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The multifunctional role of ectomycorrhizal associations in forest ecosystem processes.


Fungi are achlorophyllous, spore bearing, non vascular organism, which reproduce both sexually and asexually and whose filamentous and much branched plant body (mycelium) is surrounded by cell wall made of chitin or fungus cellulose or both. Fungi play a central role in many microbiological and ecological processes influencing soil fertility, decomposition, cycling of minerals, and organic matter, as well as plant health and nutrition. Fungi are heterotrophs requiring external sources of carbon for energy and cellular synthesis and they have adapted three different modes of nutrition to obtain this carbon, occurring as saprotrophs, necrotrophs and biotrophs. Mycorrhizal symbiosis is the most ancient, widespread form of fungal symbiosis with plants and without mycorrhizal fungi land colonization by plants would probably not have been possible. When moving from the aquatic to the aerial habitat, phototrophs faced considerable difficulties, among them the limited water supply and the scarcity of soluble minerals, especially P. The photosynthesizing organisms overcame these difficulties by forming mutualistic associations with fungi, called mycorrhizas. The name mycorrhiza, a Greek word meaning "fungus root", was introduced by Frank (1885) to describe the symbiotic association of plant roots and fungi. About the same time in 1886, Hartig described this association as purely parasitic and Stahl et al. (1990) reported that mycorrhizas were a manifestation of nutrient deficient soils. Smith and Read (1997) defined mycorrhizal associations as living together of two or more organisms. Allen (1991) defined a mycorrhiza as "a mutualistic symbiosis between plant and fungus localized in a root or root-like structure in which energy moves primarily from plant to fungus and inorganic resources move from fungus to plant". Frank (1885) distinguished two main types of mycorrhiza: ectotrophic and endotrophic. On morphoanatomical basis, mycorrhizas are categorised into three different groups, namely ectomycorrhiza, endomycorrhiza and ectendomycorrhiza. Brundrett (2004) and Finlay (2008) categorized mycorrhizas into seven main groups according to their morphology and on the basis of the fungal and plant taxa forming the symbiosis. These are ectomycorrhiza, endomycorrhiza, ectendomycorrhiza, orehidaceous, ericaceous, arbutoid and monotropoid mycorrhizas.

Of these mycorrhizal types ectomycorrhizal fungi often are considered an ecological guild distinguished by their stable biotropic association with the roots of woody plants and production of macroscopic sporocarps (Luoma et al. 1991). Globally, as many as 7-10 000 fungal species and 8000 plant species are involved in this symbiosis (Taylor and Alexander, 2005). Ectomycorrhizas are almost invariably characterized by a Hartig net composed of highly branched hyphae which entirely surround the outer root cortical cells. On the outside of the root these fungal hyphae aggregate to form a sheath (also named fungal mantle) from which emanate extraradical hyphae which explore the soil. The Hartig net is the place of massive bidirectional exchanges of nutrients between the host and the fungus. While the host plant allocates a significant amount of its photosynthates (Smith and Read, 1997) to the fungal symbionts to support almost entirely their metabolism, growth and formation of their fruit bodies, the ECM fungi transfer essential nutrients (mainly N, P and K) to the host. It is now widely acknowledged that, at least in temperate and boreal ecosystems, ECM fungi play a major role in the biogeochemical cycles and short cut mineralization processes by making directly available to their host plants complex forms of nitrogen and phosphorus (such as proteins, nucleic acids) at a very early stage of organic matter decomposition (Read and Perez-Moreno, 2003).

ECM fungi are particularly essential to the health and growth of forest trees. They can benefit forest trees in a number of ways although the most important is enhancing soil nutrient uptake, particularly for elements with a low mobility in the soil, such as P and micronutrients (Smith and Read, 2008) and also for N (Chalot and Bran, 1998). The other benefits that fungi provide include protection against pathogens (Perrin and Garbaye, 1983), tolerance to heavy metals (Jones and Hutchinson, 1986), and improvement in soil structure (Borchers and Perry, 1992). The fungi benefit by receiving 30-60 % of the net photosynthate produced by the host (Simard et al. 1997a). Fungal mycelia also provide an avenue for translocation of significant amounts of carbon among hosts of the same and different species (Simard et al. 1997a, 1997b). It is likely that carbon translocation benefits understory seedlings during establishment and may affect interspecific and intraspecific competition (Perry et al. 1992). Ectomycorrhizal fungi also provide a major link between carbon fixed by primary producers and other trophic levels in an ecosystem. For example, several rodent species rely on ECM sporocarps for 90 % of their diet (Hayes et al. 1986). Bacteria, arthropods, and other species of fungi also use or depend on ECM sporocarps as a source of food and perhaps micronutrients.

It is now widely recognized that the ectomycorrhizosphere, which forms a very specific interface between the soil and the trees, hosts a large and diverse community of micro-organisms (fungi and bacteria) that can inhibit or stimulate each other. Some of the ectomycorrhizosphere bacteria consistently promote mycorrhizal development, these are known as 'mycorrhizal' helper bacteria (MHBs) (Frey-Klett and Garbaye, 2005). ECM fungi and bacteria also jointly contribute to weathering and solubilisation processes (Calvaruso et al. 2006; Uroz et al. 2009). Many field observations suggest that ectomycorrhizal fungi and their associated bacteria contribute to a number of key ecosystem functions, such as carbon cycling, nutrient mobilization from soil organic matter, nutrient mobilization from soil minerals, and linking trees through common mycorrhizal networks. Their role is particularly crucial in performing two types of functions in which the fungal partner is complementary to the photosynthetic plant, (a) mobilizing nutrients by degrading organic matter and weathering minerals, and (b) coupling the autotrophie and heterotrophic cycles of C. The latter role is specific to the symbiotic nature of ECMs, in that the fungi associated with the fine roots can sometimes acquire C from the soil through enzymatic breakdown of organic matter as well as from the tree photosynthates (Courty et al. 2010). Finlay (2008) reported the new multifunctional perspective of mycorrhizas that includes mobilisation of N and P from organic polymers, possible release of nutrients from mineral particles or rock surfaces via weathering, effects on carbon cycling, interactions with mycoheterotrophic plants, mediation of plant responses to stress factors, such as drought, soil acidification, toxic metals and plant pathogens, as well as a range of possible interactions with groups of other soil microorganisms.

Here, in this review we have summarized the role of ECM communities in (1) C cycling, (2) nutrient mobilization from soil organic matter, (3) nutrient mobilization from soil minerals, (4) interaction of ECM fungi with soil organisms (5) stress amelioration (6) bioremediation and (7) regeneration of forest ecosystems (Fig. 1). This new knowledge will be put in perspective within the concepts of functional ecology as well as their implications in sustainable forest management.

Carbon Cycling

Ectomycorrhizal fungi play a major role in plant carbon input to soils and are primarily considered vectors for plant C input to soils. However, there is accumulating evidence that ectomycorrhizal fungi may also contribute to the direct loss of soil C by acting as decomposers, that is by producing extracellular lytic enzymes and metabolizing soil C (Talbot et al. 2008). The two major sources of C potentially available for ECM fungi are photosynthates from tree hosts and soil organic matter (SOM). Sucrose is transported from the leaves to the roots through the phloem vessels. Soil C is sequestered in various compounds like carbohydrates, proteins, nucleic acids, chitin, fatty acids or complex phenolic molecules, such as lignin.


Plant Hosts as a Source of Carbon for Ectomycorrhizal Fungi

ECM fungi mostly depend on their hosts for C supply. The transfer of C from the host tree to the fungal symbiont encompasses two steps, namely C exchange at the root-fungus interface and allocation from intra-to extraradical mycelium (Leake et al. 2001). Fitter et al. (1998), Robinson and Fitter (1999) suggested that carbon is allocated between the intraradical and extraradical mycelia according to the C-demand of the fungus rather than according to the C-demand of the autotrophic host. Nehls and Hampp (2000), Soderstrom (2002) and Hobble (2006) suggested that as much as 30 % of the total photoassimilate production is transferred to the fungal partner. Finlay and Read (1986), by using 14CO2 reported that carbon can flow from plant to plant through the mycelial systems. Simard et al. (1997a) investigated carbon transfer between tree species known to be interconnected by a number of shared mycorrhizal symbionts and by using [sup.13]C and [sup.14]C isotopes of carbon reported bidirectional movement of carbon from plant to plant. Sucrose is the major transport form of photoassimilates in forest trees and it is hydrolysed to glucose and fructose by plant derived cell wall bound acid invertases at the root-fungus interface, the monosaccharides produced are then taken up by both the fungal partner and root cortical cells (Nehls and Hampp, 2000). Fungal hexose transporters allow the transfer of glucose and fructose to the fungus and enable its growth (Nehls et al. 2001a b; Nehls and Hampp, 2000). Nehls and Hampp (2000) reported that in Amanita muscaria the expression of monosaccharide transporter was enhanced 4-6 fold in ectomycorrhizas compared to soil growing hyphae. The fungus also generated a gradient by converting glucose and fructose into compounds that are not used by the plant host (Hampp and Schaeffer, 1999), such as mannitol, arabitol, glycerol and non-reducing saccharides, such as trehalose, which are the main soluble carbohydrates found in ECM fungi (Martin et al. 1998). In fungi trehalose and mannitol play the role of reserve carbohydrates and osmoprotectants (Shi et al. 2002). They are also exuded into the soil and have been reported to contribute in selecting particular bacterial populations in the ectomycorrhizosphere (Frey-Klett et al. 2005). The proportion of fungal biomass in ECM fine roots ranges between 10 % and 40 % (Kinoshita et al. 2007). This proportion depends on the C allocated by the plant to the fungus and on the specific carbohydrate requirements of both partners (Hobbie, 2006; Hobbie and Hobbie, 2006). At the scale of a forest, the ECM fungal biomass (including the ECM mantle) can reach up to 5,000 kg [ha.sup.-1] (Nilsson et al. 2005). Hogberg and Hogberg (2002) suggested that ECM fungal biomass represents one-third of total soil microbial biomass in coniferous forests. Leake et al. (2004) and Wallander (2006) in their studies reported 10 mm growth rates per day of ECM extraradical mycelium. Querejeta et al. (2007) suggested that maximum growth of ECM extraradical mycelium occurred near the soil surface, and contributes to the formation of fruiting bodies (Hogberg et al. 1999). Hogberg et al. (2001) and Kuikka et al. (2003) observed that production of fruiting bodies depended on the photosynthetic rate of the trees as they are connected to the roots through the extraradical mycelium. These studies indicate that ectomycorrhizal fungi depend on their host trees for carbon supply.

Ectomycorrhizal fungi contribute 25 % of C[O.sub.2] efflux from the soil through respiration (up to 35 % during the period of fruiting body formation) and 15 % C[O.sub.2] efflux from the respiration of root tissues (Heinemeyer et al. 2007). ECM respiration, which mostly depends on the host tree, fungal species involved in symbiosis and N availability, corresponds to 3.5-15 % of the total photosynthates (Heinemeyer et al. 2006). These studies have shown that mycorrhizal fungi receive a significant proportion of carbon from their hosts and mostly depend on their hosts for carbon supply.

Soil Organic Matter as Source of Carbon for Ectomycorrhizal Fungi

Soil organic matter is also good source of carbon for ECM fungi and their associated host trees. Dead ectomycorrhizal sporocarps and mycelia are an important source of carbon and SOM to their associated host trees and ecosystems. Ectomycorrhizal fine roots decompose and degrade more slowly than non-mycorrhizal ones (Langley et al. 2006; Millard et al. 2007). Mycorrhizal fungi also decompose soil organic carbon as an alternate C source when supplies of photosynthates from host plant are low or unavailable. Several studies of temperate forests demonstrated that ectomycorrhizal fungi produce high extracellular enzyme activity during the winter months when photosynthetic rates decline indicating that these fungi supply carbon to host plants during these months (Buee et al. 2007; Mosca et al. 2007). Courty et al. (2007) also found that ectomycorrhizal root tips in an old-growth oak forest produce a suite of extracellular enzymes in early spring that show peak activity immediately before and following bud break. As bud burst is a strong C sink, these observations show that ectomycorrhizal fungi facilitate the formation of new tissues during this time by supplying C to their host plants (Courty et al. 2007). Mosca et al. (2007) showed that tree thinning led to significantly higher laccase, chitinase, and glucosidase production by ectomycorrhizal root tips in a declining European oak forest. Plant allocation of photosynthates to ectomycorrhizal fungi could also decline if soil nutrient availability is high enough to preclude the need for mycorrhizal fungi to facilitate nutrient acquisition by the plant. Soils with high N availability have low colonization of roots by mycorrhizal fungi (Treseder, 2004) suggesting that plant allocation to mycorrhizal fungi is potentially a risk in fertile soils, such as in agriculture systems. Treseder et al. (2005) reported that ECM fungi can also use part of carbon directly from soil organic matter. For instance, by using [sup.13]C Hobbie and Hobbie (2006) have shown that soil C may contribute as much as 43 % to total C in fruiting bodies of ECM fungi. Durall et al. (1994) using [sup.14]C labelling demonstrated that ECMs formed by different fungal species displayed different abilities to respire carbon from hemicellulose, cellulose, humic polymers or conifer needles. Ectomycorrhizal and ericoid mycorrhizal fungi can produce extracellular enzymes that decompose components of each of the major classes of organic compounds commonly found in soils (Table 1). The ability of these fungi to decompose cellulose, hemicellulose, and polyphenols is particularly important, since these are the three most abundant classes of biopolymers on land (Kogel-Knabner 2002). Production of extracellular lytic enzymes enables ectomycorrhizal fungi to mobilize nutrients from leaf litter (Bending & Read 1995) and pollen (Perez- Moreno & Read 2001). The ability of ectomycorrhizal fungi to decompose these organic substrates, which are major components of fresh organic matter in soils, implies that they could control the loss of large portions of soil C stocks. This is not surprising because ECM fungi have evolved from saprotrophic ancestors on several independent occasions (Hibbett et al. 2000). This is well illustrated by the presence of a broad range of genes coding for enzyme degrading complex organic compounds (i.e. lignin peroxidases, manganese peroxidases, laccases, tyrosinases) in basidiomycetous clades (Luis et al. 2005; Bodeker et al. 2009). However, the diversity of these genes is lower than in exclusive saprotrophic species. Some species, such as Laccaria bicolor and Amanita bisporigera are even deprived of genes coding cellulose and hemicellulose degrading hydrolytic enzymes and are also reduced in polyphenol degrading enzymes (Martin et al. 2008; Nagendran et al. 2009). Bending and Read (1995) and Gramms et al. (1998) in their studies suggested that many ECM fungi possess extracellular oxidative and cellulolytic activities but these are marginal compared with those of litter decomposing fungi as reported by Koide et al. 2008. Courty et al. (2005, 2006) and Buee et al. (2007), by using enzyme measurement activities of individual ECM tips, revealed variable laccase, [beta]-glucosidase and cellobiohydrolase activities depending on the fungal species.

Field-based studies have also indicated that ectomycorrhizal fungi may decompose soil organic matter via the production of extracellular enzymes. For instance, activities of proteases and polyphenol oxidases are often higher in ectomycorrhizal mats than in nearby uncolonized soils (Griffiths & Robinson 1992). Through the production of these extracellular enzymes, ectomycorrhizal fungi should accelerate decomposition of both labile (via proteases) and recalcitrant (via polyphenol oxidases) soil organic matter. Two studies using natural [sup.14]C signatures in ectomycorrhizal sporocarps have also provided indirect evidence that ectomycorrhizal fungi may metabolize soil-derived C (Hobbie et al. 2002). In each study, the [DELTA] [sup.14]C of sporocarps matched the atmospheric [DELTA] [sup.14]C of the previous year, suggesting that at least a portion of sporocarp biomass was derived from litter or soil C. Treseder, et al. (2006) found that ectomycorrhizal root tips did not accumulate C from [sup.14]C-labelled leaf litter in a temperate deciduous forest of the eastern US. These results suggested that ectomycorrhizal fungi do not use litter C as a significant C source. However, it is possible that any [sup.14]C acquired from the litter was respired in the mycorrhizal mycelium soon after uptake. Alternatively, ectomycorrhizal fungi might acquire C from soil organic matter rather than leaf litter. In a boreal forest study in central Sweden, Lindahl et al. (2007) observed that ectomycorrhizal taxa colonized primarily the fragmented litter and lower soil layers. Mycorrhizal fungi were spatially separated from saprotrophs, which almost exclusively occupied the upper fresh and partially decomposed litter layers (Lindahl et al. 2007). Moreover, ectomycorrhizal abundance was positively correlated with increasing soil C: N with organic matter depth and age (Lindahl et al. 2007), indicating that mycorrhizal fungi may mobilize N-rich compounds from organic matter in these soils (Hobbie & Horton 2007). Courty et al. (2007) suggested that under certain conditions, some ECM fungal symbionts behave as saprobes, using litter and soil organic matter as substrates and providing the host trees with carbon at time when demand is high and photoassimilates are not yet available. From these studies it is clear that mycorrhizal fungi that have decomposer abilities could acquire C from other sources apart from host carbohydrates, such as soil organic compounds. These compounds could be metabolized directly from labile pools present in soil solution, or acquired by enzymatic decomposition of complex soil organic matter. So these fungi have the potential to supply carbon to their plant hosts when they are in need of it.

ERM, Ericoid Myeorrhizal Fungi; ECM, Ectomycorrhizal Fungi

Mobilization and Uptake of Mineral Nutrients

ECM fungi are predominant in boreal ecosystems, where N and P are sequestered in organic forms that are not readily available to autotrophs and hence the dominant plant species are highly dependent on ectomycorrhizal symbionts for their nutrient supply and ECM fungi are known to produce a wide range of extracellular and cell wall bound hydrolytic and oxidative enzymes which degrade N and P- compounds contained in SOM, and more particularly in proteins, ligno-cellulose and polyphenol-protein complexes (Burke and Cairney, 2002; Leake et al. 2002). Lindahl et al. (2005) reviewed enzymatic activities of ectomycorrhizal mycelia and concluded that wider recognition of the ability of many mycorrhizal fungi to mobilize nutrients from complex organic sources is a necessary step in the further development of nutrient cycling models, particularly in ecosystems with low nutrient availability. Abuzinadah and Read (1986) suggested that the ability of ectomycorrhizal fungi to utilize organic forms of N would restrict losses to decomposer populations and lead to tighter nutrient cycling. Bending and Read (1995) were able to show mobilization of N from patches of organic material from the fermentation horizon of a pine forest soil by mycelia of the ectomycorrhizal fungus Suillus bovinus. Courty et al. (2005) studied laccase and phosphatase activities of the dominant ectomycorrhizal fungi in an oak forest and reported that Lactarius quietus and Cortinarius anomalus showed peak of laccase activity in spring, while those of Xerocomus ehrysenteron showed highest laccase activity in summer and autumn. Ramesh et al. (2008) studied enhancement of laccase in ectomycorrhizal fungus Hebeloma cylindrosporum in presence of different substrates and reported that lignocellulosic substrates, such as apple scrapings and pine needles induced laccase activity in the ECM fungus suggesting that laccase gene has an important role in nutrient mobilization. These fungal enzymatic activities play an important role in the dynamics of geochemical cycles and in mobilizing and transferring nutrients from SOM to forest trees.

The N organic compounds from humified material, plant litter or dead microbial cells, range from simple amino acids, amino sugars and nucleotides to chitin and polypeptides complexed with polyphenols (Lindahl and Taylor, 2004; Nygren et al. 2007). ECM fungi are able to utilize a wide range of amino acids and a large proportion of the assimilated N is transferred to the host plants by ECM fungi (Plassard et al. 2000; Taylor et al. 2004). Ectomycorrhizal fungi are known to produce a wide range of protein degrading enzymes and numerous studies, therefore, have focussed on the production of these extracellular proteases by ECM fungi (Nehls et al. 2001b; Nygren et al. 2007). Protease activity has usually been inferred from the ability of ECM fungi to grow in pure culture with protein as a sole N source (Lilleskov et al. 2002). Protease production can also be quantified by using fluorescent substrates, such as Fitc-BSA (Tibbett et al. 1999). Zhu et al. (1990) found a protease of unknown grouping in Hebeloma crustufiniforme with a molecular weight of 37.8 kDa that was stable at a pH between 2.0 and 5.0. Nehls et al. (2001b) found two proteases (45 kDa and 90 kDa) excreted by Amanita muscaria with pH optima at 3 and between 3 and 5.5, respectively. In addition, they determined the sequence for the 45 kDa protease and found that it was very similar to aspartic proteases of other fungal species. Under natural conditions, the proteolytic enzyme production is repressed or induced by many environmental factors. The repression of extracellular protease production by ammonium has been found in many fungi, particularly in Hebeloma crustuliniforme (Zhu et al. 1994). In forest soils this variability of extracellular N-mobilizing enzyme production can reflect the adaptation to high or low inorganic N-availability. Lilleskov et al. (2002) suggested that fungi colonizing sites containing high available inorganic N (nitrate or ammonium) may be less likely to use complex organic forms of N, such as protein. The secretion of protease is also regulated by pH, as demonstrated for two aspartic proteases from Amanita muscaria (Nehls et al. 2001b). Moreover, direct effect of pH and temperature on protease activity have been reported in the secreted enzyme fraction of birch roots colonized by Paxillus inovolutus (Bending and Read, 1995) or of the mycelium of Hebeloma sp. in pure culture (Tibbett et al. 1999).

ECM fungi are known to enhance the uptake of essential nutrients particularly of elements with low mobility in the soil, such as phosphorus and micronutrients (Smith and Read, 2008), and also for N (Chalot and Bran, 1998) besides water (Jones et al. 1991). They enhance uptake and mobilization of P by production of various P degrading enzymes. Bougher et al. (1990) studied growth and phosphorus acquisition of Eucalyptus diversicolor F. Muell. seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply. The authors reported that all four ECM fungi studied i.e. Pisolithus tinctorius, two isolates of Descolea maculate and Laccaria laccata increased the P content of plant tissues at sub-optimal levels of P supply. Most of the total P in forest soils is found in complex molecules, such as inositol phosphate, nucleotides and phospholipids (Criquet et al. 2004). Orthophosphate ions, the sole form of P taken up by micro-organisms and plants (Rao et al. 1996), are released into the soil solution as a result of phosphate activities. Phosphatases are classified in different groups, including phosphomonoesterases which have been extensively studied in soil litter (Turner et al. 2002) and ECM fungi (Bure et al. 2005). Phosphomonoesterases are the enzymes primarily responsible for degradation of the organic P resources in soils (Bums and Dick, 2002). These enzymes cleave phosphate-ester bonds to release inorganic P from a range of substrates, such as inositol phosphate, polyphosphates and phosphorylated sugars (Tibbett et al. 1998a). The ability of ECM fungi to produce phosphomonoesterase has been investigated in fungal isolates that are easily grown in culture. In addition to phosphomonoesterases, some mycorrhizal fungi have also been shown to produce phosphodiesterases (Leake and Miles, 1996). Phosphodiesterases have a very low persistence in soil, rarely exceeding 1% of the total P (Paul and Clark, 1989). A number of studies have demonstrated the regulation of these extracellular and surface-bound phosphatases by inorganic P (pi) is pure fungal culture (Tibbett et al., 1998b). These studies have supported the hypothesis of the active role and ecological importance of ECM fungal hyphae and mycorrhizas in the acquisition of P under conditions of P deficiency.

With regard to N mobilization, up to now, only a small number of ECM fungal species (around 50) have been studied for their capacities to mobilize organic N (Nygren et al. 2007) but significant variability in their proteolytic abilities has been demonstrated (Lilleskov et al. 2002; Nygren et al. 2007). He et al. (2004) studied reciprocal N ([sup.15]N[H.sub.4.sup.+] or [sup.15]N[O.sub.3.sup.-]) transfer between non-[N.sub.2]fixing Eucalyptus maculata and [N.sub.2]-fixing Casuarina cunninghamiana linked by the ectomycorrhizal fungus Pisolithus sp. and observed that the amount and direction of two-way mycorrhiza-mediated N transfer was increased by the presence of Pisolithus sp. and Frankia, resulting in a net N transfer from low N-demanding Eucalyptus to high N-demanding Casuarina. Lindah et al. (2007) studied spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest and reported that saprotrophic fungi were primarily confined to relatively recently (< 4 yr) shed litter components on the surface of the forest floor, where organic carbon was mineralized while nitrogen was retained a Mycorrhizal fungi dominated in the underlying, more decomposed litter and humus, where they apparently mobilized N and made it available to their host plants. These authors observed that the degrading and nutrient-mobilizing components of the fungal community were spatially separated. Colpaert and van Tichelen, (1996) reported that saprotrophic fungi were more efficient than mycorrhizal fungi in colonizing and utilizing fresh, energy-rich litter. Martin et al. (1986) suggested that fungi utilized a combination of glutamate dehydrogenase and glutamine synthase pathways to assimilate N which was then transported to the plant in the form of glutamine or glutamate. Finlay et al. (1988) used [sup.15]N-labelled ammonium to follow the N uptake and assimilation by Rhizopogon roseolus, Suillus bovines, Pisolithus tinctorius and Paxillus involutus associated with Pinus sylvestris and found that glutamine/glutamic acid, alanine and aspartate/asparagines were important nitrogen sinks and that amino acids were used for N storage. These studies suggest that mycorrhizal fungi enhance uptake and mobilization of N from one host plant to another and from soil organic matter to plant hosts.

Weathering and Dissolution of Minerals

Ectomycorrhizal fungi benefit their associated host trees by enhancing mobilization of nutrients. ECM fungi mobilize nutrients from minerals by dissolution of soil mineral particles and most of the inorganic ions taken up by ECM fungi (P[O.sub.4.sup.3-], [Ca.sup.2+], [Mg.sup.2+], [Fe.sup.3+], [K.sup.+]) came from the dissolution of soil mineral particles, such as apatite, feldspars, micas and hornblendes (Landeweert et al. 2001). The ability of the ECM fungi to dissolve minerals has been reported for identified and unidentified isolates in pure culture (Mahmood et al. 2001) as well as for ECM colonized tree seedlings. The transformation of chlorite and mica into clay minerals, as well as the dissolution of apatite, was reported for seedlings infected with Piloderma croceum and Suillus variegates, respectively (Arocena et al. 2004). Van Scholl et al. (2006) suggested that the ECM fungus Paxillus involutus significantly contributed to the dissolution of potassium-containing mineral muscovite and increased root potassium contents in tree seedlings. ECM fungi associated with seedlings have also been shown to recover phosphorus from apatite (Wallander et al. 2002) and potassium from biotite and microcline (Wallander and Wickman, 1999). Blum et al. (2002) suggested that in base-poor forest ecosystems a large part of calcium used by the trees was mobilized from apatite by ECM fungi and demonstrated the relevance of fungal weathering to plant nutrition as calcium obtained from calcium phosphate (apatite) was used mostly by ECM trees, indicating a direct transfer of calcium from fungus to plant. Another manifestation of fungal mineral dissolution could be the formation of smooth tunnels of constant diameter in feldspar and hornblende grains (Hoffland et al. 2002). The authors proposed that ECM hyphae were involved in mineral dissolution because feldspar tunnel density was positively correlated with ECM density. Van Breeman et al. (2000) found strong evidence indicating that ECM fungi, namely Piloderma croceum, Cenoeoccum geophilum and Suillus bovines were responsible for micro-penetrations into feldspar rock. These studies suggest that ECM fungi have significant role in mobilization of nutrients from soil mineral particles to their associated host trees.

The ECM fungi release elements stored in mineral particles through complexolysis and acidolysis as these are not readily available for micro-organisms. Many authors like Ochs (1996), Ahonen-Jonnarth et al. (2000) suggested that organic acids of low molecular weight are the main agents of mineral dissolution, because of their dual acidifying and complexing properties. Oxalate is one of the most widespread and abundant organic acids in forest soils (Jones et al. 2003a), and it increases the dissolution of common soil minerals, such as apatite (Wallander, 2000a; Wallander et al. 2003), biotite (Wallander, 2000b), phlogopite (Paris et al. 1996) and microcline (Wallander and Wickman, 1999). The secretion of oxalate has been reported for various ECM species, such as Cenococcum geophilum and Pisolithus sp. (Yuan et al. 2004), Cortinarius glaucopus (Rosling and Finlay, 2005), Hebeloma longicaudum (Van Scholl et al. 2006), Paxillus involums (Arvieu et al. 2003; Rosling and Finlay 2005 and Wallander and Wickman 1999), Piloderma eroeeum and Tylosphora fibrillosa, (Mahmood et al. 2001), Pisolithus tinetorius (Jayakumar and Tan, 2005), Scleroderma verrucosum (Machuca et al. 2007), Rhizopogon roseolus and Suillus eollinitus (Arvieu et al. 2003), Suillus granulatus and Thelephora terrestris (Wallander et al. 2003). Jones et al. (2003a) revealed that most ECM fungi produced oxalate in concentrations ranging from 10 to 100 [micro]M; values in accordance with the oxalate concentrations measured in soil solutions. Wallander and Wickman (1999), van Hees et al. (2003), Tahara et al. (2005) and Machuca et al. (2007) reported that Paxillus involutus, Suillus sp., Pisolithus tinctorius, and Scleroderma verrucosum produce a wide range of low molecular weight organic acids, such as citrate, formate, malate, malonate or succinate which can also act as mineral complexing agents.

For the mobilization of ferric ion ([Fe.sup.3+]) which is essential for various cell processes, such as respiration, DNA synthesis, metabolism and is also an essential cofactor for catalases, cytochromes and peroxidases it has been observed that fungi and many bacteria bring about a specialized type of complexation by siderophores (Neilands, 1995). Most of the soil ferric iron ([Fe.sup.3+]) is complexed in mineral particles. Fungi and in particular ECM, mobilize Fe by means of siderophores belonging to the hydroxamate family (Machuca et al. 2007). Siderophore production by ECM fungi has been reported for mycelia and ECM tips of a number of species (Machuca et al. 2007; Rineau et al. 2008). Siderophores have very high affinity constants for iron, but they are produced in very small amounts by ECMs. Ferricrocin, a hydroxamate siderophore has been shown to be produced in very low concentrations by Cenococcum geophilum and Hebeloma crusmliniforme (van Hees et al. 2006). Similarly, nanomolar concentratins of two siderophores, ferrichrome and ferricrocin were assumed to be produced by unidentified ECM species in the upper layers of forest soils (Essen et al. 2006).

Many bacterial communities also remain associated with ectomycorrhizal fungi (Frey-Klett et al. 2005; Uroz et al. 2007) suggesting that they might have effect on the functioning of ECMs. Frey-Klett et al. (2005), while studying Douglas fir-Laccaria bicolor mycorrhizosphere, suggested that the proportion of isolates able to mobilize iron or to solubilize phosphorous from inorganic stocks was significantly higher in the mycorrhizosphere than in the bulk soil. Calvaruso et al. (2007) and Uroz et al. (2007) obtained similar results while working with Scleroderma citrinum mycorrhizosphere. These findings suggest that the associated mycorrhizal bacteria have effect on functioning of mycorrhizal fungi.

The most efficient bacteria frequently found in ectomycorrhizosphere identified so far belong to Burkholderia and Collimona genera (Barbieri et al. 2007; Offre et al. 2007). Bacteria from the Burkholderia genus are known for their ability to solubilise inorganic phosphate (Lin et al. 2006). Recent studies have also reported their ability to weather complex minerals and rocks, such as biotite, basalt or granite (Uroz et al. 2007; Wu et al. 2008). Calvaruso et al. (2006) studied the effects of Burkholderia from the ectomycorrhizosphere on mineral weathering in an experiment with pine seedlings grown on a mixture of biotite and quartz. These authors also reported that inoculation of selected Burkholderia strains significantly enhanced the release of potassium from biotite by a factor of 1.5 when compared to non-inoculated plants. Moreover, the bacterium only significantly increased seedling growth under nutrient poor conditions suggesting that this bacterial strain promoted plant growth by releasing inorganic nutrients from the mineral. Leyval et al. (1989) studied the interaction between Laccaria laccata, Agrobacterium radiobacter and beech roots and reported that ECM fungi with associated bacterium enhanced the release and mobilization of P, K, Mg, and Fe from minerals and also enhanced plant growth. Similar results were obtained with rhizospheric bacteria by Toro et al. (1997) who used labelled phosphate and highlighted the importance of the interactions between mineral weathering bacteria and mycorrhizal fungi in mobilizing phosphorus. As in the case of fungi, the main mechanisms used by bacteria to weather minerals under aerobic conditions are acidification and chelation due to production of protons, organic acids and siderophores. Uroz et al. (2007) demonstrated that the most efficient mycorrhizosphere bacterial isolates were capable of lowering the pH of the medium from 6.5 to 3 and to induce the release of ca. 2 mg [L.sup.-1] of iron from biotite. They also pointed out that mineral weathering ability of bacteria was linked to their metabolism as bacteria were very efficient when glucose was supplied to the cultural medium. A strong reduction of weathering ability was observed when mannitol, a sugar alcohol frequently present in plants, algae or fungi, was used (Uroz et al. 2007). Variations in mineral weathering efficiency were also observed for non-mycorrhizosphere bacteria using xylose or lactose as a growth substrate (Hameeda et al. 2006). The ability to dissolve minerals can also be modified by supplying nitrate or ammonium (Nautiyal et al. 2000). These observations suggest that mineral weathering ability of the ectomycorrhiza-associated bacteria was strongly dependant on the carbon and nitrogen sources available in their environment.

Interaction with Other Soil Micro-organisms

In addition to increasing the absorptive surface area of their host plant root systems, the hyphae of symbiotic fungi provide an increased surface area for interactions with other micro-organisms, and provide an important pathway for the translocation of energy-rich plant assimilates (products of photosynthesis) to the soil. The interactions may be synergistic, competitive or antagonistic and may have applied significance in areas, such as sustainable agriculture (Johansson et al. 2004), biological control or bioremediation. Olsson et al. (1996) found inhibitory effects of about 20-50 % on bacterial activity in presence of ECM fungi, such as Paxillus involutus, Laccaria bicolor, Thelephora terrestris, Laccaria proxima, Suillus variegatus and Hebeloma crustuliniforme. Bacterial activity was recorded by measuring the incorporation of thymidine. Reduced uptake was probably a result of fungal antibiotic production and competition for limited nutrient resources (Cairney and Meharg, 2002). Contrastingly, Olsson and Wallander (1998) demonstrated stimulatory effects of Suillus variegatus on bacterial activity with amended soil containing biotite nutrient additions. The resultant stimulation/inhibition of bacterial activity as a direct consequence of the nutrient content of the soil supports the argument for potential competition for resources. Olsson and Wallander (1998) also noted effects of ECM fungi on the community structure of the bacteria in close proximity to the host plant roots. To identify the bacteria associated with ECM fungi, Bowen and Theodorou (1979) cultured the isolates from roots of Pinus radiata. These included three Pseudomonas-type and four Bacillus species. The study found a reduction of ECM colonisation of about 42-100 % in presence of these bacteria. Alternatively, the co-existence of some associated bacteria, known as mycorrhizal 'helper' bacteria, is thought to be beneficial. The review by Garbaye (1994), suggested that mycorrhizal helper bacteria stimulate ECM fungal germination and enhance ECM formation. Mycorrhizal helper bacteria are also thought to enhance the breakdown of organic nutrients by secreting digestive acids and oxalates, breaking down organic N and C in the soil (Garbaye, 1994).

Bacteria have also been identified as possible components of mineral rock weathering associated with ECM (Van Breeman et al. 2000). Lehr et al. (2007) reported suppression of plant defence response by a mycorrhizal helper bacterium. Gadgil and Gadgil (1975) highlighted the importance of the existence of both mycorrhizal and saprotrophic fungi in forest biomes. They demonstrated that there was a decrease in litter decomposition when both trophic groups were present and suggested that this was due to competitive antagonism. Leake et al. (2001), showed antagonistic interaction in microcosms between Phanerochaete velutina and Suillus bovinus and correlated the interaction with a reduced carbon pulse from the plant to the growing region of the mycelium. This implies a resultant dysfunctional ECM association where normal nutrient exchange is not occurring (Caimey and Meharg, 2002). Lindahl et al. (2001) showed competitive sequestration of phosphorus between a saprotroph, Hypholoma fasciculare and an ECM fungus, Suillus variegatus and concluded that the potential for either fungus to out-compete depended on the carbon source available to either competitor.

ECM fungi are also strong competitors of soil-borne root parasites. The antagonistic modes are both mechanical and biochemical. Marx (1973) suggested that the thick fungal mantle surrounding ECM roots presents an effective physical barrier to penetration by pathogens. Duchesne et al. (1988) observed that the presence of Paxillus involutus in the rhizosphere of Pinus resinosa significantly reduced pathogenicity of Fusarium oxysporum even without mycorrhiza formation. The biochemical mode involved antifungal compounds released by ECM fungi, as found by Kope et al. (1991) in Pisolithus arrhizus that suppressed pathogenic growth and sporulation. Chakravarty et al. (1991) and Farquhar and Peterson (1991) studied interactions between the ectomyeorrhizal fungus Paxillus involutus, damping off fungi Fusarium oxysporum and Pinus resinosa seedlings and observed significant reduction in the pathogenicity of Fusarium oxysporum in presence of Paxillus involutus. Branzanti et al. (1999) reported that the presence of Paxillus involutus, Laccaria sp., Hebeloma sp., in the rhizosphere of Castanea suppressed the chestnut ink disease caused by Phytopthora. Morin et al. (1999) observed that Paxillus sp. protected black spruce seedlings against Cylindrocladium root rot disease. Sen (2001) showed an inhibitory effect of Suillus bovinus in association with Pinus sylvestris against colonisation of pathogenic uninucleate Rhizoctonia species. The same inhibitory effects were not observed when the plant host was inoculated with Paxillus involutus and Wilcoxina mikolae, indicating differences between species in protecting host plants from pathogenic infection. Sen (2001) also found 16 species of Bacillus associated with Suillus bovinus, suggesting a combined effort of both bacteria and ECM fungi to protect the plant host. Maier et al. (2004) and Schrey et al. (2005) reported that Streptomyces sp. AcH 505 promotes the growth and mycorrhiza formation by symbiotic fungi Amanita muscaria and Suillus bovinus, but it is antagonistic against Heterobasidion annosum. Bianco-coletto and Giardino (1996) found antibiotic activity of Suillus bovinus against Bacillus cereus and Bacillus subtilis. Varese et al. (1996) found that 27 bacterial species were associated with Suillus grevillei sporocarps and ECM roots of Larix deciduas and observed that gram-positive bacteria seldom stimulated fungal growth, but among the gram-negative bacteria two Pseudomonas strains showed greatest enhancement of growth and Streptomyces always caused significant inhibition of the fungus. Stack and Sinclair (1975) reported that Laccaria laccata provided protection against Fusarium root rot on P. menziesii seedlings. Duponnois and Garbaye (1990), and Garbaye (1994) reported that inoculation of P. menziesii seedlings with Laccaria along with Pseudomonas species isolated from ECM often resulted in large increase in percent ECM colonization and in seedling growth. Frey et al. (1997) suggested that Laccaria bicolor exerted selection pressure for strains of bacteria that metabolise trehalose. Li and Castellano (1987) isolated nitrogen fixing Azospirillum species from sporocarps of Hebeloma crustuliniforme, Laccaria laccata and Rhizopogon vinicolor. Bacteria with the potential to fix nitrogen have been discovered growing endosymbiotically within tuberculate roots of ectomycorrhizal plants (Izumi et al. 2006). Obviously such tripartite symbioses would be of significance in nitrogen-limited environments. Endosymbiotic bacteria have been reported in both AM fungi (Jargeat et al. 2004) and the ectomycorrhizal fungus Laccaria bicolor (Bertaux et al. 2003). Exudation and reabsorption of fluid droplets at ectomycorrhizal hyphal tips was demonstrated by Sun et al. (1999) who concluded that it might represent an important mechanism for conditioning the hyphal environment in the vicinity of tips, creating an interface for the exchange of nutrients and carbon compounds with the adjacent soil environment and other micro-organisms.

Stress Amelioration

Ectomycorrhizal fungi have a range of effects which contribute to the amelioration of different types of stress experienced by their plant hosts, including metal toxicity, oxidative stress, water stress, and effects of soil acidification. These have recently been reviewed by Colpaert (2008) and Finlay (2008). Ectomycorrhizal fungi are known to protect host plants from heavy metals (Bellion et al. 2006). Field studies have shown that carpophores of ectomycorrhizal fungi are able to accumulate heavy metals in high concentrations, when these fungi are present in metal polluted sites (Ernst, 1985). Ectomycorrhizal fungi have been demonstrated to alleviate growth depressions of tree seedlings due to the toxic effects of A1 (Schier and McQuattie 1995, 1996), Ni (Jones and Hutchinson 1986), Zn (Brown and Wilkins 1985) and Cd (Jentschke et al. 1999). For other important heavy metals, for example Hg and Pb, direct evidence of amelioration by ectomycorrhizal fungi is still lacking. Many ectomycorrhizal fungi seem to be very suitable bioindicators of the disturbance of forest ectotrophic stability. Stages of this disturbance can be linked directly to particular phases of impoverishment of ectomycorrhizal mycocoenoses (Peskova, 2005).

The effects of mycorrhizal fungi on plant responses to drought stress have been examined by a number of workers (Smith and Read, 2008), but it is difficult to separate nutritional effects from direct effects on water transport since the hyphal contribution to nutrient uptake becomes more important as soil dries. Experiments by Querejeta et al. (2003), however, have shown nocturnal water translocation from plant roots to mycorrhizal fungi in association with hydraulic lift. Supply of water in this way would be an important way of maintaining mycorrhizal activity and improving nutrient uptake by deep-rooted plants, even when the fertile upper soil horizons were dry. The exudation of liquid droplets at ectomycorrhizal hyphal tips has also been discussed by Sun et al. (1999) who suggested that this helps to maintain better continuity between hyphal tips and the adjacent substrate, as well as more stable conditions for microbial interactions at this interface. Enhanced tolerance of AM plants to water deficit may involve modulation of drought-induced plant genes (Ruis-Lozano et al. 2006). Down-regulation of genes encoding plasma membrane aquaporins has been shown by Porcel et al. (2006) and this may play a role in the increased tolerance of AM plants to both water and salt stress.


Currently the most common practice of cleaning contaminated soil is to remove the soil from the site and transfer it to a permanent storage cell, or to an incinerator for combustion of organics. The use of microorganisms as bioremediation agents is gaining popularity based primarily on degradation studies conducted under laboratory conditions. Unfortunately these microorganisms are often not active degraders when moved from the laboratory to the field, presumably because they cannot compete with the native organisms. We are proposing the use of ectomycorrhizal fungi as bioremediation agents with special attention focused on both the fungus and the host plant. The host plant will give the fungus a selective advantage for surviving at a contaminated site. Several of these fungi are known to metabolize various chlorinated aromatic compounds, such as 2,4-dichlorophenoxyacetic acid (2,4-D), atrazine, and polychlorinated biphenyls (PCBs). This group of fungi may play an important role in the bioremediation of hazardous compounds in soil (Paula K. Donnelly and, John S. Fletcher). Meharg and Caimey (2000) reviewed possible ways in which ectomycorrhizal fungi might influence rhizosphere remediation of persistent organic pollutants (POPs). Many of the fungi screened for degradation of POPs, such as polyhalogenated biphenyls, polyaromatic hydrocarbons, chlorinated phenols, and pesticides are able to transform these compounds, but relatively few mycorrhizal taxa have been tested. Donelly et al. (1993) demonstrated degradation of two chlorinated aromatic herbicides (2, 4- dichlorophenoxyacetic acid and atrazine) by ericoid and ectomycorrhizal fungi. Meharg et al. (1997a) showed that degradation of 2, 4-dichlorophenol by the two ectomycorrhizal fungi, namely Paxillus involutus and Suillus variegatus was higher when the fungi were growing in symbiosis with Pinus sylvestris than when they were grown in pure culture. In other experiments (Meharg et al. 1997b), reported that S. variegatus had been shown to be effective in degrading 2, 4, 6-trinitrotoluene. A potential advantage of using mycorrhizal fungi in bioremediation is that they receive a direct supply of carbon from their plant hosts to support growth into contaminated substrates. Some of this carbon may subsequently be available to bacteria associated with the mycorrhizal mycelium (Sun et al. 1999) and this may have consequences for bioremediation in the mycorrhizosphere. Attempts to introduce microorganisms with biocontrol or bioremediation properties often fail because the inoculants fail to establish themselves. Sarand et al. (1998) observed that mycorrhizal hyphae were able to support microbial biofilms of catabolic plasmid ([Tol.sup.+]) harbouring bacteria which could be active in bioremediation of petroleum-contaminated soil. In subsequent experiments, these authors (Sarand et al. 2000) demonstrated that the number of [Tol.sup.+] bacteria was higher in mycorrhizospheric soil compared with bulk soil, and inoculation with bacteria had a positive effect on plant and fungal development. The presence of easily available plant-derived carbon sources did not impede the degradation of m-toluate by the bacteria (Sarand et al. 1999). However, in other experiments Genney et al. (2004) found that degradation of the polycyclic aromatic hydrocarbon fluorine was retarded in a Scots pine ectomycorrhizosphere. Joner et al. (2006) also demonstrated impeded phytoremediation of polycyclic aromatic hydrocarbons (PAHs) by the ectomycorrhizal mycelium of S. bovines that was attributed to nutrient depletion by the scavenging fungus.

Regeneration of Forest Ecosystems

The role of mycorrhizas in forest restoration has attracted lot of attention in recent past (Gaur and Adholeya, 2004; Hidelbrandt et al. 2007). It is because successful establishment of forest plants on reforestation sites often depends on mycorrhizal mutualism and on the ability of seedlings to capture site resources quickly during the early plantation establishment (van den Driessche, 1991; Dunabeitia et al. 2004). There are at least two mechanisms by which the mycorrhizas in plant roots promote forest restoration. First, as suggested by Galli et al. (1994), mycorrhizal colonization in roots plays a role in protecting the plant roots from various stresses, and the second, mycorrhizal colonization of roots increases root surface area for nutrient absorption. In fact, the extraradical mycelia of ECM fungi exploit the greater soil volume and can reach micropore areas and absorb nutrients that may otherwise be inaccessible to plants both physically and chemically (Perez-Moreno and Read, 2000).

Numerous studies have described the relationship between recovery of disturbed ecosystems and the ECM community. Byrd et al. (2000) noted an overall reduction of ECM species richness and significant changes in species composition after clear-cutting. Changes in ECM species composition after clear-cutting are influenced by the soil environment as well as by loss or change in fungal inoculum (Jones et al. 2003b). Dahlberg (2001) found a positive correlation among ECM mortality, increased burn intensity and tree mortality. Several studies have shown a short-term reduction in ECM sporocarp production or in numbers of live fine roots after clear cutting and burning (Pilz and Perry 1984; Herr et al. 1994), thinning and broadcast burning (Waters et al. 1994), burning alone (Stendell et al. 1999) or thinning alone (Gomez et al. 2003). Results suggested, however, that ECM community composition is not substantially altered by low intensity wildfires (Jonsson et al. 1999) or by restoration thinning and burning (Korb et al. 2003) if the organic layer remains relatively undamaged. In contrast, high-intensity natural or prescribed fire that severely burns the mineral soil (Feller 1998) significantly alters the ECM community (Dahlberg 2001).

Mycorrhizal inoculation is beneficial for reclamation of variety of disturbed sites (Danielson and Visser, 1989; Marx, 1991) and also has a great potential in the restoration of natural ecosystems (Miller and Jastrow, 1992). Successful revegetation and reclamation of severely disturbed mine lands in various parts of the world has been accomplished by using the biological tools (Malajczuk et al. 1994). These tools include phytobial remediation practices, which consist of planting seedlings inoculated with mycorrhizal fungi, nitrogen fixers, actinomycetes, and growth-promoting bacteria. Likewise, inoculation of nursery seedlings with appropriate mycorrhizal fungi is the most environment friendly approach, particularly, for disturbed ecosystem. This approach is known to promote uptake of nutrients and water, buffer against various stresses, and increase resistance against some pathogens, and considered essential to enhance seedling performance (Bois et al. 2005; Quoreshi et al. 2008). The lack of mycorrhizal associations on plant root systems is one of the major reasons for failure of plantation establishment and growth in various forests with low inoculum potential, mined sites, and highly disturbed areas. This is because ectomycorrhizal inoculum can persist for a short time after a disturbance as chlamydospores, sclerotia, on root tips of surviving trees, and, briefly, as hyphae emanating from dying or recently dead root tips. Without a host, however, the amount and diversity of ECM fungal inoculum decreases rapidly (Dahlberg, 2002; Jones et al. 2003a, b), with greater declines following more severe disturbances (Bradbury et al. 1998). Pre-treatment of both plants and soils are practices commonly used in programmes of revegetation and soil restoration (Alguacil et al. 2005, Caravaca et al. 2005).

The reduction in the inoculum of ECM fungi in the soil after disturbances severely compromises the natural regenerative ability of such degraded forests. Thus, role of ECM fungi assumes significance in forest restoration because these mutualists have the ability to provide buffering capacity to plant species against various environmental stresses (Malajczuk et al. 1994). Inoculation of plant stock destined for revegetation with selected bacterial or fungal strains has often demonstrated to improve its physiological quality and to ameliorate the survival and development of plants (Probanza et al. 2001; Medina et al. 2003). Pinus halepensis has been commonly used in afforestation programmes of degraded soils (Maestre and Cortina, 2004). Inoculation of Pinus halepensis with selected ECM fungal strains has been often reported to offer an adaptive advantage for its establishment in the field (Parlade et al. 2004). ECM fungi are known to enhance seedling survival under adverse edaphic and climatic conditions as well (Lakhanpal and Kumar 1993). Brearley, (2011) reported increase in survival rates of Dipterocarp seedlings when inoculated with ECM fungi, such as Scleroderma, Pisolithus and Tomentella. It has been reported that some ECM species were able to degrade phenanthrene and fluoranthrene (Gramss et al. 1999), tolerate the presence of 2 % w/v toluene, and ECM inoculated plants can grow on petroleum hydrocarbon-contaminated soil with no adverse effects on plant growth and development (Sarand et al. 1999). It is for these reasons that the importance of retaining mature trees as refuges for ECM fungal colonization has been emphasized and is illustrated by a detailed examination of two networking ECM fungi (Rhizopogon vinicolor and R. visiculosus (Kretzer et al. 2003) in an uneven-aged, old-growth, interior Douglas-fir forest in a very dry climatic region. Rhizopogon vinicolor/vesiculosus are host specialists of Douglas fir and have been observed at all stages of succession in studies examining ECM fungi of Douglas-fir forests (e.g. Horton et al. 2005; Twieg et al. 2007). They are considered strong networking species in Douglas fir forests (Molina et al. 1999). Not only do Rhizopogon taxa form strands considered important in inter-tree carbon transfer (Molina et al. 1999), but they have been shown to translocate nutrients and water from soils to host trees (Read and Boyd, 1986), resulting in increased seedling growth and resistance towards drought (Cairney and Chambers, 1999). In addition to mature trees, ten abundant shrub species native to interior Douglas-fir forests have been shown to share 11 ECM fungi in common with establishing Douglas-fir seedlings, thus potentially providing networks for ECM fungus colonization (Hagerman et al. 2001). In moist, mixed Douglas-fir forests, Betula papyrifera alone has been shown to share up to 41 ECM fungi with interior Douglas fir, with the proportion of shared types generally increasing with stand age (from 40 % to 80 %) (Twieg et al. 2007). With such a rich community of shared fungi, the potential complexity and extent of mycorrhizal networks was likely much greater than in the pure Douglas-fir forests. The frequent survival and rapid sprouting of paper birch root stocks following disturbance further ensures a refuge of mycorrhizal networks and is thought to aid in the rapid recovery of these forests from fire or clear cutting (Twieg et al. 2007). Many studies in Montane, tropical and boreal forests have also shown that seedling survival (McGuire, 2007), growth (Nara, 2006; Teste and Simard, 2008), ECM fungus colonization (Nara and Hogetsu, 2004), and ECM fungus diversity (Cline et al. 2005; Teste et al. 2009) are greater where seedlings establish within the mycorrhizal network of mature trees. Thus, it becomes evident that role of ectomycorrhizal fungi is critical to the survival of seedlings planted for restoration and rehabilitation of degraded forest ecosystems.


The ectomycorrhizas formed by symbiotic fungi with the free roots of forest trees, as well as their associated bacteria, significantly contribute to a number of important ecosystem processes and functions, especially nutrient cycling mainly P and N and C fluxes thus benefiting their host trees in a number of ways. This includes mobilization of N and P from organic polymers, release of nutrients from mineral particles or rock surfaces via weathering, effects on carbon cycling, interactions with mycoheterotrophic plants, mediation of plant responses to stress factors such as drought, soil acidification, toxic metals, and plant pathogens, rehabilitation and regeneration of degraded forest ecosystems by promoting seedling survival on degrades forest sites, as well as a range of possible interactions with groups of other soil microorganisms. The real significance of ectomycorrhizal fungi is that they connect the primary producers of ecosystems, plants, to the heterogeneously distributed nutrients required for their growth, enabling the flow of energy-rich compounds required for nutrient mobilization whilst simultaneously providing conduits for the translocation of mobilized products back to their hosts. Their role is particularly crucial in performing two types of functions in which the fungal partner is complementary to the photosynthetic plant: mobilizing nutrients (carbon and other macro and micronutrients) by degrading soil organic matter and weathering minerals, and coupling the autotrophic and heterotrophic cycles of C. The latter role is specific to the symbiotic nature of ECMs, in that the fungi associated with the fine roots can sometimes acquire C from the soil through enzymatic breakdown of organic matter especially during winter months when supplies of photosynthates from host plant are low or unavailable as well as from the tree photosynthates at a rate determined by fungal symbiont. Elucidating the diversity of mechanisms involved, the range of interactions with other organisms, and the ways in which these are regulated remains the ultimate challenge in understanding the role of these fungi in biogeochemical cycles. The use of molecular techniques is a promising tool to answer questions about the composition and activity of ectomycorrhizal communities, yet few studies have employed these techniques to look directly at patterns of soil C metabolism by ectomycorrhizal fungi. Examining resource use by ectomycorrhizal fungi under field conditions is an avenue for future research that will clarify the role of ectomycorrhizal fungi in the C dynamics of their host plants. New molecular tools have enabled identification of ectomycorrhizal fungal symbionts with a higher degree of resolution and have contributed to the realization that the degree of functional specificity in ectomycorrhizal associations may be higher than hitherto appreciated. Old views of ectomycorrhizal symbiosis, based solely on the mineral nutrition of individual plants, are giving way to new theories with a broader functional basis, using more ecologically relevant species and substrates. Comparative analysis of different systems will improve our understanding of responses to environmental and climatic perturbations. This new knowledge is an important prerequisite for future, sustainable management of terrestrial ecosystems.

DOI 10.1007/s12229-013-9126-7

Acknowledgment The authors are highly grateful to the Department of Biotechnology, Government of India for providing financial grant for the conduct of research. The authors are also thankful to head department of Botany University of Kashmir, Srinagar for his support and guidance during research.

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Zahoor Ahmad Itoo (1,2) * Zaffar Ahmad Reshi (1)

(1) Biological Invasions Research Lab, Department of Botany, University of Kashmir, Hazratbal, Srinagar 190006, India

(2) Author for Correspondence; e-mail:;

Published online: 7 August 2013
Table 1 Complex carboncom pounds that can be decomposed by
ectomycorrhizal and ericoid fungi. Adapted and extended from Chalot
and Brun (Chalot and Bran 1998) and Read et al. (2004)

Compound Enzyme Fungal Type

Cellulose Cellulase ERM, ECM
 Cellobiohydrolase ERM, ECM

Hemicellulose Xylanase ERM, ECM
 Mannosidasc ERM
 Galactosidase ERM
 Arabinosidase ERM
 Glucanasc ERM

Pectin Polygalacturonase ERM, ECM

Tannins Polyphenol oxidase ERM, ECM
 Peroxidase ERM, ECM
 Catcchol oxidase ERM, ECM
 Tyrosinase ERM, ECM
 Lactase ERM, ECM

Lignin Manganese peroxidases ECM
 Lignase ERM

Proteins Acid protease ERM, ECM

Chitin Chifnase ERM, ECM

Lipids Fatty acid esterase ECM
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