucilaginous outer

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Table 10.3 Recommended management decisions based on host status and crop-weed community composition for use of arbuscular mycorrhizal fungi (AMF) in integrated weed management (IWM) approach Dominant crop Strong host crop

Dominant weed Weak host weed

Weak host crop Weak host crop Strong host crop

Strong host weed Weak host weed Strong host weed

Management for greater AMF weed control AMF are mostly weed suppressive under these conditions.

Practices supporting high AMF diversity and low N and P fertilizer addition are suggested Practices supporting high AMF diversity and relatively high N and P fertilizer addition are suggested Low N and P fertilizer addition suggested AMF suppression of weeds is not favoured

Fig. 10.13 Proposed interactions among crops, weeds and arbuscular mycorrhizal fungi (AMF).

Black arrow: AMF may directly suppress the growth of weak host weeds through impeding their root growth. Grey arrows: AMF may indirectly suppress the growth of some strong host weeds through increasing the competitive ability of their adjacent strong host crops

hyphal wall zone and in the cell wall. Copper was associated with traces of arsenate inside the cytoplasm of the ERM of Glomus mosseae (Gonzalez-Chavez et al.

2002).

Although the mycorrhizal mechanisms for enhancing uptake are not entirely known, some of them could be the following: 1. Transfer of metals to the hyphae by cation exchange and chelation (non-metabolic binding of metals to cell walls).

2. Interacting with hyphal synthesized products or metabolites that act as biosorption agents such as chitin and glomalin, an insoluble glycoprotein.

3. The thin hyaline layer of the spore wall of Glomus geosporum AMF is composed mainly of chitin (Sabrana et al. 1995).

4. Chelation of metals inside the fungus. Intracellular precipitation with phosphate (PO4).

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Table 10.4 Elemental content of 14-week-old maize grown in heavy metal-contaminated soil from Breinigerberg with and without the arbuscular mycorrhizal fungus Glomus intraradices Sy167. The elemental concentrations in roots and shoots were measured by AAS and are given in mg/kg of dry weight Element Mg Ca Al Fe Zn As Pb

Shoot (+AMF) 3330 ± 35 7190 ± 45 30 ± 4 62 ± 2 830 ± 15 <3 45 ± 2

Shoot (−AMF) 5475 ± 30 30,300 ± 140 1124 ± 3 820 ± 20 1170 ± 120 10 ± 2 200 ± 15

Root (+AMF) 8750 ± 10 26,200 ± 40 2720 ± 4 3030 ± 150 4600 ± 200 <3 1200 ± 90

Root (−AMF) 4520 ± 6 21,900 ± 20 5500 ± 50 5670 ± 150 5900 ± 200 40 ± 3 1800 ± 60

Data are from Kaldorf et al. (1999) Standard deviations are for n = 2

However, arbuscular mycorrhizal fungi (AMF), especially Glomus intraradices, colonized Festuca and Agropyron species that have shown higher heavy metal (Zn, Cd, As and Se) content. As for hyperaccumulators, fungi can synthesize cysteine-­ rich metal-binding proteins called metallothioneins (Gadd and White 1989).

Mycorrhiza might therefore be directly implicated in heavy metal hyperaccumulation in plants. Maize colonized by Glomus intraradices has considerably smaller amounts of heavy metals in both its roots and its shoots than non-AMF controls (Table 10.3). In contrast, essential elements like P, Mg2+ and Ca2+ are enriched in the roots of AMF-colonized plants, as shown by atomic absorption spectrometry.

This is in contrast to Fe, Zn, Pb and also other toxic elements such as Al and As. The location of the heavy metals in plant tissues can be demonstrated by biophysical techniques such as EDXA, SIMS or LAMMA (Kaldorf et al. 1999) (Table 10.4).

10.7 Future Perspective Since the concepts of “rhizosphere” and “mycorrhizosphere” were coined, it has been recognized that microbial populations may vary in different fractions of soil and in the various zones of the rhizosphere and the mycorrhizosphere. A large proportion of mycorrhizosphere bacteria remains unculturable, and it is therefore difficult to assess the microbial diversity in the mycorrhizosphere and the relative contribution of unculturable microorganisms to the interactions in the mycorrhizosphere. AM fungi themselves cannot be grown in pure culture, but root organ cultures are routinely used to culture AM fungi in vitro and can be used for investigating the interactions of AM fungi with their biotic and abiotic environment (Filion et al.

1999). Although the composition of microbial communities in the various parts of the mycorrhizosphere in different ecosystems has been described and discussed in many papers, the underlying mechanisms behind the interactions are still poorly known. Protein identification is strongly dependent on gene and protein sequences

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available in databases, and the constant increase in the number of sequenced genomes in the past decade, together with improvement of mass spectrometry technology, has helped scientists to obtain more reliable data. Novel MS/MS techniques developed in the past few years in other research fields could also be applied to investigate plant-fungus symbiotic interactions. For example, selected reaction monitoring (SRM) is a targeted MS technique used to complement untargeted shotgun methods.

SRM is used to measure across multiple samples – in a consistent, reproducible and quantitatively precise manner – a set of candidate proteins involved in a particular cellular process (Picotti and Aebersold 2012). However, methodological advances have greatly improved the monitoring of the fate and behaviour of microorganisms in both natural and artificial systems. An intriguing field of research that needs to be further explored is the role of cell-to-cell interactions of microorganisms. Mycorrhizal fungi mobilize P and N and are an important C sink in the soil, having therefore an important impact on the cycling of these elements (Klironomos 2005). As biofertilizers, they may counteract fertilization excess and thus promote sustainable agriculture. The selection of new crop varieties giving yields on poor soils and in low fertilization conditions should therefore consider new aspects, such as their responsiveness to mycorrhizal fungi, which has never consciously been taken into account during plant domestication (Sawers et al.

2008). If the promises of mycorrhizal research are easy to catalogue, many constraints related to the biology of mycorrhizal fungi still limit their fulfilment.

Identification of the signalling molecules released by AM and EM fungi is a first necessity. Although the potential Myc factor from AMs is currently under investigation (Bucher et al. 2009), on the basis of potential similarities with the Nod factor, the production of similar molecules did not emerge from the genomes of EM fungi; rather, there is evidence of the presence of small secreted proteins. Once these basic biological questions have answers, we will be ready to exploit the mycorrhizal fungal community hidden in the soil but quietly benefiting plants and humans. Studying the spatiotemporal stability of such fungal associations would provide more information on this potential and improve our understanding of microbial interactions, which may be important for the development of sustainable management of soil fertility and crop production.

10.8 Conclusions Mycorrhizal fungi are now known to provide a wide range of significant benefits to their plant hosts. In addition to enhancing mineral nutrition, they induce greater resistance to soil pathogens, enhance tolerance to drought stress and reduce sensitivity to toxic substances occurring in the soil. Mycorrhizal colonization in plant root improves mineral nutrient uptake and plant growth. Macronutrient concentration and uptake as well as micronutrient concentration may be an efficient strategy to utilize environment-friendly biofertilizer instead of chemical fertilizer.

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AMF play important roles in agroecosystems, including the involvement of the extraradical mycelium in providing soil aggregation. GRSP has been shown to be correlated with soil aggregate water stability. Many efforts have been made in recent years to accrue benefits from mycorrhizae for agriculture, horticulture, forestry and site remediation. The results have been consistently positive, with some difficulties due to complications from diverse variables under field conditions. Mycorrhizal interactions between plants, fungi and the environment are complex and often inseparable. Proteomic techniques will be powerful tools to unravel the molecular component involved in plant-mycorrhizal fungal interactions. Mycorrhizae are an essential belowground component in the establishment and sustainability of plant communities, but thorough knowledge is required to achieve maximum benefits from these microorganisms and their associations.

Acknowledgement The authors thank the Head of Soil Biology Division, IISS, Bhopal, Dr. MC Manna for spending his valuable time for review.

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