Mycorrhiza in Pines: Comparison
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Mycorrhiza is one of the fundamental phenomena of nature, characteristic of land plants from the moment of their formation, representing a form of symbiosis between plants, fungi, and bacteria.

  • mushroom–root symbiosis  pathogens  artificial mycorrhization  forest protection
  • mushroom–root symbiosis
  • pathogens
  • artificial mycorrhization
  • forest protection

1. Introduction

A refined model of the predicted distributions of 12 European forest tree species under three climate change scenarios from 2061 to 2080 showed that Abies alba, Fagus sylvatica, Fraxinus excelsior, Quercus robur, and Quercus petraea would be among the ‘winners’, while the ‘losers’ would be the pioneer species Betula pendula, Larix decidua, Picea abies, and Pinus sylvestris [1].
Assuming limited migration, most of the species analyzed would be confronted with a considerable reduction in the areas of suitable habitat. The ecological consequences of the predicted shrinking of distribution areas would be serious for both forestry and nature conservation. Other studies on the effects of climate change on Scots pine growth across Europe confirm this tendency [2]. If these predictions turned out to be true 75% of forest-forming species in Poland would be affected.
Mycorrhiza is one of the fundamental phenomena of nature, characteristic of land plants from the moment of their formation, representing a form of symbiosis between plants, fungi, and bacteria. More than 90% of vascular plants in underground ecosystems are associated with mycorrhizal fungi, which have direct access to the assimilates of their hosts and serve as carriers of mineral nutrients [3][4].
Mycorrhizal fungi serve as mediators in the interactions of plants with various soil microbes and influence the dynamics with pathogens as well as with the mutualists of the mycorrhizosphere, which contribute to vitamin production and protect against antagonists [5][6][7]. The symbiotic relationship goes even further, as mycorrhizal root connections influence underground plant properties, regulate relationships between plants, and alter general ecosystem processes.
Mycorrhizal networks, which extend over extensive underground connections, establish physical links between plants of the same or different species. This network facilitates the transfer of nutrients and the transmission of chemical signals between plants [8]. The different types of mycorrhiza—arbuscular mycorrhiza (AM), ectomycorrhiza (ECM), ericoid mycorrhiza (ErM), and orchid mycorrhiza (OM)—each have different evolutionary backgrounds, anatomical structures, and ecological functions. Consequently, these mycorrhizal associations exert different influences on plant protection, nutrient acquisition, and the cycling of carbon and nutrients in the soil.
Mycorrhizal fungi generally play a central role in influencing the dynamics of plant populations and communities, with notable differences between different mycorrhizal types.
Mycorrhizal associations are of great benefit to terrestrial plants, as they improve access to nutrients and stress tolerance. These fungi mediate plant interactions with the soil microbiome and influence nutrient uptake, vitamin production, and protection against pathogens [7]. Given the importance of symbiotic relationships between plants and mycorrhizal fungi, the use of mycorrhizal fungi is important for rehabilitating degraded soils and increasing their fertility [9][10].

2. Invaluable Mycorrhizal Network

The phenomenon of symbiosis has long been at the center of scientific interest and is also of interest to representatives of various biological disciplines. Scientists are interested in the forms and types of mycorrhizal fungi, their distribution in the plant and animal world, the nature of the relationships between the components of symbiotic associations, and the adaptations of symbionts [8].
It is widely known that the network of mycorrhizal fungi in the soil, which connects the root systems of different plants, is divided according to mycorrhizal type and association specificity and influences the redistribution of carbon and nutrients, underground signaling, and the regulation of competition. Mycorrhizal fungi transport plant carbon into the soil to maintain the microbiome of the mycorrhizosphere. Larger plants significantly contribute to the maintenance of mycorrhizal networks in certain symbioses.
There is also nutrient transfer between plants, but indirect pathways such as the decomposition of roots and leaf litter often play a more important role than transport by mycorrhizae. Mycorrhizal fungi communicate with plants via various compounds that mediate underground signaling and kin recognition. Signaling and nutrient transfer are most pronounced between related plants, suggesting direct communication [11]. Communication between unrelated plants and plants of different mycorrhizal types is weaker, apart from occasional losses due to parasitism.
In forest communities, an important factor for species diversity is the dependence on the density of conspecifics. However, as an important biotic component of the soil environment, soil microbes can also contribute to the formation of plant diversity and biomass patterns [11][12]. The rich diversity and biomass of ericoid, ectomycorrhizal, and saprotrophic fungal guilds in forest soils play a crucial role in conservation and ecosystem processes. In addition, many ectomycorrhizal fungi are important for nature conservation. However, there is a lack of comprehensive information on the functions of soil fungi, their relationships to forest conservation values, and the effects of inter- and intra-guild interactions on soil organic matter.
Trees generally form two main types of mycorrhizal associations: arbuscular mycorrhizal (AM) associations with fungi from the subphylum Glomeromycota and ectomycorrhizal (EM) associations with fungi belonging mainly to the phyla Ascomycota and Basidiomycota [13]. An increasing number of studies have focused on the mycorrhizal network in different countries around the world [3][4][7][13][14][15][16], including Poland [17][18][19][20] and Ukraine [21][22][23]. Pachlewski’s team in Poland carried out the most important mycorrhiza identifications [2324], contributing to the physiology of mycorrhiza, the isolation of mycorrhizal fungi and their influence on the vitality of trees, and the artificial mycorrhization of forest tree seedlings under laboratory conditions.
Unfortunately, soils that have been degraded, for example, due to many years of agricultural use, often lack mycorrhizal fungi [9]. Therefore, before planting pine seedlings, it is recommended to introduce organic material from the forest into the soil, e.g., in the form of logging residues. This treatment not only increases the biodiversity of the mycobiome and microbiome [2425] but also restores the fungal species that form mycorrhizal associations with pine seedlings, making them healthier and better adapted, for example, to longer periods of drought (as a result of climate change). This means that the silvicultural goal of creating grassy and diverse stands for future generations has a better chance of being realized [10].

3. Mycorrhizal Components of Pine Trees and Their Properties

Pinus species are highly dependent on the presence of compatible ectomycorrhizal (ECM) fungi. The presence of mycorrhizal communities in the soil, which are characteristic of this species, provides the trees with access to nutrients in the soil and creates favorable conditions for their growth and development.
Large-scale mycological observations in Poland have identified species of mycorrhizal fungi that accompany pine regardless of the type of forest area and have confirmed the ability of many fungi to form ectomycorrhizae with it [2324]. Species from the genera Amanita, Tricholoma, Suillus, Rhizopogon, and Hebeloma are probably among the most important associates of pine. Genera such as Lactarius, Cortinarius, and Russula contain a wide range of species that can form ectomycorrhizas with pine. The genera Collybia, Clitocybe, and Mycena are demonstrably unable to form mycorrhiza with pine trees [2526][2627].
Studies conducted in Ukraine have demonstrated symbiotic relationships between pines and the mycorrhizal fungi Suillus luteus and Amanita muscaria [2728]. Scleroderma species form symbiotic relationships not only with pine trees but also with Pinus patula [2829], P. menziesii, and P. pinaster [2930]. Such symbioses were also found in forests with P. sylvestris, P. resinosa, Larix decidua [3031], Betula pendula, Quercus petraea/robur [31][32][33][34], Alnus spp. [3435], Picea abies [16], and Eucalyptus spp. [3536]. To date, the genus Scleroderma comprises about 60 species, and most of them can form mycorrhiza, although these fungi can also exist as saprotrophs [3637][3738]. One of the main benefits of symbiotic relationships with Scleroderma spp. is the increase in vigor and stress resistance of young plants.
Imleria badia (Fr.) is also a mycorrhizal partner of pine. It has an ecological advantage over other pine companions and grows well under various environmental conditions, even in metal-polluted areas [3839]. The fungus Imleria badia grows in coniferous and mixed forests in Europe, Australia, and Japan and most commonly forms mycorrhizae with pines and spruces [3940]. It is widespread in North America (from eastern Canada, western Minnesota, and south to North Carolina), as well as in China and Southeast Asia.

4. Peculiarities of Ectomycorrhizal Fungi and Their Characteristics

The symbionts of most temperate and boreal forest trees are ectomycorrhizal (ECM) fungi, which supply their host plants with nutrients and water in exchange for carbon [4041][4142]. Scientists hypothesize that ECMs oxidize organic matter in the soil, thereby releasing nitrogen and leading to improved plant nutrition, but direct empirical evidence for this is lacking [4243][4344]. A quantitative field assessment of the uptake of organic nitrogen by ECM fungi would be an important advance in understanding the potential extent of this phenomenon.
Most ectomycorrhizal (ECM) fungi are characterized by the absence of invertase [4445][4546], which distinguishes them from phytopathogenic [4647] and ericaceous mycorrhizal fungi [4748]. The ability of plants and root microorganisms to respond to nutrient deficiency was investigated by Calvaruso et al. [4849]. They found that plants and their microbial partners can alter their life cycles within limits to maintain an appropriate level of inorganic nutrient availability [4950][5051].
There are several views that ectomycorrhizal (ECM) fungi differ in their ability to supply their host plants with nitrogen fixed in soil organic matter and that this ability can affect soil carbon storage both positively and negatively [5152]. At the same time, it remains unclear whether all ECM taxa can store the nitrogen fixed in soil organic matter [4344][5253]. Recent studies suggest that ECMs alter organic matter stocks differently in different soil horizons [5354], which may be related to differences in the surrounding biotic communities [5455]. This remains a largely unexplored ecological aspect that may have important consequences for plant growth, as well as soil carbon and nitrogen cycling.
The ability to accumulate heavy metals and promote the survival and growth of tree species on degraded soils has been studied by many scientists, who have emphasized that the economic efficiency of the application of mycorrhizal fungi in these areas can have long-term results [55][56][57][58].
Adaptive tolerance to Cd is a rare phenomenon in plants and their symbiotic partners [5859][5960]. The accumulation of this and other heavy metals in plants impairs the expression of their genes [6061], suppresses DNA repair [6162], causes a decline in photosynthesis, reduces the uptake of water and nutrients [6263][6364], and leads to visible symptoms of damage, such as chlorosis, growth inhibition, browning of the root tips, and ultimately death [6465].
Krupa and Kozdrój [6566] reported on the positive role of ectomycorrhizal fungi and the bacteria associated with the respective fungal species in the distribution of heavy metals in the roots and shoots of inoculated pines (Pinus sylvestris L.). They investigated the ability to promote the translocation of Zn (II), Cd (II), and Pb (II) in species such as Scleroderma citrinum, Amanita muscaria, and Lactarius rufus [6566][6667].
The double inoculation of pine seedlings with ectomycorrhizae and bacteria of the genus Pseudomonas helped increase the storage capacity of these metals, especially Zn (II). The effectiveness of this approach to protect plants from heavy metals is recommended for use on soils contaminated with heavy metals [6566].
Populations of S. luteus are tolerant to soil contamination with heavy metals (zinc, copper, cadmium, etc.) [6768][6869]. Plants inoculated with S. luteus have adapted to cadmium and accumulate more fruiting body biomass than non-adapted plants, representing a kind of barrier that prevents the translocation of heavy metals into the plant tissue [6970][7071].
Studies carried out in Poland have shown that the concentrations of aluminum (Al), cadmium (Cd), and lead (Pb) in the mycorrhizae formed by the fungal species studied varied greatly, from low to high. The most intensive uptake of cadmium (Cd) was found in the species Amanita muscaria, whereas the highest concentration of aluminum (Al) was found in Thelephora terrestris. The mycorrhizal accumulation of iron (Fe), manganese (Mn), and zinc (Zn) was not significant, but these metals were generally taken up by most fungi [17].
The results of Cejpková’s study [7172] proved the ability to accumulate trace elements in tissues, especially gold (Ag), cadmium (Cd), chlorine (Cl), and zinc (Zn), in species such as I. badia and Thelephora terrestris. The concentrations of these metals in the ECM tissues were significantly higher than in the plant roots. Scientists hypothesize that ECMs benefit the host by forming a protective barrier against heavy metal toxicity [6566].
The species S. cutrinum can be regarded as a source of natural melanin. This fungus has broad insecticidal [7273], antibacterial [7374], antifungal [2829][7475], and antiviral [7576] activity, including radioprotective, thermoregulatory, chemoprotective, antitumor, antiviral, antimicrobial, immunostimulatory, and anti-inflammatory properties [76][77][78][79]. Suillus cutrinum produces cyathin-like antibiotics that inhibit some types of bacteria and fungi [7980]. Scientists have identified effective doses (ED50) of DMVA compounds that can significantly inhibit mycelial growth of Phytophthora palmivora and Colletotrichum gloeosporioides at concentrations of 58 and 81 μg/mL, respectively [7475][7576].
The ability to produce substances with steroidal character is characteristic of the species S. citrinum, which are natural inhibitors against the phytopathogenic fungi Phytophthora palmivora and Colletotrichum gloeosporioides [8081]. The species I. badia (Fr.) is rich in antioxidant compounds [8182][83]. It contains vitamins, especially those of the B group, as well as macro- and microelements [8284], which show antibacterial or antifungal activity. Mycorrhizal fungi belonging to the genus Suillus, as well as the species Gomphidius roseus, Rhizopogon luteolus (III phase), Laccaria laccata, Boletus luridus, and Cortinarius vibratilis, intensively process auxins like IAA. The genera Hebeloma, Tricholoma, and Xerocomus (Imleria) and the species Rhizopogon rubescens and Cenococcum graniforme are characterized by lower productivity of IAA. Auxins were not detected in the mycelium of all analyzed fungi of the genera Amanita, Lactarius, Russula, and Cortinarius (except C. vibratilis), in five Tricholoma species, and in Scleroderma verrucosum, S. aurantium, Collybia butyracea, and Mycens pura. The absence of IAA in the mycelium does not always mean that the fungus is unable to produce these compounds, as some fungal species do not accumulate them in the mycelium but release them into the environment. This has been observed in several Amanita species, as well as in Lactarius rufus, Cortinarius armillatus, and Hygrophorus hypothejus [2324].
Colpaert et al. [6768] compared the effect of Thelephora terrestris (Ehr.) Ft., Suillus bovinus (L.: Fr.) O. Kuntze, and Scleroderma citrinum Pers. on the carbon and nitrogen uptake of mycorrhizal and non-mycorrhizal seedlings of Pinus sylvestris L. grown in a semi-hydroponic system with nitrogen as a limiting growth factor. The authors concluded that mycorrhiza influences the above- and below-ground distribution of nitrogen. Specifically, they found that the mycelium of S. citrinum retains a significant proportion (32%) of the nitrogen supplied to the plants, thereby significantly reducing its assimilation by the host plants.
The ability of mycorrhizal fungi to synthesize various compounds that contribute to the adaptability and development of the host plant, accumulate and retain heavy metals, and influence the distribution of nitrogen could be important for the creation of pine forests on degraded and polluted soils [9][10][6768].

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