Studies on Ectomycorrhiza: An Appraisal.
It was Albert Bernard Frank (1885), a forest pathologist, who for the first time introduced the term mycorrhiza. In Greek language "mykes" refers to Fungus and "rhiza" refers to Root. Since Frank's description of mycorrhizal association in 1880's (Frank, 1885), a lot of work has been generated by different investigators as a consequence of which it is estimated that 86% of terrestrial plant species are benefited as they acquire their mineral nutrients via mycorrhizal roots (Brundrett, 2009). In fact the mutualistic phenomenon of symbiosis has been reported to result from the coevolution between plants and fungi and became essential and obligatory for terrestrial plant nutrition (Allen, 2007; Alvez et al., 2010; Brundrett, 2002; Bucking & Heyser, 2003; Trappe, 1977).
Of the seven types of mycorrhizae described (arbuscular, arbutoid, ectomycorrhiza, ectendo, ericoid, monotropoid, and orchidaceous), both arbuscular (AM) and ectomycorrhizae (ECM) are reported to be the most abundant and widespread in forest communities (Smith & Read, 2008; Taylor & Alexander, 2005). The number of ECM fungal species is estimated between 20,000-25000, and the number of plants, mainly trees and woody shrubs of tropical and temperate forests are estimated to 6000 species (Brundrett, 2009; Rinaldi et al., 2008; Roy-Bolduc et al., 2016). Forest trees belonging to Pinaceae, Fagaceae, Betulaceae, Nothophagaceae, Fabaceae, Gnetaceae, Leptospermoidae of Myrtaceae, Dipterocarpaceae and Amhersteae of Casalpiniaceae, which form dominant component in boreal, temperate and tropical rain forests, are reported to harbour a great diversity of ECM fungi. ECM fungi that associates with these ecologically and economically important trees appears to differ greatly in their ecology and dispersal abilities and could be subject to different selective forces. Recent studies suggest that typical biogeographic patterns and distance decay of similarity resulting from dispersal limitation are usually evident in ECM fungi, but these patterns do not always match those observed in plants and animals (Bahram et al., 2013; Tedersoo et al., 2012). A number of liverworts and lycophytes are also reported to form fungal associations that physically resemble ectomycorrhizas (Bidartondo et al., 2003; Horn et al., 2013). The ectomycorrhiza-like associations of these liverwortfungus and Lycophytes-fungus associations are integral parts of terrestrial ecosystems, but have rarely been studied.
In different forest ecosystems, ECM fungi have been reported to play an important role in seedling survival, establishment and growth (Sebastiana et al., 2017; Smith & Read, 2008; Tedersoo et al., 2010a). Studies have shown that the ECM fungi mostly belong to higher Basidiomycetes, Ascomycetes and a very few Zygomycetes. Researches have confirmed that ECM fungi play a key role in terrestrial ecosystems as drivers of global carbon and nutrient cycles. ECM plant provides photosynthetically fixed carbon and habitat for the fungi, while mycobionts provide dissolved and organically bound nutrients mainly nitrogen (N) and phosphorus (P) to their hosts (Simard et al., 1997; Simard & Durall, 2004; Tedersoo et al., 2010a). ECM symbiosis differ from other mutualistic plant fungi interactions by the presence of a mantle, formed by fungal colonisation of short feeder roots, and a Hartig net representing an intercellular hyphal penetration between epidermal or cortical cells (Agerer, 1999; Smith & Read, 2008; Grelet et al., 2009). Hartig net is the place of massive bidirectional exchanges of nutrients between the fungus and host plant. ECM symbionts are normally reported to colonise soils where nutrients are bound in organic compound. The mycelium of ECM fungi promotes the release of complexed nutrients through the excretion of extracellular enzymes and acids (Finlay, 2008).
Mycorrhizal taxonomy and molecular techniques have uncovered the unexpected diversity and functioning of mycorrhizal associations and their temporal and spatial dynamics in boreal, temperate, tropical and subtropical ecosystems. The development of-omics (transcriptomics, metagenomics) have now revolutionised our knowledge of ECM functioning, diversity and biogeograpy. At the ecosystem levels, more and more clues have revealed the role of mycorrhizal fungi in evolution, plant growth, soil structure and responses to environmental changes and global carbon and nutrient cycles. The present review aims at summarizing our knowledge on ECM biology, evolution, global diversity, specificity, ecology and potential role of their association in ecosystem sustainance.
Evolutionary History of ECM:
The origin of ECM association is reported to be approximately 125 million year old. Despite being widespread they are associated with only 3% of vascular plants families (Smith & Read, 2008). The oldest ECM root fossil was reported to be Pinaceae which was recorded about 50 million year ago (mya). In this regard Berbee and Taylor (1993) has emphasized that ECM origin may date from the time of mushroom evolution (130 mya) on earth, although this view seems to lack evidence as the fossilised plant material of Pinaceae, an ECM family known since the Triassic (200 mya; Hibbett et al., 1997), suggests that ECM association may have appeared before mushroom forming fungi.
Molecular evidences suggest that ECM taxa, belonging to class Agaricomycetes and some members of order Pezizales originated around 200 and 150 mya, respectively (Berbee & Taylor, 2001, 2010). In this regard largest numbers of fungal lineages are reported in mushrooms belonging to orders Pezizales, Agaricales, Helotiales, Boletales and Cantherellales (Tedersoo et al., 2010a, 2012). This phylogenetic diversity shows that ECM symbiosis has arisen several times independently (Floudas et al., 2012; Hibbett et al., 2000; Tedersoo et al, 2010a, 2012). The examination of available ECM fungi Laccaria bicolor and Tuber melanosporum genomes (Martin et al., 2008, 2010) and new genomic data documented by the Mycorrhizal Genomics Initiative Consortium (MGI) concurs with the hypothesis that mycorrhizal symbiosis in nature has originated with a loss of lignocellulose--degrading genes compared with saprotrophic ancestors (Eastwood et al., 2011; Martin & Selosse, 2008; Plett & Martin, 2011; van der Heijden et al., 2015; Wolfe et al., 2012). The loss of lignocellulose degrading enzymes has been reported to be responsible for the dependence of ECM fungi on their host plant for harvesting fixed carbon. Molecular clock analysis on the reconciled tree suggested that ECM fungi evolved far latter than the appearance of the last common ancestor of brown and white rot fungi about 300 mya (Marcel et al., 2015). These results supported the long standing hypothesis that ECM fungi evolved polyphyletically from multiple saprophytic species. The regular updates of the ECM lineages and genera can be found at the UNITE homepage http://unite.ut.ee/EcM_ lineages (Abarenkov et al., 2010).
Diversity and Specificity of ECM
ECM are reported to be common in temperate and boreal ecosystems and in large forested areas of tropical and subtropical regions (Corrales et al., 2016; Diedhiou et al., 2014; Henkel et al., 2011; Sharma et al., 2009; Tedersoo et al., 2012). In the temperate and boreal ecosystems most studies have been focused on ECM of Picea and Pinus. In the "Colour Atlas of Ectomycorrhiza" by Agerer (1987-2012) most morphotypes documented are from coniferous trees. A large number of fungal species, mostly belonging to Basidiomycota and Ascomycota associate with conifers. Species of Amhinema, Boletus, Hebeloma, Laccaria, Paxillus, Phialophora, Russula, Lactarius, Suillus and Thelephora are the commonest associates of conifer roots (Bent et al., 2011; Gao & Yang, 2010; Garcia et al., 2016; Obase et al., 2009) and the Cenococcum geophilum often dominate the community (Horton & Bruns, 1998; Koide et al., 2008; Obase et al., 2009; Taniguchi et al., 2007). These fungi often coexist and for example 100 different ECM fungal species have been detected on the same tree species locally (Roy-Bolduc et al., 2016). In a field survey of Swedish boreal forest soil, 60,000 to 1.2 million ECM have been reported in one square meter of forest soil in which 95% of plant roots are reported to form ECM association. While investigating the ECM associates of Pinus radiata over 2 years in New Zealand, Walbert et al. (2010) documented eighteen species fruiting above ground and nineteen ECM species fruiting below ground. Similarly 20 fungal taxa were reported to form ECM association with Pinus muricata by Gardes and Bruns (1996) and 27 taxa with P. thumbergii by Obase et al. (2009). In all these studies Cenococcum geophilum and species of Clavulinaceae, Russulaceae and Thelephoraceae are reported to be the main members of ECM fungal communities.
In Europe, Cenococcum geophilum and members of other genera including Lactarius, Russula, Tomentella, Cortinarius, Laccaria and Paxillus were found to be most diverse in these ecosystems (Rudawska et al., 2016). Most temperate and boreal tree species of Europian mountains including Abies alba (Silver fir) have been documented to develop obligate mutualism with Lactarius, Russula, Tomentella, Laccaria and Cortinarius, which plays significant role in the survival and growth of trees (Wazny, 2014). Moreover in a Japanese conifer forest, Matsuda et al. (2009) documented the members of family Clavulinaceae, Russulaceae, Thelephoraceae and the genus Trichophaea as ECM associates of Pinus thunbergii. Similarly, Kranabetter et al. (2009) documented 63 ECM taxa, including a dark septate fungus, four species of Piloderma, 7 of Tomentella and Psudotomentella, 8 of Russula, 27 of Cortinarius, 1 of Tricholoma and several unknown fungi from boreal forest of British Columbia (Canada).
In India, ECM diversity of different conifer species are being investigated from North West Himalayas since 1979 by Lakhanpal and his associates (Bhatt & Lakhanpal, 1990; Lakhanpal & Kumar, 1984). In South India, Mohan et al. (1993) and Natarajan et al. (2005) has done substantial work on ECM association of different fungi with coniferous trees. In a survey conducted in North-Western Himalyas for about 12 year by Lakhanpal and his associats, 72 species belonging to 15 fungal genera of mushrooms and toadstools were observed to form ECM association with Abies pindrow, Betula utilis, Cedrus deodara, Picea smithiana, Pinus roxburghii, P. wallichiana, Rhododendron arboreum, Quercus incana and Q. semicarpifolia. Beside these records, ECM fungi forming close association with coniferous and angiospermic trees have also been reported by various workers from India (Atri & Saini, 1986; Atri et al., 1997; Bhatt & Lakhanpal, 1990; Kumar & Atri, 2016; Pande et al., 2004; Sharma et al., 2008a, 2008b, 2009; Sharma et al., 2016; Watling & Abraham, 1992). The lack of trained mycorrhizal taxonomists in India and even in Asian continent has been a major limiting factor in the generation of knowledge on ECM symbiosis from this region.
In China, The ECM community composition of Castanopsis fargesii (Fagaceae) was investigated by Wang et al. (2011) in a subtropical evergreen broad-leaved forest and Zhang et al. (2013) studied the ECM fungal communities of Quercus liaotimgensis (Fagaceae), along local slopes in the temperate oak forests on the Loess Plateau. Members of Thelephoraceae (Tomentella spp.), Clavulinaceae (Clavulina spp.) and Russulaceae (Lactarius spp.) are reported to be the most species-rich and abundant ECM fungi in these regions. Similarly, Wang et al. (2017b) investigated ECM communities associated with Quercus liaotungensis, from five typical habitats, and documented some of the dominant ECM lineages in these communities (/tomentellathelephora, /cenococcum, /russula-lactarius, and /inocybe). The ECM fungal richness and diversity was reported to be positively correlated with soil organic matter and elevation. Amongest the various lineages documented, /tomentella-thelephora, /russulalactarius, and /cenococcum are the most dominant lineages associated with Fagaceae in a wide range of northern China (Smith et al., 2007; Jumpponen et al., 2010; Wang et al., 2017b).
ECM Fungal diversity of wet and dry sclerophyll Australian temperate eucalypt (Eucalyptus delegatensis, a Myrtaceae) forests was investigated by Horton et al. (2017). They hypothesised that ECM fungal community richness and composition would differ between forest types. Cortinariaceae represented the dominant family irrespective of forest type. Similarly, Waseem et al. (2017) investigated ECM fungal diversity of Tristaniopsis (Myrtaceae) tree species growing under contrasting soil conditions in the natural ecosystems of New Caledonia, about 1200 km east from Australia. They also documented Cortinarius to be the most dominant genus followed by Pisolithus and Russula.
Only recently, tropical rain forests in South East Asia (Peay et al., 2010; Riviere et al., 2007; Yuwa-Amornpitak et al., 2006), Africa (Ba et al., 2012; Diedhiou et al., 2010; Riviere et al., 2007; Suvi et al., 2010) South America (Genii et al., 2014; Morris et al., 2008; Smith et al., 2011, 2013; Tedersoo et al., 2010b) and southern Ecuador (Haug et al., 2005; Kottke et al., 2008, 2013) have been studied for below-ground ECM fungal diversity. However, very little is known from the tropical forests that cover relatively large forested areas in the world (Alexander & Selosse, 2009). ECM plants in tropical forests mostly belong to families Dipterocarpaceae, Fabaceae, Juglandaceae, Betulaceae, and Fagaceae (Henkel, 2003; Henkel et al., 2011; Morris et al., 2008). Tropical Fagaceae are still most studied in comparision Dipterocarpaceae in this regard. Castanopsis fargessii (Fagaceae) in subtropical evergreen broad leaved forest host 3 ECM fungi belonging to Ascomycetes and 14 belonging to Basidiomycetes especially, Russulaceous and Thelephoroid members (Wang et al., 2011). Morris et al. (2008) characterised diversity and richness of ECM communities in Quercus crassifolia in a tropical forest in Southern Mexico and documented Russulaceae, Cortinariaceae, Inocybaceae and Thelephoraceae as dominant ECM fungal families. Similar results were documented by Hynes et al. (2009) in California and Lancelloti and Franceschini (2013) in North-West Sardinia, while studying the ECM community in a declining Fagaceae stand. Dipterocarpaceae in South--East Asia comprises 470 tree species including dominant tree Shorea robusta, which is the only dominant tree species of tropical South--East Asia including India (Maury-Lechon & Curtet, 1998). Despite having great bio-geographic significance Shorea robusta ECM fungi have received little attention. However, Shorea robusta associate with diverse fungi such as species of Russula, Boletus, Agaricus, Amanita, Lactarius, Lactifluus, Cortinarius, Laccaria, Pisolithus, Sclerodenna, Siullus, Strobilomyces and Cantharellus (Kumar & Atri, 2016; Natarajan et al., 2005; Pyasi et al., 2011; Tapwal et al., 2013). Moreover dipterocarp forest revealed 17 phylogenetic lineages spread over 69 species primarily belonging to the /russula-lactarius, /tomentella-thelephora, /sordariales, /sebacina and /cantharellus lineages. As in temperate forests, these lineages were the most species-rich and Cenococcum geophilum was found to be the most frequent fungal taxon (Dickie, 2007; Matsuda et al., 2008, 2009; Phosri et al., 2012; Smith et al., 2013).
In tropical Africa, The /russula-lactarius and /tomentella--thelephora lineages dominated ECM fungal flora on caesalpionioid legumes, Dipterocarpaceae, Sarcolaenaceae, Phyllantaceae, Asterpeiaceae, Sapotaceae, Papilionoideae, Gnetaceae and Proteaceae. Most studies, in Africa indicated that ECM is mainly found on caesalpinoid legume tree species that play a major role in forestry and agroforestry (Ba et al., 2012). As in the temperate region, Russulales (Russula and Lactarius) showed the largest number of described species in West Africa. Some of the species of Russula harvested from West African region have also been described from East and Central Africa (Ba et al., 2012). Ba et al. (2011) investigated 195 fungal taxa from West Africa, with dominant thelephoroid taxa. Tedersoo et al. (2011) identified 18 phylogenetic lineages from Zambia, Gabon, Madagascar and Cameroon, with some shared species. The work of Tedersoo et al. (2011) confirmed the previous studies of ECM fungi from West Africa (Riviere et al., 2007; Diedhiou et al., 2010) and the Seychelles (Tedersoo et al., 2007), from where the dominance of species of the /russula-lactarius, /tomentella--thelephora, /boletus and /pisolithus-scleroderma lineages have been reported. The remarkable dominance of the /russula-lactarius and /tomentella-thelephora lineages is reminiscent of temperate and other tropical forests (Horton & Bruns, 1998; Peay et al., 2010). Other ECM fungal lineages such as /sebacina, /sordariales, /marcelleina-peziza gerardii and/ elaphomyces were absent or rarely encountered from African tropical habitats (Riviere et al., 2007; Tedersoo et al., 2007; Diedhiou et al., 2010; Jairus et al., 2011), whereas Cenococcum geophilum, one of the most widespread or dominant ECM fungi in Holartic communities was absent (Ba et al., 2012). In African tropical forests plant species diversity is much higher than in temperate forests, and also the ECM fungi associated with tropical trees could be very diverse and similar to that observed in temperate forests; so further efforts should be made to assess the genetic and functional ECM diversity of Africa.
ECM fungi are phylogenetically highly diverse in South America, but tropics are very much overlooked in this regard (Roy et al., 2017). The orders Pezizales, Agaricales, Boletales, Helotiales and Cantharellales include the largest number of fungal lineages of host families Fabaceae, Fagaceae, Dipterocarpaceae, Nyctaginaceae and Polygonaceae. ECM fungal diversity of Dicymbe corymbosa, Dicymbe altsonii, and Aldina insignis trees in Guiana Shield are reported to show high species diversity and richness in the /tussula-lactarius, /boletus and /tomentellathelephora lineages (Henkel et al., 2011; Smith et al., 2011), which was on a par with dipterocarp forests of Borneo and many ECM-rich forests from boreal and temperate zones (Peay et al., 2010). The community structure of ECM in Nothofagus forests of South America are reported to be relatively diverse, mostly involving members of the /cortinarius, /inocybe,/tomentella-thelephora, /clavulina and /tricholoma lineages (Tedersoo et al., 2010a, 2010b, 2010c; Nouhra et al., 2013; Geml et al., 2014). The/ russula-lactarius lineage was relatively poor in this region, whereas the /suillusrhizopogon, /boletus and /pisolithus-scleroderma lineages were not recovered, which is a unique distribution at the global scale (Tedersoo et al., 2012). Similarly, Moyersoen and WeiB (2014) and Smith et al. (2013) examined the ECM fungal community associated with Pakaraimaea dipterocarpacea in Venezuela and Guyana respectively, and reported thirteen ECM fungal lineages (/amanita, /boletus, /cantharellus-craterellus, /clavulina, /coltricia, /cortinarius, /hydnum, /inocybe, /russula-lactarius, /sebacina, /tomentella-thelephora, /elaphomyces and /hysterangium). The diversity of ECM fungi associated with Pakaraimaea dipterocarpacea is reported to be similar to what has been documented with dipterocarps in Southeast Asia and Africa (Peay et al.. 2010; Tedersoo et al., 2011).
The different ECM communities on different plant species support similar ecosystem functions in the soil (Wang et al., 2017a), but all these studies on ECM diversity point out that Russulaceae show a great diversity in tropical forest ecosystems, and are among the commonest ECM family (Maba et al., 2014, 2015; Malysheva et al., 2016; Peay et al., 2010; Riviere et al., 2007). Smith et al. (2011) reported that, only the/ russula-lactarius lineage is more diverse in tropical than in temperate habitats and by contrast, the/mocybe lineage is more diverse in the temperate zones. The dominance of Russulaceae in low nutrient soil has been linked with its unique role in nutrient uptake from the soil (Alexander, 2006).
ECM fungi are reported to be more or less host plant specific. On the basis of specificity to the host, Molina and Trappe (1982) classified ECM fungi into three groups, fungi with wide ECM host potential, fungi with limited host potential and fungi with narrow host potential, that only form ECM with a specific host species. Most ECM fungal species associate with a broad host range, or at least several species of the same genus (Dickie, 2007). This potential has been attributed to the wood-wide-web of fungal mycelium, where one fungus is reported to be connected with several plants to stabilise forest ecosystem (Dickie, 2007; Diedhiou et al., 2010; Peay et al.. 2015). Only few ECM fungi are specialized on a single plant species (Bruns et al., 2002; Tedersoo et al., 2008, 2010c). Reciprocally, only few ECM plants associate with a low number of ECM fungi, such as the species of genus Alnus (Pritsch et al., 1997; Roy et al., 2013).
Most studies indicate that large numbers of ECM fungi are associated with multihost. Peay et al. (2015) studied 13 genera of Dipterocarpaceae and observed non significant differences in ECM communities of different genera. Similarly, RoyBolduc et al. (2016) also observed non significant differences in ECM community of four different tree species of family Pinaceae, indicating that at family level ECM hostfungus interaction is well conserved. Some earlier studies, however, in contrast reported host identity as the main determinant of ECM fungal community structure and composition (Ishida et al., 2007; Morris et al., 2008; Tedersoo et al., 2014). Due to the lack of knowledge of complex interactions between host plants and microbial communities, the extent of this host effect has been documented to remain incompletely understood (Peay et al., 2015; Roy-Bolduc et al., 2016). In the northern hemisphere heath plants (Ericaceae) and some groups of liverworts and lycophytes form mycorrhizal associations with the same group of fungi (Chambers et al., 1999; Horn et al., 2013). Several myco-heterotrophic vascular plants have been shown to be epiparasitic upon neighbouring photosynthetic plants through shared ECM fungal symbionts (Cullings et al., 1996; Horn et al., 2013; Leake, 2004). Although photosynthetic plants are generalists in their compatibility with fungal partners, the epiparasites examined so far are reported to display exceptional specificity towards narrow groups of closely related fungi (Bidartondo et al., 2003). Leafy liverworts genera (Jungermanniales) predominantly associate with the members of Sebaciana species and thalloid liverworts associate nearly exclusively with Tulasnella species (Bidartondo & Duckett, 2010; Pressel et al., 2010). For example, Cryptothallus (liverworts) associates with a narrow clade of Tulasnella and that these same fungi have the ability to form ECM on Betula and Pinus (Bidartondo & Duckett, 2010). Horn et al. (2013) reported that Sebacinales Fungi colonise the Diphasiastrum alpinum (Lycopodiaceae) gametophytes as well as adjacent Ericaceae plants simultaneously; indicating mycoheterotrophic gametophyte to be epiparasitic on Ericaceae.
Recently, more and more studies have emerged on ECM diversity in plantations or associated with invasive plants. Outside their native range, tree species are reported to have relatively species-poor ECM communities in comparison to those growing in their natural environment (Dickie et al., 2010; Nunez et al., 2009; Tedersoo et al., 2007; Walbert et al., 2010). This has been primarily attributed to low number or lack of specific symbionts (Bahram et al., 2013; O'Hanlon, 2012; Wazny, 2014). More generalist fungi are reported to survive through the invasion of several Pinaceae in the southern hemisphere including Argentina, Brazil and New Zealand (Alberton et al., 2014; Hayward et al., 2015; Hynson et al., 2013; Moeller et al., 2015). Moreover ECM fungi with low host specificity tend to be more successful in colonizing new hosts in the invaded ranges than those with high specificity (Wolfe & Pringle, 2012). For example Amanita phalloids becomes widespread throughout North America, showed host shift from pine plantation in which it was introduced, to pines and oaks in the surrounding native forests (Pringle et al., 2009; Wolfe et al., 2010). In contrast high host specificity ECM fungi can not grow beyond its host range and can not colonise new host. For example, /suillus-rhizopogon lineage is specific to Pinaceae and even individual species of ECM fungi to different genera of Pinaceae, and Laccaria which is generalist shows additional host jumps which is responsible for diversification shifts and dispersal events associated with its ECM ecology and dispersal throughout the southern and northern hemisphere (Wilson et al., 2017). Thus ECM fungi of /suillusrhizopogon lineage is unsuccessful in colonizing new hosts in the invaded ranges than those with low specificity lineages of ECM (Tedersoo et al., 2010c). So host preference or specificity is the most important determinant of ECM fungal community composition in most studies ranging from local to global scale (Ishida et al., 2007; Tedersoo et al., 2008, 2012; Bahram et al., 2013).
Factors Affecting ECM Diversity and Composition in Terrestrial Ecosystem
It is well recognised that ectomycorrhizal fungal communities are diverse and species rich, containing a few dominant species and some rare species (Horton & Bruns, 1998; Izzo et al., 2005). ECM fungal diversity plays an important role in influencing the ecosystem functioning, as well as plant diversity (Johnson et al., 2012; Kottke et al., 2013; van der Heijden et al., 1998). In turn environmental and biological factors such as host plant diversity and competition are also reported to influence fungal community dynamics (van der Heijden et al., 1998; Peay et al., 2010). There are number of factors including heterogenous distribution of nutrients, pH, elevation, soil moisture, disturbance, coexistence of different host plants and competition between fungi and other soil microbes which have been reported to play a significant role in this regard (Bruns, 1995; Diedhiou et al., 2014; Druebert et al., 2009; Gao et al., 2014; Kennedy & Peay, 2007; Kranabetter et al., 2009; Lambers et al.. 2010; Malysheva et al., 2016).
Nutrient status of soil is reported to be the most important factor affecting the ECM diversity and richness (Erlandson et al., 2016; Garcia et al., 2016; Taniguchi et al., 2008; Tedersoo et al., 2011). Erlandson et al. (2016) studied the influence of soil environment on ECM fungal communities across hydrologic gradient in temperate North America and documented that ECM diversity is influenced by soil nutrient status primarily P and N. Similar observations have also been made by Garcia et al. (2016) on ECM communities of ponderosa pine (Pinus ponderosa) and lodgepole pine (Pinus contorta) in south-central Oregon. Higher nutrient status of soil has been reported to negatively influence the ECM diversity and richness (Corrales et al., 2016; Cox et al., 2010; Lilleskov et al., 2002; Parrent et al., 2006). Erlandson et al. (2016) documented that ECM fungi richness and diversity is negatively correlated with phosphorus availability. Similar observations have been made by Corrales et al. (2016) while working with the Oreomunnea adult saplings and seedlings across site differing in soil fertility. In the characterization of the ECM fungal community associated with Oreomunnea, it has been documented that, infection frequency of ECM fungi is lower in more fertile soils, which is consistent with the general view that benefits of ECM fungi depend on soil conditions (Treseder, 2004). So in high-fertility sites phylogenetic diversity of ECM fungi and ECM colonization rate has been reported to decrease.
The decrease in pH level in the soil up to certain extent has been reported to positively affect ECM diversity (Barrow, 1984; Benucci et al., 2016; Kluber et al., 2010; Wang et al., 2017a). Marx et al. (1984) while investigating the effect of soil pH and Pisolithus tinctorius on pecan seedlings (Carya illinoensis) documented that the percentage of roots infected by ECM increased from 22% to 44% as soil pH decreased from 6.5 to 5.5. Plant dry weight, N and K content has also been reported to increase with decreasing pH.
Elevated atmospheric C02 concentration has also been reported to affect ECM diversity and richness by increasing carbon allocation to ECM fungi by their tree host (Andrew & Lilleskov, 2009; Druebert et al., 2009; Parrent et al., 2006; Rouhier & Read, 1999). It is also reported that elevated C02 more strongly and positively influences production and composition of ECM sporocarps which suggest that ECM sporocarps are most sensitive to a reduction in C supply (Andrew & Lilleskov, 2014). With the available techniques in hand the elevated C02 concentration and future climate change will definitely have a strong influence on ECM diversity (Cairney, 2012; Corcobado et al., 2015) and this should be seen as priority area for future research.
Light is also another important abiotic factor that has been reported to influence ECM diversity and richness.Various studies have shown that plant biomass decreases with the reduction of light (Tester et al., 1986; Welander & Ottosson, 1998). Recently it has been shown that under low light condition, Pinus sylvestris seedlings inoculated with the ECM fungus Suillus bovinus decreased P acquisition and P transfer to the host plant (Bucking & Heyser, 2003; Nehls et al., 2010). While working on this aspect, Lambers et al. (1998) reported that shaded ECM plants showed lower root biomass in comparison to plants grown under optimum light conditions. This is primarily because under low light condition plants are reported to allocate proportionally less carbon to the roots which result in decrease in the ECM fungal diversity and richness.
It has been reported that in contrast to light, host damage, clear cutting, low soil moisture, and elevation may also negatively affect ECM fungal abundance and diversity (Lilleskov et al., 2002; Perez-Moreno & Read, 2000; Trocha et al., 2016; Kyaschenko et al., 2017). Trocha et al. (2016), while evaluating the effect of biotic (interspecific competition) and abiotic (organ loss or damage, light shortage) stresses on ECM root tip colonization, diversity, seedling biomass, and nitrogen content of leaf, reported that for both light demanding (Pinus) and shade-tolerant (Fagus) species, the amount of light had a more pronounced effect on ECM colonization and diversity than did juvenile damage. Wang et al. (2017a) reported that, in Austrian Alps species richness and diversity of ECM fungi decreased with increasing elevation and decreasing soil moisture. ECM diversity and species richness has also been reported to be affected by successional stages in the ecosystem. With the ecosystem development, the communities of ECM fungi are reported to become more diverse with earlysuccessional species and additional species or late successional species which appear in the later stages of ecosystem development (Dickie et al., 2009; Kyaschenko et al., 2017; Muhlmann et al., 2008; Nara, 2006; Peay et al., 2011, 2012).
All these factors shape ECM diversity locally, and interestingly, at a larger scale, some other factors explain ECM distribution, such as the host, soil quality and volume (Tedersoo et al., 2012, 2014). The host remain the main factor shaping ECM communities, which confirms that ECM fungi preferences are conserved at a larger scale (Bahram et al., 2013; Tedersoo et al., 2012). For example, Tedersoo et al. (2014) have compared Alnus ECM fungal communities across large scales (Europe, Asia, South America and North America), and found that soil chemistry explained only a small amount of variability. Intrageneric phylogenetic relations among Alnus spp. indicate that closely related hosts generally exhibit more similar fungal communities largely independent of geographical distance and environmental variables at global scale. Finally, the distribution of ECM diversity centered in the temperate zone, contrasts with the latitudinal gradient of diversity observed for plants and insects. This trend shows that ECM biogeography may also modulate their species richness locally. More and more studies have investigated the biogeography of ECM genera (Kennedy et al., 2012; Looney et al., 2016; Matheny et al., 2009), and such studies have highlighted that tropical zone could host diverse ECM taxa, or even their center of origin (for Inocybaceae, see Matheny et al., 2009). Most ECM fungi have relatively restricted ranges. Koljalg et al. (2013) reported that approximately 80% of molecularly defined species level operational taxonomic units were restricted to a single continent. Tedersoo et al. (2014) also found that, at a global scale, biogeographic regions contained unique species and the differences between geographic regions are consistent with the effectiveness of oceans and mountains as dispersal barriers, which play a major role in the current structure of ECM fungal communities. A major aim of these biogeographical studies is to identify predictable drivers of ECM fungal composition, so there is a need to work more on ECM biogeography. It is reported that ECM fungi follow biogeographical rules of microbes, such as island biogeography (Bahram et al., 2013; Peay et al., 2012, 2015) and relationships with altitude (Bahram et al., 2013; Tedersoo et al., 2012). Bahram et al. (2013) try to find out the spatial patterning and the underlying mechanisms driving these patterns across different ecosystems at the local and global scales. They examined the distance decay of similarity--diminishing similarity with increasing geographical distance. The distance-decay relationship reflects the rate of ECM species turnover (i.e. beta diversity) with increasing geographical distance and enables the prediction of gamma diversity (global richness) based on alpha diversity (local richness; Bahram et al.. 2013). Distance from the equator and host density was reported to be the main determinants of the extent of distance decay in ECM fungal communities. Tropical ECM fungal communities are reported to be exhibit stronger distance-decay patterns compared to non-tropical communities, suggesting a relatively greater spatial aggregation of ECM fungi diversity and richness in tropical ecosystems. At the global scale, Bahram et al. (2013) reported that lineage-level ECM community similarity decayed faster with latitude than with longitude, suggesting that climate has an important effect on distance decay of ECM fungal communities at the global scale, directly or indirectly by influencing host-plant distribution and soil processes. Despite considerable progress in our understanding of alpha diversity and community composition of ECM fungi, little is known about spatial structure of ECM fungal communities in different ecosystems and the relative roles of niche processes in creating these patterns of diversity.
Morphoanatomical and Molecular Studies on ECM
Despite recent advances in the use of molecular techniques, there are still many advantages associated to classical methods for studying ECM fungal diversity. Tracing mycelial connections between fruit bodies and ECM is still the most reliable way of assessing the trophic status of fungi in the field. For the recognition of fungal relationship and type of mycorrhizal association is advantageous over molecular method (Rinaldi et al., 2008). Some time morphoanatomical based taxonomy is not well supported by molecular taxonomy. To overcome such discrepancy, combined approach of morphoanatomical and molecular characterization of ECM in combination with phylogeny was applied (Mrak et al., 2017). Before molecular revolution, most studies on ECM roots were focused on morphoanatomical characters. Detailed structure of the ECM mantle was for the first time given by Foster and Marks (1966). Zak (1973) documented that mantle surface can range from thin to profuse and texture may vary from smooth, cottony, velvety and warty to granular. The mantle can differ in organisation, colour, texture, thickness and presence or absence of cystidia on mantle surface, and Hartig net, depending on the host and ECM fungus identity (Agerer, 1986; Smith & Read, 2008; Tedersoo et al., 2010a). The presence or absence of rhizomorphs and mycelial growth pattern have also been used to classify fungi by exploration type, which is an important aspect to understand their ecological function (Agerer, 2001), and the concept has since been widely used in the studies of ECM ecology.
Before the contribution of Agerer and his co-investigators (Agerer. 1986, 2006; Agerer & Rambold, 2004-2016) the method for describing the ECM association varied greatly. Agerer through series of publications started to publish descriptions for identification and characterisation of ECM which has now become standard and is being widely used throughout the world. Computer based software has also been developed to follow unifonn pattern for characterisation and determination of ECM (Agerer & Rambold, 2004-2016). Agerer (1986) described and identified the mycorrhizae of Spruce with Lactarius deterrimus, L. picinus, Russula ochroleuca and R. xerampelina by tracing hyphal connections between the fruiting bodies and the ECM roots and also observed that morphological and anatomical characteristics of ECM are conserved at the genus and species level. Yamada et al. (2001) worked out ECM either synthesized in vitro or produced in natural conditions in association with Pinus densiflora seedlings and reported that mycorrhizal morphology and anatomy within a species/isolate may vary with substrate and other external environmental conditions. The similarity in hyphal features of sporophores and the mantle, sometimes help in conformation of organic connections. For example, Kumar and Atri (2016) and Leonardi et al. (2016) reported similar laticifers in mantle and sporocarp while investigating the ECM formed by Lactifluus. Indeed, observations on ECM roots are scarce and more observations in Neotropics are still required to correct sampling bias, and to answer more specific puzzels and challenges (Roy et al., 2017).
Most studies available till date have focused on ECM of coniferous trees such as Picea and Pinus (Agerer & Rambold, 2004-2016). Roman et al. (2005) compiled 1244 descriptions of ECM published in 479 papers till 2005. Most ECM described by them were collected from Europe (862), Germany (331) followed by Italy (177). A significant number of ECM was also reported to be collected from USA (96) and Canada (175). Gymnospenns are reported to be the most common tree associates in as many as 510 descriptions with Pinaceae being the commonest host. Among angiosperms, only members of Fagaceae family are reported to be the ECM hosts in 339 descriptions with Quercus (188) being the commonest host followed by Fagus (116). Other angiosperms are poorly represented in comparison (Fig. 1). In South America, most studies on ECM descriptions deal with Fagaceae, Fabaceae, Nyctaginaceae, and Polygonaceae family (Becerra & Zak, 2011). However, in Africa, most ECM described belongs to caesalpionioid legumes, Dipterocarpaceae, Sarcolaenaceae, Asterpeiaceae, Sapotaceae, Gnetaceae, and Proteaceae host (Ba et al., 2012). The available data indicate that most ECM studies have been undertaken in the temperate and boreal forests. The ecologically and economically most important ECM trees dominate woodland and forest communities in boreal, Mediterranean, and temperate forests of the Northern Hemisphere and parts of South America, seasonal savanna and rain forest habitats in Africa, India and Indo-Malay as well as temperate rain forest and seasonal woodland communities of Australia. ECM-dominated habitats in Southeast Asia, Africa, Australia and to some extent South America, remain undersampled relative to the north temperate regions (Fig. 2). In comparision, ECM diversity of tropical and sub tropical plants is least investigated, which require exploration in this regard to supplement the present figures.
Earlier studies on ECM fungal communities were only based on morphological and anatomical observations. However, these investigations proved to be time consuming and the connection between feeder root and ectomycorrhizal fungi was sometime hard to trace. The application of molecular techniques has dramatically changed the situation. Along with ECM morphoanatomical study it is now possible to investigate accurately both fungi and plant (Tedersoo et al., 2006). The ECM species that dominate in a given forest soil are not the abundant fruiting ones, indicating fruiting--body based fungal inventories are not sufficient to describe ECM fungal communities (Zoll et al., 2016). In recent years, use of molecular methods has provided new insights into the below-ground fungal community and a more precise approach to fungal diversity studies. The Genetic analysis of ECM symbiosis is largely being done using PCR techniques. Internal transcribed spaces (ITS region) of rDNA are reported to be the most frequently used sequences for the identification of ECM fungi (Avis, 2012; Bahrain et al., 2011; Benucci et al., 2016; Healy et al., 2013; Horton et al., 2017). The DNA analysis of ECM also relied on the use of restriction fragment length polymorphisms to evaluate the unique types of strains (Dahlberg, 2001; DeBellis et al., 2006; Gehring et al., 2006; Gryta et al., 2006; Molinier et al., 2016; Wang & Guo, 2010). The techniques were often improved to avoid sequencing contaminants: a direct PCR analysis of ECM mantle can be more accurate and precise than amplifying the whole root tip (Lotti & Zambonelli, 2006). The development of late oligo-array based transcript profile now allow to investigate the molecular mechanisms within ECM root tip, such as N and P exchanges (Willmann et al., 2014; Zhang et al., 2010; Zheng et al., 2016), hormone cross-talks (Plett et al., 2014) and belowground ECM fungal communities interactions (Taniguchi et al., 2007). Comparative proteome analysis between mycorrhizal and nonmycorrhizal plants is also used to understand the mechanism behind nutrient exchange (Sebastiana et al., 2017).
Several scientists have pioneered the use of molecular markers for studies into the ecology of ECM fungi and contributed to the recent advances in mycorrhizal research where DNA sequencing and phylogenetic analyses have been used to identify species, and trace the phylogenetic position of known and unknown ECM fungi directly from ECM root tips (Avis, 2012; Bahram et al., 2011; Benucci et al., 2016; Healy et al., 2013; Horton et al., 2017; Morris et al., 2008; Smith & Peay, 2014; Tedersoo et al., 2014). Through DNA-sequencing and phylogenetic analyses, it has become clear that many of the unidentified taxa on the roots belonged to species which had previously not been known to form ECM. The data provided by DNA sequences have provided the tools necessary for mapping of microbial distributions, and have advanced the development of ECM fungal biogeography in a number of critical dimensions (Tedersoo et al., 2014). Recent advances in DNA sequencing have greatly progressed the field of ECM ecology and allowed for the study of complex communities in unprecedented detail. Next generation sequencing (NGS) can reveal powerful insights into the diversity and richness of cryptic ECM species. NGS is reported to be advantageous compared with the traditional Sanger method because of its much higher data throughput and much lower cost. It works best when species are mixed together, and generates thousands to millions of sequences at low cost, where traditional methods do not work well (Smith & Peay, 2014; Zoll et al., 2016). The traditional methods are adequate for sequencing ITS from fruit bodies, pure cultures, and even individual ECM root tips, but not as suitable when samples include multiple species (forest soil sample). NGS have made outstanding contributions for our understanding of ECM fungal diversity, ecology and biogeography (Smith & Peay, 2014; Peay & Matheny, 2017; Roy et al., 2017).
Molecular and proteomics techniques in ECM provide opportunities for visualizing how organisms interact in the soil and to assess the ECM community structure. The use of fluorescent markers, that can reveal the location of the nucleic acid (DNA) of specific organisms, can provide important additional information on microbial-plantsoil interactions. With the advances in sequencing technology it becomes possible to further explore mycorrhizal networks and interactions with other organisms, including interactions with bacteria colonizing the ECM or even endosymbiotic bacteria living inside mycorrhizal hyphae (Deveau et al., 2016).
Potential Role of Ectomcorrhiza to Sustain Terrestrial Ecosystems
ECM associations bring several advantages to host plants. Potential role of ECM in plant growth and development have been evaluated by number of investigators including Aroca et al., 2009; Camilo-Alves et al., 2013; Danielsen et al., 2013; Diagne et al., 2013; Jourand et al., 2014; Kayama & Yamanaka, 2014; Luo et al., 2011, 2014; Maurel & Plassard, 2011; Mohan et al., 2015; Tapwal et al., 2015 Xu et al., 2016 and Zong et al., 2015.They enhance water absorption, nutrient uptake, reduce the need of external fertilizer, improve plant resistance against pathogens, improve seedling growth, survival and establishment, can protect against heavy metal stress and other pollutants. However, ECM fungal species show differences in host compatibility and host growth. The host populations have diverged in community composition of their ECM fungi, and have also diverged genetically in several traits related to interactions of seedlings with particular ECM fungi, growth, and biomass allocation. Even some ECM symbionts are reported to decrease the growth of plant. Patterns of genetic variation among host plant populations for compatibility with ECM fungi has been reported to differ for the species of ECM fungi, suggesting that host plant can evolve differently in their compatibility and function with different symbiont species (Hoeksema et al., 2012).
Role in Growth and Establishment of Seedlings
The idea of inoculating ECM fungi on seedlings in plant nurseries was developed by Fortin (1966). Vozzo and Hacskaylo (1971) while working on ECM in United States experimentally demonstrated that field survival and growth of tree seedlings with specific potantial ECM enhance the performance of seedlings and contribute to the proper functioning of forest ecosystems. Numerous investigators demonstrated the impact of ECM fungi in enhancing the survival rate and early growth performance of various plant species (Danielsen et al., 2013; Kayama & Yamanaka, 2014; Kumla et al., 2016; Menkis et al., 2012; Rincon et al., 2007; Tapwal et al., 2015).
Several techniques were developed to inoculate nursery seedlings with selected ECM fungi. Mostly spore, solid substrate and liquid mycelia slurry inoculi are being used in normal practice (Marx et al., 1991; Molina & Trappe, 1982, 1994; Wan et al., 2016). Out of these solid substrate inoculums (venniculite--peat or wheat grains) of ECM fungi are reported to be as effective as liquid mycelia slurry and more effective as compared to spore slurry inoculums (Quoreshi et al., 2008; Quoreshi & Khasa, 2008). However, soil obtained from natural forests or established plantations was also directly used. One problem with this type of inoculant is that large amounts of soil are required to inoculate nursery plants, and another important problem is the risk of introducing plant pathogens and weeds. Moreover, there is no precise information on the introduced fungal species (Castellano & Molina, 1989).
Potential isolates of ECM fungi are selected based on their efficiency and compatibility which is usually measured by evaluating parameters such as the height of plant, the diameter of the stem, the overall fresh, the dry mass and the nutrient content of the inoculated plant, especially phosphorus (Desai et al., 2014; Jourand et al., 2014; Marx et al., 1991). Tuijaman et al. (2005) reported a greater survival of Shorea pinanga, when seedlings were inoculated with Pisolithus arhizus and Scleroderma sp. in comparison to control seedlings. Artificially inoculated ECM fungi are also reported to enhance growth and nutrition of the seedlings both under nursery conditions and in the field after outplanting (Browning & Whitney, 1993; Kropp & Langlois, 1990; Quoreshi et al., 2008; Villeneuve et al., 1991). The establishment of Diphasiastrum (Lycopodiaceae) gametophytes by their ECM fungal partners are reported to develop improved conservation strategies for this genus, which is endangered throughout Central Europe (Grulich, 2012; Horn et al., 2013).
In some ECM association even bacteria are reported to play a mediatory role in mycorrhizal symbiosis. In plant-fungus-bacterial association mycorrhiza helper bacteria (MHB) are reported to have positive influence in enhancing the efficiency and intensity of the ectomycorrhizal symbiosis (Brule et al., 2001; Cumming et al., 2015; Deveau et al., 2016; Dominguez et al., 2012; Izumi et al., 2006; Kurth et al., 2013; Mediavilla et al., 2016; Shakya et al., 2013; Zhang et al., 2010). Mediavilla et al. (2016) undertook in-vitro synthesis of ECM between Boletus edulis and Cistus ladanifer to test the effects of fungal culture and co-inoculation with the MHB Pseudomonas Jluorescens. This co-inoculation with a MHB doubled the plant mycorrhization and plant growth levels as compared to plant colonized with Boletus edulis alone. Similarly significant increase in colonization of Pinus halepensis root by Tuber melanosporum in the presence of Pseudomonas Jluorescens has been reported by Dominguez et al. (2012). Pseudomonas Jluorescens greatly improve the symbiotic relationship of ECM by increasing the percentage of mycorrhizal short roots to total short roots (Duponnois & Garbaye, 1991; Duponnois, 2006), the stimulation of mycelial growth, the reduction of environmental stress on the mycelium and solublisation of nutrients (Brule et al., 2001; Frey-Klett et al., 2007; Kurth et al., 2013).
Role in Regeneration of Forest Ecosystems
It is well established that artificial ECM inoculation has a great potential in the restoration of natural ecosystems, degraded and disturbed sites (Bent et al., 2011; Bois et al., 2005; Danielson & Visser, 1989; Dickie et al., 2013; Marx et al.. 1991; Miller & Jastrow, 1992; Rincon et al., 2006; van der Heijden & Horton, 2009). Successful revegetation of severely disturbed mine lands in various parts of the world has been accomplished successfully by using biological tools. The inoculation of nursery seedlings with appropriate ECM fungi is reported to be the most environment friendly approach, particularly, for disturbed and degraded ecosystem. This inoculation of nursery seedlings with appropriate ECM fungi is known to promote uptake of nutrients and water, protection against various stresses, increased resistance against some pathogens and enhanced seedling regeneration and performance (Bois et al., 2005; Quoreshi et al., 2008;). Without a host, however, the amount and diversity of ECM fungal inoculums has been reported to decrease rapidly (Dahlberg, 2002; Jones et al., 2003).
Role of ECM in Improving Soil Fertility
It is well known that soil microorganisms influence the growth and development of plant communities through increasing soil nutrient availability and mediating plant coexistence (Ba et al., 2002; Bonfante & Genre, 2010; Pritsch & Garbaye, 2011; van der Heijden et al., 2008; van der Putten et al., 2013). It is a well established fact that in ECM fungi improves the nutritional status of their host plant by supplying macro and micronutrients (Table. 1) while plant provides increased allocation of carbohydrates to the fungi in order to sustain the symbiosis (Sebastiana et al., 2017). Hatch (1936) was amongst the pioneers to document increased N and P content in mycorrhizal white pine (Pinus strobus) in comparison to non mycorrhizal plant. ECM fungi are reported to produce ectoenzymes which help to facilitate the release of organic N and P into the soil which are otherwise unavailable to the plants (Desai et al., 2014; Ma et al., 2013; Quoreshi & Khasa, 2008).
Mycorrhizal symbionts are reported to improve the host plant nutrient uptake, especially P uptake quite efficiently (Bucher, 2007; de Campos et al., 2013; Smith & Read, 2008; Stonor et al., 2014). Smith and Smith (2012) and Pedersen et al. (2013) documented that high affinity phosphate transporters of mycorrhizal fungi play an important role in absorbing P from outside of P depletion zone. Similar observation was made by Facelli et al. (2014). From ECM fungi, the PT genes in case of Boletus edulis (Wang et al., 2014), Hebeloma cylindrosporum (Tatry et al., 2009), Laccaria bicolor (Martin et al., 2008) and Tuber melanosporum (Martin et al., 2010) have been characterized. So far at least 34 PT genes of 11 ECM fungal species, including Amanita muscaria, Laccaria amethystina, Paxillus involutus, Paxillus rubicundulus, Piloderma croceum, Pisolithus microcarpus, Pisolithus tinctorius, Scleroderma citrinum, Sebacina vermifera, Suillus luteus, and Tulasnella calospora are reported (Casieri et al., 2013).
ECM fungi contribute to increased P demand of trees when they increase their root colonisation level, mostly during active growth period of plant because at that time requirenment of nutrient has been reported to increase many fold (Cairney, 2011; Szuba, 2015). While working on Pinus tabulaeformis during active growth period in Northern China, Zhang et al. (2010) isolated two phosphate transporter genes, R1PT and LbPT from Rhizopogon luteolus and Leucocortinarius bulbiger, respectively. Further investigations have revealed that R1PT and LbPT are significantly up-regulated at lower P level, and enhance P uptake and transport (Zheng et al., 2016).
Importance of ECM fungi in the N nutrition of trees and in forest N cycling process has been emphasised in recent years (Averill et al., 2014; Avis et al., 2008; Cairney, 2011; Danielsen et al., 2013; Obase et al., 2009; Taylor et al, 2004; Willmann et al., 2007, 2014; Wu et al., 2003). ECM fungi are reported to use different nitrogen sources such as nitrate, NH4+, urea (Guidot et al., 2005; Morel et al, 2008), di- and tripeptides (Benjdia et al., 2006), and protein (Guidot et al., 2005). Mycorrhiza formation strongly increase expression of fungal high-affinity NH4+ transporters (Couturier et al., 2007; Javelle et al., 2001, 2003; Kuster et al., 2007; Willmann et al, 2007).
The breakdown and mobilization of nitrogen from complex organic matter, as well as the nitrogen transporter genes transcription, are strongly activated by carbon availability (Rineau et al., 2013). The inhibition of mycorrhization when mineral supply is sufficient and its subsequent reversal when mineral supply is insufficient has been reported (Kemppainen et al., 2009), revealing the crucial role of the nitrogen in establishing ECM symbiosis. Javelle et al. (2003) reported that genes that are typically induced by nitrogen starvation are suppressed by high nitrogen availability. The silencing of LbNrt--the nitrate-transporter-encoding gene of the fungus substantially decreases growth and symbiotic interaction with plant (Kemppainen & Pardo, 2013), illustrating the important role of fungi during the establishment of ECM.
It is well known fact that fungi exude several organic acids that contribute to the release of some other nutrients such as potassium (K), calcium (Ca) and magnesium (Mg) which become available to the plants (Benito & Gonzalez-Guerrero, 2014; Kayama & Yamanaka, 2014; Plassard & Dell, 2010). So as to obtain C in the form of sugars, ECM fungi provide physical, physiological and biochemical access to nutrients in soil that the host tree would otherwise be unable to access. Similarly soil bacteria which ubiquitously colonize these ECM roots and rhizospheres are documented to play an important role along with ECM fungi in influencing tree productivity by providing limiting nutrients (N, P, K, Ca, Mg) to the host plant (Frey-Klett et al., 2007; Navarro-Rodenas et al., 2016). Moreover ECM roots are reported to select bacteria with higher mineralising potential (Calvaruso et al., 2007; Kataoka et al., 2009; Kluber et al., 2010; Uroz et al., 2007).
Many non-photosynthetic gametophyte and vascular plants, such as some liverworts and lycophyte obtain all of their carbon from fungi (Bidartondo & Duckett, 2010). The liverwort Cryptothallus mirabilis is epiparasitic and is specialized on Tulasnella species that form ECM with surrounding trees. By using microcosm experiments it was observed that the interaction with Tulasnella is necessary for growth of Cryptothallus (Bidartondo et al., 2003). Diphasiastrum alpinum (Lycopodiaceae) gametophytes colonised by ECM fungi and obtain all of their carbon and nutrition from Ericaceae plant through ECM fungi (Horn et al., 2013).
ECM Role in Amelioration of Heavy Metal Stress:
There are number of heavy metals like Zn, Fe, Cu, and Mn which are otherwise essential micronutrients for plant growth and a wide variety of cellular processes but are reported to become toxic above threshold limit (Adeleke et al., 2012; Chen et al., 2015; Ott et al., 2002). Other heavy metals in soil like Pb, Cd, As, Se, Cr, and Al are biologically non essential and toxic to plant. Despite their toxic effect on plant growth, heavy metals also influence the uptake and concentration of essential elements such as P and N (Krznaric et al., 2009; Luo et al., 2014). It has been suggested several times that microorganism exhibit higher tolerance to metal toxicity in comparison to plants. At least some ECM fungi possess the ability to grow in and possibly decompose such compounds and also impart protective effect to plants against heavy metals via prevention of translocation of heavy metals into the host (Table 2). Till date most studies have indicated that ECM plants accumulate less metal inside their tissue and grow better than non-mycorrhizal plants, when exposed to heavy metal stress (Adriaensen et al., 2004, 2005, 2006; Jourand et al., 2010; Kayama & Yamanaka, 2014; Luo et al., 2014).
Fungal organic acids are reported to play an important role in binding heavy metals thereby preventing their translocation in the host plant (Ahonen-Jonnarth et al., 2000; Fomina et al., 2006). Hentschel et al. (1993) emphasized the importance of Lactarius thiogalus, L. rufus, and Paxillus involutus in association with Picea abies for mycoremediation of Al. Krupa and Kozdroj (2004) documented that the fruiting body of fungi accumulated several times higher contents of Cd and Pb compared to those found in the soil and five fold higher concentration of metals in mycorrhizal roots compared to plants, indicating the importance of mycorrhizal fungi in forming an efficient biological barrier for checking the movement of heavy metals into the host tissues.
Ahonen-Jonnarth and Finlay (2001) reported that Laccaria bicolor is a potential ECM associate of Pinus sylvestris which prevent the uptake of Ni and Cd into P. sylvestris in polluted soil. Paxillus involutus and Suillus bovinus associated with Pinus sylvestris are also reported to prevent the uptake of Zn in contaminated soil (Adriaensen et al., 2004; Fomina et al., 2006).The impact of association of Astraeus hygrometricus and Scleroderma citrinum on the seedlings of Quercus glauca, Q. saliciana and Castanopsis cuspidata in Al polluted soil was investigated by Kayama and Yamanaka (2014). In the leaves of seedlings of C. cuspidata inoculated with Astraeus hygrometricus and Scleroderma citrinum the amount of Al has been reported to be higher in comparision to those of Quercus glauca and Q. saliciana indicating the role of ECM fungi in protection of Q. glauca and Q. saliciana from heavy metal stress.
The cellular mechanisms involved in detoxification of heavy metals by mycorrhizal fungi include biosorption of metals to fungal cell wall, chelation of metal ion in the cytosol by compounds such as Glutathione and Metallothioneins, metal exclusion mechanisms in metal-tolerant ECM fungi and the compartmentation of metals in the vacuole, where metal ions are probably complexed in a chemically inactive form (Colpaert et al., 2011; Daghino et al., 2016; Krpata et al., 2009; Luo et al., 2014). Thus metal tolerant fungal isolates are reported to successfully colonize heavy metal polluted soils and act as a better filter than non-tolerant ecotypes because the former are known to more strongly prevent metal transfer to their host (Colpaert et al., 2005, 2011; Luo et al., 2014)
Role of ECM in Disease Resistance to Plants:
It has been documented by several authors that mycorrhizal fungi improve disease resistance of their host plant primarily by direct competition, enhanced or altered plant growth, nutrition and morphology, induced resistance and development of antagonist microbiota. Direct competition or inhibition is reported to be due to production and release of antibiotics and physical sheathing by mantle of ECM (Blom et al., 2009; Branzanti et al., 1999; Corcobado et al., 2015; Duchesne et al., 1988). Japanese red pine (Pinus densiflora) inoculated with ECM fungi Suillus lubens and Rhizopogon rubescens has been reported to result in improved growth of seedlings and decreased seedlings mortality caused by pinewood nematode (Kikuchi et al., 1991). Similar observation was made by Nakashima et al. (2016) while working on Japanese black pine (Pinus thunbergii). Number of pathogenesis related (PR) proteins and enzymes that help in defense are reported to be produced in ECM infected plants by number of investigators (Guenoune et al., 2001; Guillon et al., 2002; Pfabel et al., 2012).
Pisolithus tinctorius, Laccaria laccata, Leucopaxillus cerealis and Suillus luteus are reported to show antagonistic effect against pathogenic fungus Phytophthora cinnamomi (Marx, 1972). Shrestha et al. (2005) investigated the antagonistic activity of ECM fungi Pisolithus and Scleroderma against plant pathogen such as Pythium sp., Rhizoctonia solani, Fusarium sp., Agrobacterium tumifaciens, Klebsiella sp., Staphylococcus aureus, Shigella dysetriae and Escherichia coli. Mohan et al. (2015) investigated the pathogenic effect of ECM fungi including Alnicola sp., Laccaria fratema, Lycoperdon perlatum, Pisolithus albus, Russula parazurea, Scleroderma citrinum, Suillus brevipus, and S. subluteus against pathogenic fungus Alternaria solani, Botrytis sp., Fusarium oxysporum, Phytophthora sp., Pythium sp., Rhizoctonia solani, Sclerotium rolfsii, and Subramanispora vesiculosa. The antagonistic effect was reported to be maximum in the ECM fungus Suillus brevipes (60.31%) followed by S. subluteus (49.46%). Out of the pathogenic fungi employed for investigation, growth of Phytophthora sp. was reported to be highly inhibited by all 8 different ECM fungi.
Camilo-Alves et al. (2013) documented Phytophthora cinnamomi to be the main biotic factor in Quercus ilex decline. This invasive pathogen has been reported to be responsible for multiple fine root infections and tree death due to impairment of Q. ilex water uptake and photosynthesis (Corcobado et al., 2013a, 2013b). ECM fungi have been shown to protect trees from P. cinnamomi infection along with supporting their survival and growth in comparison to non mycorrhizal seedlings (Azul et al., 2014; Branzanti et al., 1999; Corcobado et al., 2015). Thus ECM fungi can also be used as fungicide in nursery plantations for better growth, survival and establishment of seedlings.
Role of ECM in Drought and Salt Tolerance:
Symbiosis between plants and mycorrhizal fungi, have also been reported to enhance drought and salt tolerance of their host plant (Breda et al., 2006; Luo et al., 2011, 2014; Richard et al., 2011; Xu et al., 2016). Water has been documented as vital regulator of plant growth, and mycorrhizal fungal colonisation of root tips has been reported to significantly impact root water uptake by altering both apoplastic and symplastic pathways (Lehto & Zwiazek, 2011; Smith & Read, 2008) and formation of more lateral roots (Felten et al., 2009). Under drought stress, mycorrhizal symbiosis has been documented to possess a remarkable capacity to alter hydraulic properties of plant roots by altering symplastic pathways and by their impact on plant aquaporins (AQPs) (Aroca et al., 2009; Dietz et al., 2011; Maurel & Plassard, 2011; Nehls & Dietz, 2014; Xu et al., 2015). As reported by Xu et al. (2015) in case of Picea glauca seedlings colonized by Laccaria bicolor, the fungal aquaporin (JQ585595) have significant impact on root hydraulics under water stress.
Symbiosis between plants and ECM fungi has been documented to help plants to cope with salt stress (Ishida et al., 2009; Luo et al., 2011, 2014; Richard et al., 2011). While working with Poplar, Langenfeld-Heyser et al. (2007) documented the positive effect of ECM on the host in increasing plant biomass and decreasing Na+ accumulation in poplar leaves. Similarly while working on roots under salt stress, Li et al. (2012) reported that there is ECM mediated remodeling of ion flux which helps to maintain K+ /Na+ homeostasis by increasing the release of [Ca.sup.2+]. ECM has also been reported to change the plant phytohormone balance during salt stress. The presence of Paxillus involutus as ECM partner has been associated with increased level of abscisic acid and salicylic acid and decreased level of jasmonic acid and auxin in poplar roots in comparison to non-mycorrhizal roots under water stress (Luo et al., 2009; Szuba, 2015).
ECM in Carbon Cycling and Decomposition of Organic Matter:
The 'mycorrhizal decomposition theory' of Frank seems to have been largely ignored until the mid-1980s, when main emphasis was laid on the abilities of ectomycorrhizal fungi to retrieve nitrogen (N) and phosphorus from plant litter. In such situations ECM fungi are reported to act as facultative saprotrophs and benefit from organic matter decomposition primarily through increased nitrogen mobilization rather than through release of metabolic carbon (Lindahl & Tunlid, 2015; Hupperts et al., 2017). This view was supported by the observation of Rineau et al. (2013) that organic matter transformation by Paxillus involutus in pure culture was stimulated rather than repressed by glucose additions. In the study of Bodeker et al. (2014), organic matter degrading enzyme activity has been reported to decline after the addition of ammonium because organic N mobilization was suppressed in the presence of more easily accessible N. Facultative saprotrophism has been reported to help mycorrhizal fungi in survival in the absence of host plants or when host plants fail to supply enough carbon (Buee et al., 2005; Courty et al., 2007). Hupperts et al. (2017) proposed two competing models to explain carbon mobilization by ectomycorrhizal fungi. 'Saprotrophy model', where decreased allocation of carbon may induce saprotrophic behaviour in ectomycorrhizal fungi, resulting in the decomposition of organic matter to mobilize carbon and second 'nutrient acquisition model', where decomposition may instead be driven by the acquisition of nutrients locked within soil organic matter compounds.
Hofrichter et al. (1999) demonstrated oxidation of synthetic lignin to C02 in a cellfree in vitro system. Martin et al. (2008) reported limited capacity of ECM fungi to decompose plant litter. Some of the mycorrhizal mushrooms including Laccaria bicolor (Martin et al., 2008), Tuber melanosporum (Martin et al., 2010) and Amanita species (Wolfe et al., 2012) are reported to have lost most of their enzymes degrading plant cell wall over a period of time. At the contrary, in some ECM fungi including Cortinarius glaucopus the retention of a large number of Class II peroxidase genes has been reported (Bodeker et al., 2014), which plays an important role in lignin degradation (Sinsabaugh, 2010). Furthermore, the potential ability to degrade lignin is more common in lowbiomass ectomycorrhizas as compared to high-biomass ectomycorrhizas (Hupperts et al., 2017). Thus, Cortinarius and some other ECM species are documented to have retained the capacity of their Agaricales ancestors, such as white-rot fungi (Matheny et al., 2006; Shah et al., 2016), able to enzymatically oxidize and decompose phenolic macromolecules, and especialiy the lignin. Indeed, peroxidase activity in soils has been found to positively correlate with the species richness and relative abundance of ECM fungi (Phillips et al., 2014; Talbot et al., 2013).
Hupperts et al. (2017) tested whether phenology-induced shifts in carbon reserves of fine roots of aspen (Populus tremuloides) affect potential activity of four carbon-compound degrading enzymes, [beta]-glucuronidase, [beta]-glucosidase, N-acetylglucosaminidase and laccase, by ectomycorrhizal fungi. Ectomycorrhizal roots from mature aspen were collected and analysed during tree dormancy, leaf flush, full leaf expansion and leaf abscission and observed that extracellular enzyme activity to be highest when root carbon reserves were lowest and root carbon reserves were positively correlated with invertase of plant, suggesting that phenology may affect carbon allocation to ECM fungi.
Ectomycorrhizal fungi represent an important component of soil microbiota and associate with roots of several and abundant tree species. ECM associations are formed by a restricted group of higher plant families such as Pinaceae, Betulaceae, Fabaceae, Dipterocarpaceae, Fagaceae and Myrtaceae with fungal symbionts belonging to the Basidiomycota and Ascomycota. There are about 80 phylogenetic lineages of ECM fungal species that are reported to have independently evolved from saprotrophic ancestors (Tedersoo & Smith, 2013). ECM association is the result of co-evolution between plant and fungi which show mycorrhiza to be essential in terrestrial plant nutrition and play a significant role in survival and growth of associated trees. It is now established fact that mycorrhizal inoculation is beneficial for reclamation of variety of disturbed sites and had great potential in restoration of natural ecosystem. Most studies on ECM have been carried out in temperate and boreal forests and the associated fungi mostly belong to Basidiomycota, especially Russuleceae.
Earlier studies on ECM fungal communities were carried out using morphoanatomical characters, however presently molecular techniques are being employed which along with morphoanatomical features helps to precisely understand the ECM communities structure and diversity. Present day molecular tools along with standard PCR analysis and transcriptome analysis such as oligoarray based transcriptome profiling are being used so as to understand the molecular mechanisms of ECM influence on host plant including N and P acquisition and carbohydrate transport. Investigation done so far in this regard clearly suggest that plants inoculated with ECM fungi have greater biomass and survival rate than those without associated mycorrhizal partner, or those growing only with fertilizers. NGS has changed the face of microbial ecology, and have gained unprecedented insight into the community dynamics and biogeography of cryptic ECM species.
Despite recent advances in understanding community ecology of ECM fungi, little is known about spatial distribution patterns of ECM fungal communities from local to global scales. However, using population genetics and phylogenetic tools based on a group of closely related species or within biological species, spatial and phylogenetic scale of ECM fungal biogeography needs to be further explored. There are many areas which remain to be explored on ECM interactions and their dynamic. Accurate mycological data in man-made, native, or disturbed forests are required to better manage plant and fungi biodiversity. We need to work on the complete ECM microbiome so as to unearth information of all fungi and bacteria associated with plant roots and magnitude of infection amongst them. Increased taxonomic efforts especially in tropical and subtropical forests are required in this regard where not much information is available. The development and identification of new strains able to increase forest productivity is yet another area which requires attention. Along with molecular investigation of ECM and host species, scope of application of proteomics and metabolomics needs to be investigated with a view to elucidate the biochemistry underlying this ECM related symbiosis. Coevolutionary processes between plants and mycorrhizal fungi are also still poorly understood along with the effect of ECM responses to expected future climate change and its consequences: these are some of the areas which need to be thoroughly investigated.
Acknowledgements We are grateful to Melanie Roy and another anonymous reviewer for their useful comments on the manuscript. Thanks are due to Council of Scientific and Industrial Research (CSIR), New Delhi, India for financial assistance under CSIR-JRF fellowship scheme to the first author. To University Grants Commission we are indebted for giving liberal grants to the department under SAP programme and to Department of Biotechnology, Government of India, for grant under IPLS programme.
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Jitender Kumar (1) * N. S. Atri (1,2)
(1) Department of Botany. Punjabi University. Patiala--147002, India
(2) Author for Correspondence: e-mail: email@example.com
Published online: 25 October 2017
Caption: Fig. 1 Pie chart showing the proportion of ECM plant families studied so far
Caption: Fig. 2 Global map showing location of the ECM diversity and morphoanatomical study sites (Triangles)
Table 1 ECM fungi, associated host plant and their role in nutrient uptake Sr. No Fungi Host Nutrient 1 Hebeloma crustuliniforme, Betula pendula N Amanita muscaria. Paxillus involutus 2 Trichoderma harzianum, Pinus N. P, K Laccaria laccata wallichiana 3 Suillus varigatus, Rhizopogon Pinus P, K, Mg, S roseolus sylvestris 4 Hebeloma longicaudum, Pinus N, P, K, Mg Laccaria bicolor sylvestris 5 Paxillus involutus. Picea abies P. Ca Betula pendula 6 Paxillus involutus, Suillus Pinus spp. N bovines 7 Pisolithus tinctorius Eucalyptus P pilularis 8 Suillus bovinus. Schima P Boletus edulis. wallichii Scleroderma citrinum 9 Hebeloma cylindrosporum Pinus pinaster K 10 Descolea maculata, Pisolithus Eucalyptus P tinctorius, Paxillus diversicolor involutus 11 Paxillus involutus Picea abies P 12 Suillus bovinus Populus tremela P P. alba 13 Suillus bovines Pinus P sylvestris 14 Laccaria lateritia Eucalyptus P globules 15 Paxillus involutus. Pinus P Suillus luteus. sylvestris Sitillus bovinus, Thelephora terrestris 16 Laccaria bicolor, Pintts rigida P Pisolitluis tinctorius, Paxillus involutus 17 Pisolithus tinctorius, Pinus N, P Rhizopogan vulgaris, wallichiana Suillus granulates, Laccaria laccata, Hebeloma crustuliniforme. 18 Laccaria bicolor Populus P tremuloides 19 Pisolithus albus. Scleroderma Acacia mangium N dictyosporum. S. verrucosum, Scleroderma sp. 20 Tuber melanosporum Quercus ilex. P Quercus faginea. 21 Tuber melanosporum Quercus P, N, K, petraea, Quercus faginea. Pinus Ca, Mg halepensis 22 Rhizopogon roseolus. Pinus N Suillus bovinus. sylvestris Pisolithus tinctorius. Paxillus involutus 23 Thelephora terrestris Pinus contorta N 24 Amanita muscaria, Elaphomyces Eucalyptus N, P, K antracinus, Pisolithus urophylla microcarpus. Scleroderma areolatum 25 Hebeloma cvlindrosporum Pinus pinaster P, K 26 Thelephora terrestris Pinus N sylvestris 27 Pisolithus arhizus Pinus N sylvestris 28 Paxillus involutus Picea abies Mg 29 Laccaria bicolor, Thelephora Eucalyptus P terrestris coccifera 30 Wilcoxina sp., Cenococcum Picea N sp., Amphinema byssoides engelmannii 31 Pisolithus albus Acacia N. P spirorbis. Eucalyptus globules 32 Scleroderma verrucosum Quercus P. K, Mg, acutissima Ca 33 Rhizopogon occidentalis, Pinus muricata N R. salebrosus, R. vulgaris, Tomentella sublilacina 34 Pisolithus albus Eucalyptus Ca, K tereticornis 35 Paxillus involutus Populus P, Ca, Mg deltoids 36 Pisolithus sp. Pinus pinaster N, P, K, Ca, Mg 37 Laccaria laccata Fagus sylvatica K, Mg 38 Pisolithus tinctorius Pinus caribaea N. P var. hondurensis 39 Hebeloma cylindrosporum Pinus pinaster N 40 Suillus tomentosus Pinus contorta N 41 Laccaria laccata Picea mariana N 42 Melanogaster ambiguous, Pinus pinea N, P Pisolithus tinctorius. Rhizopogon luteolus, Rhizopogon roseolus. Scleroderma verrucosum 43 Pisolithus tinctorius. Pinus taeda P Cenococcum geophilum 44 Hebeloma crustuliniforme Populus N tremuloides 45 Hebeloma cylindrosporum Pinus pinaster P 46 Amanita rubescens. Pinus N Lactarius deterrimus sylvestris 47 Pisolithus arhizus, Shorea seminis N, P Scleroderma columnare 48 Suillus variegates Pinus P sylvestris 49 Pisolithus tinctorius Pinus resinosa N 50 Pisolithus sp., Pinus K, P, Ca, Cenococcum geophilum, densiflora. Mg Laccaria laccata Quercus variabilis Sr. No Fungi References 1 Hebeloma crustuliniforme, Abuzinadah & Read, 1986 Amanita muscaria. Paxillus involutus 2 Trichoderma harzianum, Ahangar et al., 2012 Laccaria laccata 3 Suillus varigatus, Rhizopogon Ahonen-Jonnarth et al., 2000 roseolus 4 Hebeloma longicaudum, Ahonen-Jonnarth et al., 2003 Laccaria bicolor 5 Paxillus involutus. Andersson et al., 1996 6 Paxillus involutus, Suillus Arnebrant, 1994 bovines 7 Pisolithus tinctorius Ashford et al., 1999 8 Suillus bovinus. Bendangmenla & Ajungla, 2014 Boletus edulis. Scleroderma citrinum 9 Hebeloma cylindrosporum Benito & Gonzalez-Guerrero, 2014 10 Descolea maculata, Pisolithus Bougher et al., 1990 tinctorius, Paxillus involutus 11 Paxillus involutus Brandes et al., 1998 12 Suillus bovinus Bucking & Heyser, 2001 13 Suillus bovines Bucking & Heyser, 2003 14 Laccaria lateritia Chen et al., 2000 15 Paxillus involutus. Colpaert et al., 1999 Suillus luteus. Sitillus bovinus, Thelephora terrestris 16 Laccaria bicolor, Cumming, 1996 Pisolitluis tinctorius, Paxillus involutus 17 Pisolithus tinctorius, Dar et al., 2007 Rhizopogan vulgaris, Suillus granulates, Laccaria laccata, Hebeloma crustuliniforme. 18 Laccaria bicolor Desai et al., 2014 19 Pisolithus albus. Scleroderma Diagne et al., 2013 dictyosporum. S. verrucosum, Scleroderma sp. 20 Tuber melanosporum Dominguez Nunez et al., 2006 21 Tuber melanosporum Dominguez Nunez et al., 2008 22 Rhizopogon roseolus. Finlay et al., 1988 Suillus bovinus. Pisolithus tinctorius. Paxillus involutus 23 Thelephora terrestris Finlay & Soderstrom, 1992 24 Amanita muscaria, Elaphomyces Gandini et al., 2015 antracinus, Pisolithus microcarpus. Scleroderma areolatum 25 Hebeloma cvlindrosporum Garcia et al., 2014 26 Thelephora terrestris Hilszczanska et al., 2008 27 Pisolithus arhizus Hogberg et al., 2003 28 Paxillus involutus Jentschke et al., 2000 29 Laccaria bicolor, Thelephora Jones et al., 1998 terrestris 30 Wilcoxina sp., Cenococcum Jones et al., 2009 sp., Amphinema byssoides 31 Pisolithus albus Jourand et al., 2014 32 Scleroderma verrucosum Jung & Tamai, 2013 33 Rhizopogon occidentalis, Kennedy & Peay, 2007 R. salebrosus, R. vulgaris, Tomentella sublilacina 34 Pisolithus albus Khosla & Reddy, 2008 35 Paxillus involutus Khosla et al., 2009 36 Pisolithus sp. Lamhamedi et al., 1992 37 Laccaria laccata Leyval & Berthelin, 1989 38 Pisolithus tinctorius Marx et al., 1985 39 Hebeloma cylindrosporum MUller et al., 2007 40 Suillus tomentosus Paul et al., 2007 41 Laccaria laccata Quoreshi & Timmer, 2000 42 Melanogaster ambiguous, Rincon et al., 2005 Pisolithus tinctorius. Rhizopogon luteolus, Rhizopogon roseolus. Scleroderma verrucosum 43 Pisolithus tinctorius. Rousseau et al., 1994 Cenococcum geophilum 44 Hebeloma crustuliniforme Siemens et al., 2011 45 Hebeloma cylindrosporum Tatty et al., 2009 46 Amanita rubescens. Taylor et al., 2004 Lactarius deterrimus 47 Pisolithus arhizus, Turjaman et al., 2006 Scleroderma columnare 48 Suillus variegates Wallander. 2000 49 Pisolithus tinctorius Wu et al., 2003 50 Pisolithus sp., Zongetal., 2015 Cenococcum geophilum, Laccaria laccata Table 2 ECM fungi and their plant associate mediating heavy metal stress Sr. No. Fungi Host Heavy metal 1 Suillus luteus Pinus Zn sylvestris 2 S. luteus P. sylvestris Cu 3 S. bovines P. sylvestris Zn 4 S. varigatus, Rhizopogon P. sylvestris Al, Cu, Ni roseolus 5 Hebeloma longicaudum, P. sylvestris Al Laccaria bicolor 6 Pisolithus tinctorius Eucalyptus Mn grandis 7 Pisolithus sp., Cenococcum Pinus Cu geophilum densiflora 8 Paxillus involutus Pinus Zn sylvestris 9 Amanita muscaria, Cenococcum Pinus spp. Hg geophilum, Laccaria laccata, Piloderma bicolor, Pisolithus tinctorius, Suillus decipiens, 10 Pisolithus tinctorius, Pinus rigida Al Hebeloma crustuliniforme 11 Hebeloma crustuliniforme Picea abies Cd, Zn 12 Pisolithus tinctorius Populous alba Cd X glandulosa 13 Paxillus involutus Picea abies Al 14 Laccaria bicolor, Paxillus Picea abies Cd involutus 15 Pisolithus albus Eucalyptus Ni globules 16 Pisolithus albus Acacia spirorbis. Eucalyptus globules 17 Paxillus involutus Populus Al deltoids 18 Suillus luteus Pinus Cd sylvestris 19 Suillus luteus Pinus Zn sylvestris 20 Astraeus hygrometricus. Quercus glauca. Al Scleroderma citrinum Q. saliciana, Castanopsis cuspidate 21 Pxillus involutus Populus x Cd canascens 22 Pisolithus tinctorius Pinus taeda Al 23 Pisolithus tinctorius Pinus strobes Al 24 Cadophora finlandica Salix sp. Cd, Zn 25 Suillus hovines, Pinus Cu Thelephora terrestris sylvestris Sr. No. Fungi References 1 Suillus luteus Adriaensen et al., 2004 2 S. luteus Adriaensen et al., 2005 3 S. bovines Adriaensen et al., 2006 4 S. varigatus, Rhizopogon Ahonen-Jonnarth et al., 2000 roseolus 5 Hebeloma longicaudum, Ahonen-Jonnarth et al., 2003 Laccaria bicolor 6 Pisolithus tinctorius Canton et al., 2016 7 Pisolithus sp., Cenococcum Chen et al., 2015 geophilum 8 Paxillus involutus Colpaert & Van Assche, 1993 9 Amanita muscaria, Cenococcum Crane et al., 2010 geophilum, Laccaria laccata, Piloderma bicolor, Pisolithus tinctorius, Suillus decipiens, 10 Pisolithus tinctorius, Cumming & Weinstein. 1990 Hebeloma crustuliniforme 11 Hebeloma crustuliniforme Frey et al., 2000 12 Pisolithus tinctorius Han et al., 2011 13 Paxillus involutus Hentschel et al., 1993 14 Laccaria bicolor, Paxillus Jentschke et al., 1999 involutus 15 Pisolithus albus Jourand et al., 2010 16 Pisolithus albus Jourand et al., 2014 17 Paxillus involutus Khosla et al., 2009 18 Suillus luteus Krznaric et al., 2009 19 Suillus luteus Krznaric et al., 2010 20 Astraeus hygrometricus. Kayama & Yamanaka, 2014 Scleroderma citrinum 21 Pxillus involutus Ma et al., 2013 22 Pisolithus tinctorius Moyer-Henry et al., 2005 23 Pisolithus tinctorius Schier & McQuattie, 1995 24 Cadophora finlandica Utmazian et al., 2007 25 Suillus hovines, Van Tichelen et al., 2001 Thelephora terrestris
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|Author:||Kumar, Jitender; Atri, N.S.|
|Publication:||The Botanical Review|
|Date:||Jun 1, 2018|
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