Open access peer-reviewed chapter
Abstract
Ectomycorrhizal (ECM) fungi play a fundamental role in the nutrient cycle in terrestrial ecosystems, especially in forest systems. In this chapter, the value of ECM fungi is reviewed from a global framework, not only to increase the production of edible fruit bodies and biomass of plants but also for the regular practices of reforestation and restoration of ecosystems, with implicit applications in biofertilization, bioremediation, and control of soil pathogens. Ecological functions of the ECM fungi are briefly reviewed. The direct implications of the ECM fungi in forestry are described. To do so, its role as a biotechnological tool in forest nursery production is briefly analyzed, as well as the role of mycorrhizal helper bacteria (MHB). Subsequently, the direct role as biofertilizers of the ECM fungi in forest management is discussed: reforestation, plantation management, and ecosystem restoration. The importance of ECM fungi to increase the tolerance of plants against biotic or abiotic stresses is analyzed.
Keywords
- forestry
- ectomycorrhiza
- restoration
- sustainable development
- nutrients
1. Introduction
It was Albert Bernhard Frank (1885), a forest pathologist, who for the first time introduced the term mycorrhiza. In the Greek language, “mykes” refers to fungus and “rhiza” refers to root. Since Frank’s description of mycorrhizal association in the 1880s [1], 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 [2]. These groups of fungi establish a symbiotic relationship with the roots of plants, called mycorrhizas. Frank established two large subdivisions of mycorrhizas, ecto- and endomycorrhizas. Ectomycorrhizal fungi form mantle and Hartig network of intercellular hyphae in the roots of forest species. Endomycorrhizas are classified as arbuscular mycorrhizas, ericoid mycorrhizas, arbutoid mycorrhizas, monotropoid mycorrhizas, ectendomycorrhizas, or orchid mycorrhizas [3]. The Arbuscular Mycorrhizal fungi (AM) form arbuscules and vesicles, they are more variable than ECM fungi since they form symbiosis with trees and herbaceous plants. Each of these categories is characterized by the invasion of plant root cells by fungal hyphae but differs in the nature of intracellular hyphal development [4, 5].
Ectomycorrhizal fungi are predominantly
The community of mycorrhizal fungi can be determinant in the structure of the plant community [9]. Therefore, the identification of the mycobiont partner and its functional structure [10] are fundamental to understand the ecological importance of this symbiotic relationship. ECM fungal diversity studies were initially based on studies of fruiting bodies and, more recently, on the direct identification of ectomycorrhizal morphoanatomical characters [11]. Despite recent advances in the use of molecular techniques, there are still many advantages associated with classical methods for studying ECM fungal diversity. For the recognition of fungal relationship and type of mycorrhizal association is advantageous over molecular method [7]. Sometimes morphoanatomical-based taxonomy is not well supported by molecular taxonomy. To overcome such discrepancy, the combined approach of morphoanatomical and molecular characterization of ectomycorrhizas in combination with phylogeny was applied [12].
Most of the cultivated species of edible fungi are saprophytes, and only some of them are ECM fungi [13]. The tickets (
2. Ecological functions of ECM fungi
In different forest ecosystems, ECM fungi have been reported to play an important role in seedling survival, establishment, and growth [3, 17, 18]. Researches have confirmed that ECM fungi play a key role in terrestrial ecosystems as drivers of global carbon and nutrient cycles [19].
Some of these traditionally known functions of the ECM fungi on the ecosystem are:
ECM fungi increase the water and nutrient supply plant, extending the volume of land accessible to the plants.
Different fungal species (drought-sensitive hydrophilic or drought-tolerant hydrophobic) can have different effects on hydraulic redistribution patterns [20]. The mechanisms to enhance the acquisition of P by tree mycorrhizal roots are the extension of extramatrical mycorrhizal hyphae, the increase of inorganic P transfer, the increase of inorganic P transporters in the fungus/soil interface, the mobilization of organic P (labile) by emission of phosphatases, and the mobilization of mineral insoluble P by the emission of organic acids (LMWOAs) [21, 22].
The mechanisms of improvement in nitrogen (N) absorption would be the intervention in the mineral N cycle (NH4+, NO3−) and the assimilation of organic N (by emitting proteases, chitinases, and others) [23, 24].
Currently, recent advances in the knowledge of nutrient translocation processes in the fungus-plant and fungus-soil interaction are especially interesting, in particular the priority role of transporters of P, N, and C [25]. The inorganic P and mineral or organic forms of N, such as NH4+, NO3−, and amino acids (AA), are absorbed by transporters specialized located in the fungal membrane in the extraradical mycelium. NH3/NH4+ and inorganic P (from polyphosphates) are imported from the symbiotic interface to the cells of the plant through selective transporters. Transporters of hexoses import carbon of plant origin into the fungus. The nutritional strategies seem to be different between symbiotic and pathogenic fungi, for example, in the translocation of C. Even different transport strategies have been found between ECM symbionts
On the other hand, the ECM colonization of the root can provide protection against soil pathogens [27]. Also, the non-nutritive benefits to plants due to changes in water relations, the level of phytohormones, the assimilation of carbon, etc. have already been verified [3]. The carbon is transferred through the ECM fungal mycelium that connects different species of plants. This can reduce competition among plants and contribute to the stability and diversity of ecosystems [28]. The extraradical mycelium of the ECM fungi provides a direct pathway for the translocation of photosynthesized carbon to microsites in the soil and a large surface area for interaction with other microorganisms [29, 30]. Recently, Hupperts et al. [31] 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. Moreover, epigeous and hypogeal sporocarps of ECM fungi are important food sources for placental and marsupial mammals [32]. The ectomycorrhizal roots, the mycelium, and the fruiting bodies of the fungi are important as food sources and habitats for invertebrates [33]. The hyphal networks produced by ECM fungi significantly alter and improve the structure of the soil [34]. In a global way, the ECM fungi improve the plant tolerance to (biotic and abiotic) environmental stresses.
3. Applications: ECM fungi to forestry
Much of our understanding of the functions of ECM fungi has come from research directed toward practical application in forestry. Some of the most common criteria considered for the selection of a most valued species or strain of ECM fungi (some of them implicit in others) are the abiotic criteria: climatic conditions such as temperature, insolation, and humidity; improvement of soil properties, such as texture and permeability; abiotic soil stress mitigation; soil contamination mitigation; soil metal mobilization; or nutrient cycling. There may also be criteria regarding the host, such as the plant/fungus specificity, the improvement of plant health, or the increase in the biomass of the plant. Finally, there are criteria regarding the fungus, such as abundance, effectiveness, propagules competitiveness, fungus growth rate, or edibility. Other criteria may be the conservation of native biodiversity, the functioning of the ecosystem, human health, food, nutraceutical value, etc. [30, 35].
3.1 ECM fungi in forest nurseries
Since the late 1950s, mycorrhizal fungi were utilized as biofertilizers to promote plant growth, because of their ability to increase the plant uptake of P, N, mineral nutrients, and water [36, 37, 38]. The idea of inoculating ECM fungi on seedlings in plant nurseries was developed by Fortin [39]. Vozzo and Hacskaylo [40] while working on ECM in the United States experimentally demonstrated that field survival and growth of tree seedlings with specific potential ECM enhance the performance of seedlings and contribute to the proper functioning of forest ecosystems.
Although successful inoculation of tree seedlings (already planted) in the field has been known, nursery inoculation is more common. Seedlings inoculated in the nursery can establish a healthy ECM system before planting. The challenge in the controlled synthesis of the ectomycorrhizal symbiosis is to produce a quality mycorrhizal plant, only colonized by the desired fungus. Accurate identification of the inoculum used and avoiding contamination during the growth of the inoculated plants are essential parts of the production process to avoid the introduction of unwanted species and to avoid the mixing of their genetic material with indigenous species [41]. The appropriate selection of suitable plant-host species is essential for the success of mycorrhization [42]. Relatively fast-growing fungi are generally preferred for inoculation because of their short incubation period. Unfortunately, many otherwise desirable ECM fungi grow slowly. According to Marx [43], fresh cultures are preferred to cultures repeatedly transferred and stored for several years. He further suggests passing important fungus cultures through a host inoculation and mycorrhiza formation followed by re-isolation, every few years to maintain mycorrhiza-forming capacity. Moreover, fungi, which produce large hyphal stands of rhizomorphs in the culture of the soil, may be superior in soil exploration and mineral uptake to those which lack rhizomorphic growth. On the other hand, the fruiting of the ECM fungi species is not based solely on the mycorrhizal state of the seedlings. After planting, in addition to the presence of indigenous competitors, the biotic and physicochemical characteristics of the soil also influence the persistence and spread of the cultivated fungus [44]. The type of ECM material used for inoculation can affect the success of a mycorrhizal inoculation program. In addition to remaining viable during storage and transport, the inoculant must also maintain its infectivity for several months after its introduction [45].
There are three main sources of fungal inoculum: soil, spores, and mycelium.
Initially, the soil or humus collected from the mycorrhizal plantation area was frequently used. Its main disadvantage is the lack of control of ECM species in the soil or of microorganisms and harmful germs. Another problem with this type of inoculant is that large amounts of soil are required to inoculate nursery plants. This method is widely used in developing countries, although it is currently discarded in mycorrhization programs. Also, planting mycorrhizal “nurse” seedlings or incorporating chopped roots of ECM hosts into nursery beds as a source of fungi for neighboring young seedlings has been successful [46].
Other sources of inoculum are the spores of fruit bodies collected in the field. The main advantages are that the spores do not require the extension of the aseptic culture and that the spore inoculum is not heavy [47]. Most of the recent research has been with
The most appropriate inoculum is the use of hyphae in a solid or liquid medium or substrate. Hyphae are cultivated mainly from sterile parts of fruiting bodies, less frequently from mycorrhiza due to their low (approx. 5–20%) success rate [48] and rarely from sclerotia [49] or sexual spores [50]. It is considered the most appropriate method since it allows the selection of particular strains of a fungus previously tested for its ability to promote the growth of plants [43]. Many species do grow well in culture, e.g., most species of
3.1.1 Ectomycorrhizal helper bacteria
The concept of “mycorrhiza helper bacteria” (MHB) was introduced in a “Tansley Review”: Helper Bacteria—a new dimension of mycorrhizal symbiosis [53], which has led to new research in the plant-fungus model system, as for the meaning of these bacteria that promote the formation of mycorrhizas and cause many physiological effects of mutualistic interaction. In general, the ability of some microorganisms to influence the formation and functioning of the symbiosis is known, through activities of various kinds such as the activation of infective propagules of the fungus in presymbiotic stages [54], facilitating the formation of entry points in the root [55] and increase of the growth rate [56]. The MHB improve mycorrhiza formation, although the same MHB can benefit mycorrhization for certain fungi and be negative for others [57]. The above reflects the fungal specificity by isolate, which exemplifies the genetic distance between isolates of different origin.
Among the mechanisms presented by the MHB are:
Promotion of the establishment of the symbiosis by stimulation of the mycelial extension. The germination of spores and mycelial growth are improved by the production of growth factors [58].
Increased contact and colonization root-fungus: increase in the number of lateral roots, mediated by the production of phytohormones [59] and the improvement of radical colonization by induction of flavonoid production [60].
Reduction of the impact of adverse environmental factors on the mycelium of the mycorrhizal fungus. Bacteria can detoxify soils, restoring their conductivity, similarly freeing them from contamination generated by heavy metals [61], and reducing the concentrations of phenolic antagonist compounds produced by the same mycorrhizal fungi [62]. The rhizospheric microorganisms also have an effect on the growth of the plants, reaching a synergistic effect, where the presence of the microfungus and the other microorganism produces an increase in the growth, vigor, and protection of the plant [63]. These effects are based on activities such as the acquisition of nutrients, inhibition of the growth of pathogenic fungi [64], and improvement of the root ramification [65]. In recent years, a potential capacity of bacteria associated with ectomycorrhizas to fix atmospheric nitrogen has been suggested [66]. Several studies suggest a real possibility that the bacteria present in mycorrhizal tissues contribute to the nutritional needs of both the fungus (ascocarp development) and consequently the plants, by providing them with available nitrogen derived from atmospheric nitrogen (N2).
MHB belong to a wide range of genera (
Research in mycorrhizas should, therefore, strive toward an improved understanding of the functional and molecular mechanisms involved in interactions in the mycorrhizosphere, in order to develop ad hoc biotechnology that allows the application of optimized combinations of microorganisms as effective inoculators within sustainable systems of plant production [74].
3.1.2 Polymicrobial formulations
A polymicrobial formulation containing a diverse mixture of beneficial rhizosphere microorganisms with multiple functionalities is attractive because combining different classes of soil organisms can take advantage of multiple plant growth-promoting mechanisms and could be applied to multiple crops [75, 76, 77, 78, 79]. A key concept in constructing effective polymicrobial multifunctional formulations is the selection and use of a right combination of rhizosphere bacteria and fungi that are mutually compatible, have complementary functionalities, effectively colonize the rhizosphere of the crop(s) of interest, and bring about a synergistic promotion of growth and yield of crop(s) [75, 80, 81, 82]. It is to be expected that well-designed multifunctional formulations such as the one described would be a welcome addition to the fast-growing inoculant enterprises worldwide. Such an inoculant is also expected to be eco-friendly and suitable for organic farming and other integrated production systems, where synthetic fertilizer inputs are not allowed or restricted by law. However, construction of such complex formulations is technically demanding [83].
Ectomycorrhizal fungi exhibit synergistic interactions with other plant-beneficial organisms such as symbiotic N2-fixers. For example, ectomycorrhizal symbiosis enhanced the efficiency of inoculation of two
Also, using plant growth-promoting microorganism (PGPM) strains that form stable and effective biofilms could be a strategy for producing commercially viable inoculant formulations [78, 87]. A majority of plant-associated bacteria found on roots and in the soil are found to form biofilms [88]. Bacterial, fungal, and bacteria/fungal biofilms were suggested as possible inoculants. This is a novel and interesting idea, but to what extent this approach would be practiced remains to be seen [83].
3.2 Application of ECM fungi in forest management: restoration of ecosystems
The inoculation of ECM fungi can be done with the objective of producing edible carpophores but also because of its considerable value in forest management; in particular, they have had great importance in reforestation programs where it was expected that the quality and economic productivity of the plantations would increase [89]. The success of the plantations with mycorrhizal seedlings from the nursery depends on their ability to quickly access the nutrients and water available within the soil matrix [90]. The relationships between the various native edible ECM fungi have been, until relatively recently, insufficiently considered in the strategies of forest management [91].
In ectomycorrhizal plantations (productive or conservation reforestations), a consequence of the recognition of the advantages of fungal diversity in ecosystems will be an increase in the refusal to introduce potentially dominant species in mixed communities. On the other hand, unfortunately, it seems that many of those fungi selected for optimal colonization in the nursery have been poor competitors in the field, especially when the planting sites contained indigenous populations of mycorrhizal fungi. There are several possible explanations for the inoculation failure (from the nursery) to produce beneficial effects in the planting sites. Probably, among the most important of these is the inability of inoculum introduced to persist in the roots of the plant after the transfer of the nursery to the field. The soil conditions experienced in the nursery and with the plant growing in a container are very different from those of most of the planting sites; in addition, the raising, storage, and transport of seedlings can reduce the vigor of fine roots and their fungal associates. Species such as
In the restoration of ecosystems, the biofertilization, the bioremediation, and the biocontrol of soil pathogens are prominent roles of the ectomycorrhizal fungi. Degraded ecosystems are the result of a wide range of characteristics and factors related to unfavorable land management or industrial activities. Environmental degradation of the soil is increasing worldwide at an alarming rate due to erosion, acidity, salinization, compaction, depletion of organic matter, and water scarcity. On the contrary, in a healthy ecosystem, there is a balanced microbiota of the soil, in such a way that the potential of pathogenic and mycorrhizal fungi coexists in apparent harmony. Ectomycorrhizal fungi can survive in extreme habitats with high or low temperature [95, 96], salt and metal concentration [97, 98], drought [99], and other circumstances related to the degradation of the ecosystem. The importance of ECM fungi in the balance of the ecosystem can be enormous, since they can be used to increase the tolerance of plants against biotic or abiotic stresses, especially their capacity to fix heavy metals or to degrade a wide variety of persistent organic compounds; to interact with soil bacteria; to attack fungi, bacteria, and pathogenic nematodes; and to improve the vegetative growth and the nutritional status of its symbiont plant.
It has been documented by several authors that mycorrhizal fungi improve the 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 the production and release of antibiotics and physical sheathing by the mantle of ECM [27, 100, 101, 102]. For example, ECM fungi have been shown to protect trees from
Under drought stress, ectomycorrhizal symbiosis has been documented to possess a remarkable capacity to the uptake of water and alter hydraulic properties of plant roots by altering both apoplastic and symplastic pathways and by their impact on plant aquaporins (AQPs) [103, 104, 105, 106]. A symbiosis between plants and ECM fungi has been documented to help plants to cope with salt stress [97, 107, 108, 109]. Li et al. [110] reported that there is ECM fungus-mediated remodeling of ion flux which helps to maintain K+/Na+ homeostasis by increasing the release of Ca2+. Also, ECM fungi have been reported to change the plant phytohormone balance during salt stress [111, 112]. Research efforts are still in progress to select new pioneer symbiotic couples for land reforestation [113].
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 [114, 115, 116, 117, 118]. Also, Meharg and Cairney [119] revised potential ways in which ectomycorrhizal fungi might support rhizosphere remediation of persistent organic pollutants (POPs). Krupa and Kozdrój [120] documented the importance of mycorrhizal fungi in forming an efficient biological barrier for checking the movement of heavy metals into the host tissues. Recently, the importance of LMW organic acids and metal chelating agents (such as siderophores) from ECM fungi in the fixation of metal ions and their transmission or not to the root of the host plant has been described [121]. 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 [98, 118, 122, 123].
4. Conclusions
The ectomycorrhizal fungi are predominantly
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