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Review Article

Mycorrhizal Fungi as a Biocontrol Agent

M.M. Tahat, Kamaruzaman , Sijam and R. Othman
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Arbuscular mycorrhizae fungi (AMF) are the symbiotic fungi that predominate in the roots and soils of agricultural crop plants. The AMF form beneficial symbioses in most terrestrial ecosystems and crop production systems. Ninty percent of land plant species are colonized by one or more of the mycorrhizal fungi species ranging from flowering to non flowering plants, while only a few plant families do not form this association. The relationship between mycorrhiza and plant is very widely spread among terrestrial vascular plants. The AMF must have a host to complete its life cycle and this association has been found to be mutually beneficial; thus, the fungus assists the plant in mineral nutrients uptake, while the plant supplies the fungus with carbon as a result of this relation. The negative-antagonistic interaction of AMF with various soilborne plant pathogens is the reason for their use as a bio-control agents. Many workers have observed an antagonistic effect of AMF against some fungal pathogens.

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M.M. Tahat, Kamaruzaman , Sijam and R. Othman, 2010. Mycorrhizal Fungi as a Biocontrol Agent. Plant Pathology Journal, 9: 198-207.

DOI: 10.3923/ppj.2010.198.207

Received: August 28, 2010; Accepted: September 17, 2010; Published: November 12, 2010


Mycorrhizal fungi are a major component of the agricultural natural resource and they are members of the fungus kingdom. Asymbiotic association of fungus and roots has been discovered in Monotropa Hypopity by Franciszek Kamienski (1881). The studies of the Polish botanist Frank 1885 had initiated worldwide interest on a fungus-root (Myco-rhiza). Also, he gave the name MYCORRHIZA to the peculiar association between root trees and ectomycorrhizal fungi. The AMF play an important function in the reduction of plant pathogens (Whipps, 2004; St-Arnaud et al., 1994; Azcon-Aguilar and Barea, 1997), such as Rhizoctonia solani (Yao et al., 2002) and Pythium ultimum and Phytophthora species (Trotta et al., 1996; Cordier et al., 1996). In different crops the AMF have also been shown to reduce bacterial diseases (Dehne, 1982), for example, Glomus mossease suppressed Ralstonia solanacearum, bacterial wilt causal organism on tomato (Tahat et al., 2009).

There have been a few studies of the potential role of Arbuscular Mycorrhizal Fungi (AMF) for the protection of plant from pathogens.


Mycorrhizal fungi association widely varied in structures and functions, but the Arbuscular Mycorrhizae (AM) are the most common interactions (Harrier, 2001). Six genera of arbuscular mycorrhizal fungi have been recognized based on morphological characteristics of a sexual spores and also based on various biochemical studies as well as molecular methods (Peterson et al., 2004). Further, various criteria have been used for the identification of AMF like hyphal character, auxiliary cells subtending hyphae, spore or sporcarp ontogeny, morphology, germination, shield spore wall, biochemical, molecular and immunological characteristics (Mukerji et al., 2002). Few species of host roots synthesize a yellow pigment when colonized by mycorrhizal fungi which is considered as a sign of infection (Peterson et al., 2004). AMF are zygomycetous belonging to the genera Glomus, Gigaspora, Sclerocystis, Acaulospora, Entrophospora and Scutellospora (Garbaye, 1994).

The classification of AMF is based on the structure of their soil-borne resting spore, biochemical properties and molecular studies (Morton and Benny, 1990). The latest classification of AMF contains 4 orders with 9 families (Table 1) (Sieverding and Oehl, 2006). Plant species belonging to the cruciferae and chenopodiaceae are not known to form AMF symbiosis (Smith and Read, 1997).

The AMF reproduce asexually by spore production. There is no evidence that AMF reproduce sexually (Kuhn et al., 2001).


Seven different types of mycorrhizal fungi association have been recognized and the most important types are:

Table 1: Recent classification of arbuscular mycorrhizal fungi (Sieverding and Oehl, 2006)
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Endo-mycorrhizae: Endo-mycorrhizae represent a group of fungi that are associated with most agricultural crops and provide biological protection against soil-borne diseases (Smith and Read, 2008). They occur in most ecosystems of the world and are found in many important crop species (wheat, maize, rice, grape, soybean and cotton) and horticultural species roses, petunias and lilies) (Peterson et al., 2004). AMF are obligatory biotrophs feeding on the products of their live plant host and those fungi are not specialized to their potential hosts. The host plant receives mineral nutrients from outside the roots depletion zone via the extraradical fungal mycelium, while the AMF obtains photo-synthetically produced carbon compound from the host (Smith and Read, 1997).

Many endomycorrhizal fungi form terminal or intercalary vesicles in the root cortex. When the vesicles are expanded the thin walled structures, which are not septum and it's contain a large quantity of lipids. They may be oval, spherical, or lobed in shapes and may become thick walled and resting spores (Pirozynski and Dalphe, 1989). The term arbuscular mycorrhiza replaced the earlier term vesicular arbuscular mycorrhizae (VAM) because some endomycorrhiza produce vesicles, but all form arbuscules (Strack et al., 2003).

Ecto-mycorrhizae: Ecto-mycorrhizal (ECM) fungus forms a thick mantle structure within the intercellular spaces of root cortex and a sheath around the feeder root acting as an interface for channeling of nutrients from the plant to the fungus and vice versa (Kumar and Satyanarayana, 2002). Ectomycorrhizal fungi do not penetrate living cells in host roots, but can only surround them. The extensive mycelium produced by ectomycorrhizal may function in transferring nutrients directly from the decaying leaves (Suverch et al., 1991).

Ectomycorrhizas are most common in ornamental and forest trees species in the family Pinaceae, Myrtaceae, Salicaeae, Dipterocarpecae, Fagaceae and Gentum plants (Shalini et al., 2000). Ectomycorrhizas are distinguished by the presence of mantle and the hartig net. Hartig net (develops in cortical cells or epidermal cells. Hartig net consists of branch systems which can provide a large surface contact between cells of the two symbionts (Peterson et al., 2004).

Other types of mycorrhizal fungi include (Ecto-endo Mycorrhiza, Ericoid Mycorrhiza, Monotropoid, Arbutoid mycorrhizas and Orchid mycorrhiza) (Smith and Read, 2008).


Mycorrhizal fungi offer protection against pathogens (bio-control agents): Soil borne pathogens were controlled by using several agricultural practices methods, such as resistant cultivars, seed certification, chemical fungicide,s crop rotation and soil fumigation etc. There are many problems associated with controlling pathogens with long-term persistent survival structures due to difficulties in reducing pathogen inoculum and lack of good sources of plant resistance (Azcon-Aguliar and Barea, 1997). Therefore, many researchers were trying to use alternate approaches based on either manipulating or adding microorganisms to enhance plant protection against pathogens (Grosch et al., 2005). The beneficial microorganisms (antagonistic bacteria) (e.g., Pseudomonas fluorescens, Bacillus subtilis, etc.) and fungi (e.g., AMF, Trichoderma, etc.) compete with plant pathogens for nutrients and space, by producing antibiotics, by parasitizing pathogens, or by inducing resistance in the host plants. These microbes have been used for biocontrol of pathogens (Berg et al., 2007).

The extensive use of chemicals to control diseases poses a serious threat to the present day plant production systems (Dehne, 1982). Currently the use of beneficial microorganisms is one of the alternative management practices reviewed to have protective effect against plant soilborne pathogens (Brimmer and Boland, 2003; Mukerji et al., 2002).

The protective effect of mycorrhizal symbioses against root pathogenic fungi has been tested by many researchers (Caron, 1989; Dehne, 1982). Disease reduction within host plants colonized by AMF is the result and output of the complex interactions between pathogens, AMF and plant (Harrier and Watson, 2004). AMF symbiosis has been shown to reduce the damage caused by soilborne pathogens (Azcon-Aguilar et al., 2002). Phytophthora parasitica proliferation greatly reduced when tomato root colonized by Glomus mosseae and P. parasitica compared with non-mycorrhizal tomato roots (Cordier et al., 1996). Trotta et al. (1996) found that phosphate by AMF may contribute to lessen the damage by P. parasitica in tomato. The presence of AMF successfully delays the time required by Ganoderma boninense to infect and kill oil palm plant and the seedlings were more resistant to G. boninense (Rini, 2001). AMF has shown no indirect interaction with soilborne pathogen through antagonism, mycoparasitism and or antibiosis (Harrier and Watson, 2004). Different mechanisms have been reported to explain bio-control by AMF including biochemical changes in plant tissues, microbial changes in rhizosphere, nutrient status, anatomical changes to cells, changes to root system morphology and stress alleviation (Hooker et al., 1994). Therefore, those mechanisms by which AMF could control the soil borne pathogen are listed below:

Enhancing plant nutrition uptake: Improvements in plant growth followed by root colonization by AMF occurs as a result of enhancement of the mineral nutrient status of plants. Some reports indicate that phosphorus induced changes in root exudation could reduce the germinations of pathogen spores (Graham, 1982; Sharma et al., 2007). Some studies suggest that competition for space between AMF and pathogen, AMF may increase host tolerance to pathogen by increasing the uptake of essential nutrients rather than phosphorus which are otherwise deficient in the non-mycorrizal plants (Gosling et al., 2006). The AMF spores germinate and thick-walled hyphae penetrate the host root causing internal infection. After penetrating into the root, the hyphae spread inter- and/or intra-cellularly in the root cortex without damaging the integrity of the cells (Strack et al., 2003). The increasing nutrient uptake resulted in more vigorous plants; thus, the plant itself may be more resistant or tolerant to pathogen attack (Linderman, 1994).

Damage compensation: It is suggested that AMF increase host tolerance of pathogen attack by compensating for the loss of root functional and biomass caused by soilborne pathogens (Linderman, 1994) including fungi and nematodes (Cordier et al., 1996). This illustrates an indirect contribution to the biological control through the conservation of root system function both by AMF hyphae growing out into the soil and increasing the root absorbing surface area as well as by the maintenance of root cell activity through arbuscules formation (Gianinazzi-Person et al., 1995).

Soil microbial population interactions: The first report attempted to specifically study the interaction of plant pathogenic fungus and a species of AM fungus was that of Safir (1968). The role of AMF in improving plant nutrition and their interactions with other soil biota have been investigated with reference to the host plant growth. Few information’s known about how these interactions affect soil structure (Schreiner and Bethlenfalvay, 1995). Plants colonized by AMF differ from non-mycorrhizal plant in rhizosphere microbial community, resulted in alterations in root respiration rate quality and quantity of the exudates (Marschner et al., 2001).

Hyphae emerging from spores in the presence of bacteria smoothly developed small vesicles, longer and more branched than those without bacteria (Khan, 2005). The growth and health of plants influenced by the microbial shifts occur in the mycorrhizosphere (Azcon-Aguilar et al., 2002). This effect has not been specifically evaluated as mechanisms for AM-associated biocontrol, but there are indications that such a mechanism does operate (Linderman, 1994). Some reports suggest that AMF alter the composition of functional groups of microbes in the mycorrhizosphere, including the numbers and/or activity of pathogens antagonists (Secilia and Bagyaraj, 1987).

No alteration was observed in the total numbers of actinomycetes or bacteria isolated from Trifolium subterraneum L. and Zea mays colonized by Glomus fasciculatum. However, there was a change in the functional groups of these microbes, including more facultative anaerobic bacteria in mycorrhizosphere of AMF colonized T. subterraneum. The total number of bacteria isolated from rhizoplane of T. subterraneum and Zea mays increased as a result of AMF colonization (Meyer and Linderman, 1986). The population of Fusarium oxysporum in the mycorrhizosphere soil of tomato reduced in AM plants relative to non-mycorrhizal one (Johansson et al., 2004).

Plant root systems colonized by AMF differ in their effects on the bacterial community composition within the rhizosphere and rhizoplane (Burke et al., 2002). Several biotic and a biotic factors are very important for determination of efficiency of AMF as a disease control agent. The most important factors are, soil moisture, soil contents, host genotype, mycorrhizal level inoculums, inoculation time of mycorrhiza, mycorrhizal fungi species virulence, inoculums potential of pathogen and soil microflora (Singh et al., 2000).

Systemic bio-protection of plant against take all disease of barely plant depends on a high degree of AMF root colonization (Khaosaad et al., 2007). The use of AMF resulted in resistance increment against the wilt pathogen Fusarium oxysporum f. sp. Lini (Dugassa et al., 1996). Two zones of interactions can be defined (1) The rhizoplane and the surrounding rhizosphere soil and (2) The mycosphere (Bansal and Mukerj, 1994). Mycorrhization Helper Bacteria (MHB) certainly improve the ability of mycorrhiza fungi to colonize plant roots (Fitter and Garbaye, 1994).

Competition for colonization and infection sites: Physical competition between endomycorrhizal fungi and rhizosphere microorganisms to occupy more space in the root architecture is the first mechanism to explain the interaction between AMF and soil microorganisms (Bansal and Mukerji, 1996). Mycorrhizal fungi depend on the plant host photosynthates, so the competition for carbon compounds maybe, a cause of the pathogen suppression in mycorrhizal plant. The interaction between AMF and Phytophthora in tomato plant has shown that the pathogen dose not penetrate arbuscular containing cells (Cordier et al., 1998). Dehne (1982) documented how AM fungi and root pathogens colonize in the same host tissues and how they develop in different root cortical cells, indicating some sort of or competition for space. The interaction of Glomus mosseae and phytophthora nicotiana var. parastica in tomato was shown to increase the AMF at the root apex site.

Morphological and anatomical changes: Root morphology system can be altered due to the colonization of root by AMF (Tahat et al., 2008). Roots colonized by AMF are more highly branched compared to non colonized plants and also the adventitious root diameters are larger (Berta et al., 1993), which can provide more infection sites for a pathogen (Hooker et al., 1994). Dugassa et al. (1996) found that the infection of tomato and cucumber by Fusarium wilt might slow down due to the morphological changes in the root cells of the endodermis of AM plants which include lignifications incensement. The raising lignifications may protect the roots from penetration by other pathogens, while elevating of phenolic metabolism within the host plant (Miranda, 1996).

The colonization of tomato root by Glomus mosseae lead to a bigger root size and more branching which increase the number of root tips, length, surface area and root volume (Tahat et al., 2008). Root damage by Gaeumannomyces graminis var. tritici was systemically reduced when barley plants showed high degree of mycorrhizal root colonization. Allowing mycorrhizal root infection exhibited no affect on Gaeumannomyces graminis var.tritici infection (Khaosaad et al., 2007).

Competition for host photosynthates: The growth of AMF and root pathogen depends on the host photosynthates and they compete for the carbon compounds received by the root (Smith and Read, 1997). When AMF have primary access to the photosynthates, the higher carbon demand may inhibit the pathogen growth (Linderman, 1994). AMF is dependent on the host plant for carbon source. 4-20% net photosynthates of host are transferred to the fungus; nevertheless, there is only a limited data to support this mechanism (Smith and Read, 2008).

Changes in chemical constituents of plant tissues (root exudates): Phytoalexins toxic components are not detected during the first stages of AM formation but can be detected in the later stages of symbiosis (Miranda, 1996). Wall-bound peroxidase activity has been detected during the initial stage of AM colonization (Azcon-Aguilar et al., 2002). Phytophthora parasitica development decreased in Glomus mosseae and non G. mosseae parts of tomato mycorrhizal root systems in association with plant cell defense responses and accumulation of phenolics. Cortical cells containing G. mosseae are immune to the pathogen and exhibit a localized resistance response (Cordier et al., 1998). Corresponding proteins involved in plant defense responses have been studied in AMF symbioses; these include hydroxyproline-rich glycoproteins, phenolics peroxidases, chitinase, B-1-3 glucanases-callose deposition and PR-phathogenesis related proteins (Miranda, 1996).

Root exudates play an important role in AMF establishment symbiosis (Vierheilig et al., 2003). The germination of Fusarium oxysporum f.sp., Lycopersici was inhibited in the presence of root exudates from tomato (Scheffknecht et al., 2006). Root exudates from mycorrhizal strawberry plants suppressed the sporulation of Phytophthora fragariae (in) in vitro study (Norman and Hooker, 2000). Differential growth of Fusarium oxysporum f.sp chrysanthemi, Trichoderma harzianum, Clavibactor michiganesis and Pseudomonas chlororaphis was explained by substances released from Glomus intraradices under in vitro culture conditions (Filion et al., 1999). Grandmaison et al. (1993) suggested that phenolic compounds bound to cell wall could be indirectly responsible for the resistance of AMF roots to pathogenic fungi since they increased the resistance of cell wall to the action of digestive enzymes.

Nutrient uptake: The primary goal of AMF inoculation is to increase and enhance the yield and production of plants (Brundrett and Juniper, 1995). The main benefits of AMF are enhancing plant the acquisition of mineral nutrients and increasing the ability of host plants to withstand or reduce acquisition of toxic elements to growth (Clark, 1997). AMF provide a greater effective root surface area to explore greater volumes of soil and to overcome water and nutrient depletion zones around active root surfaces (Smith and Read, 2008).

Mycorrhizal plant roots have increased weight, length, number and layer diameters than the non-mycorrhizal one (Hetrick et al., 1988). Since, the average diameter of fungal hyphae is 3-4 μM, which is smaller than the root hair diameter (>10 μM). Therefore, fungal hyphae penetrate soil pores and contact with soil so that roots hair would not able to contact. AM roots greatly enhance the acquisition of mineral nutrient in plant (Jakobsen, 1995). Mycorrhizal research has shown the increased nutrient uptake; mainly Phosphorus (P), in mycorrhizl plants compared to non-mycorrhizal plants (Akthar and Siddiqui, 2008). Soil phosphorus absorption by mycorrhizal plants is complete and faster than the non-mycorrhizal plants, because the distance of diffusion for HPO4-2 and H2PO4 ion in the soil will be shorter to the hyphae than to the root (Li et al., 1991). Some studies indicate that increased phosphorus nutrition has the same effect as inoculation with AMF (Davies et al., 1992). Numbers of physiological changes are induced in AMF root as a result of an increase in nutrition uptake (Graham, 2001). Enhancement of phosphorus status is the major benefit of mycorrhizal fungi. This is due to the uptake of phosphorus from the soil by the AMF and then transfers it to the host plant (Smith et al., 2003).

The improvement of P nutrition of plants has been the most recognized and well established beneficial effect of mycorrhizas (Karandashov and Bucher, 2005; Cardoso et al., 2006). Phosphate is converted into polyphosphate by polyphosphate kinase in vacuoles (incorporated) and is transported between the hyphal tips and a sink at the symbiotic interface (Pearson and Tinker, 1975). Translocation rate is affected by rates of net efflux of P at hyphal tips and net uptake (Johanson et al., 1993). The abnormally high P loss from the arbuscules has been explained and two mechanisms have been proposed in this connection: Firstly, a high arbuscular P concentration will reduce hyphal re-absorption of lost P and this is in accordance with low expression of high P affinity transporter in the fungal tissue inside roots, compared to its expression level in the external hyphae (Harrison and Van Buuren, 1995). Secondly, P efflux may be promoted by altered operation of trans-membrane that is carrying and opening of ion channels. Mycorrhizal fungi are able to mobilize P and N from their organic substrates (Smith and Read, 1997).

AMF is the most efficient ecological factor in improving growth and N content in legumes (Barea et al., 2002b). Enhanced nitrogen (N) acquisition by AM plants has been reported. This enhancement has been explained by high nitrogen demand because of enhanced phosphorus (George et al., 1995). The hyphal of AMF have the capacity to take-up and transport N from soil to root (Bago and Becard, 2002). The uptake and translocation of nitrogen by hyphal fungus is regulated by host plant’s demand for N (Hawkins and George, 2001). AM hyphae absorb and translocated amounts of nitrogen when provides as NH+4 and NO-3 (George et al, 1992). Hyphae took up about 40 % of the nitrogen applied as (NH4)2SO4 to a hyphal soil compartment, while some nitrogen was transported by hyphae over a distance of 5 cm within six days (Fery et al., 1994). In addition to phosphorus and Nitrogen, AM fungi are known to have enhanced uptake of Zn, S and Ca (Clark and Zeto, 2000) and also Iron (Fe) acquisition has been enhanced. It is found that AM plants that are grown at low pH had higher Fe acquisition than AM plants grown at high pH (Treeby, 1992). Manganese acquisition generally was lower in AM plants compared to non AM plants (Azaizeh et al., 1995).

Enhance tolerance to heavy metals (bioremediation): The effect of AMF plants on trace elements uptake was reported (Clark and Zeto, 2000). The AMF have higher shoot concentrations of copper (Cu) and zinc (Zn) when grown in soil with low concentration of these elements. Copper and zinc concentrations increased in leaves of AM soybean plants compared to nonmycorrhizal plants. Sulfur acquisition was enhanced in sorghum colonized by Glomus fasciculatum compared to non colonized plants (Raju et al., 1990). Boron content was increased in AM maize shoot in acidic and alkaline soils while the acquisition of calcium (K), sodium (Ca) and magnesium (Mg) was also increased compared to the non AM Gigaspora gigantia soybean plants in low Phosphorus. At the same time Gigaspora gigantia colonized maize plant was decreased (K) and Ca but increased Mg acquisition (Lambert et al., 1979). Aleminum (Al) acquisition toxicity was lower in AM switch grass grown in acidic soil compared to non AM plants (Clark, 1997).

The AMF were shown to enhance the acquisition of (Br) and (Cl) (Ellis et al., 1995) and (Cd) (Copper and Tinker, 1978). (Co), (Cs) and (Ni) (Rogers and Williams, 1986). AM hyphae can uptake trace elements in very low concentration including Zn, Fe and Cu from the soil solution (Bago et al., 1996).

Mycorrhizosphere: Mycorrhizosphere refers to the zone of soil influence by mycorrhizal association (Oswald and Ferchau, 1968). The first reported about the role of the mycorrhizosphere in biocontrol of pathogens was by Meyer and Linderman (1986). They found that extracts of rhizosphere soil from mycorrhizal plants reduced sporangia formation of Phytophthora cinnamomi in comparison with extracts of rhizosphere soil from non-mycorrhizal plants. These authors postulated thateither the sporulation-inducing microorganisms were missing or that the number of sporulation-inhibiting microorganisms increased. The changes in root exudates affect the microbial communities around the roots leading to the formation of mycorrhizosphere (Varama et al., 1999). In mycorrhizosphere the appearance of mycorrhizae exert a strong influence on the microflora in the rhizosphere. The mycorrhizosphere microbiota differs qualitatively as well as quantitatively from the non rhizosphere mycorrhizal plants. Mycorrhizosphere has two components:

The layer of soil surrounds the mycorrhizal roots

The layer of soil surrounding AMF hyphae in the soil referred to as the hyphosphere

Data have been acquired that rhizosphere bacteria have efficient impacts on AMF growth (Azcon-Aguilar et al., 2002). The interaction between AMF and other soil microbes in mycorrhizosphere can be classified as positive (synergistic) as well as negative (antagonistic) interaction (Mukerji et al., 2002). The positive interaction of AMF with Plant growth promoting bacteria (PGPR), phosphorus-solubilising bacteria and N2-fixing bacteria can enhance the AMF spores germination and the plant growth (Mayo et al., 1986). Negative interaction is related to the ability of AMF to suppress and inhibit the occurrence of various pathogens (Dehne, 1982).

Arbuscular mycorrhizal fungi and beneficial soil microorganism’s interactions: The interaction between mycorrhizal fungi and other soil organisms are complex and often poorly understood; they may be inhibitory or stimulatory (Fitter and Garbaye, 1994). The PGPR interact with mycorrhiza in the mycorrhizosphere. Inoculation of Glomus faciculatum has shown a positive influence on actinomycetes population in tomato rhizosphere. The survival of Azotobacter paspali increased in mycorrhizosphere (Barea et al., 2002b). Higher bacterial population and number of nitrogen fixer such as streptomycin were reported and it has been detected that plants in the presence of AMF and bacteria produced more phytohormones (Secilia and Bagyaraj, 1987).

The relationship between Phosphate-Solubilizing Bacteria (PSB) and AMF is well reported (Barea et al., 2002a). The PSB can survive longer in mycorrhizospher root. A plant with higher concentration of P benefits the bacterial symbiont and nitrogenase functioning (Barea et al., 1993). Dual inoculation of AMF and PSB significantly increased microbial biomass and N and P accumulation in plant tissues (Barea et al., 2002a, b). Mycorrhizae increased nitrogen nutrition in plant by facilitating the use of nitrogen forms that are difficult for mycorrhizal plants to exploit. Many ryhizobium strains improve processes involved in AM formation (mycelia growth, spore germination) (Barea, 1997).


The authors are grateful to Prof Dr. Lynette Abbott (University Of Western Ausralia), for her notes and ideas presented here.


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