
==== Front
Appl Microbiol Biotechnol
Appl Microbiol Biotechnol
Applied Microbiology and Biotechnology
0175-7598
1432-0614
Springer Berlin Heidelberg Berlin/Heidelberg

39249589
13298
10.1007/s00253-024-13298-w
Mini-Review
Mycorrhizal symbiosis and the nitrogen nutrition of forest trees
http://orcid.org/0000-0002-7985-6906
Pena Rodica rodica.pena@reading.ac.uk

12
Tibbett Mark 1
1 https://ror.org/05v62cm79 grid.9435.b 0000 0004 0457 9566 Department of Sustainable Land Management, School of Agriculture, Policy and Development, University of Reading, Reading, UK
2 https://ror.org/01cg9ws23 grid.5120.6 0000 0001 2159 8361 Department of Silviculture, Transilvania University of Brasov, Brasov, Romania
9 9 2024
9 9 2024
2024
108 1 46110 7 2024
27 8 2024
28 8 2024
© The Author(s) 2024
2024
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Abstract

Terrestrial plants form primarily mutualistic symbiosis with mycorrhizal fungi based on a compatible exchange of solutes between plant and fungal partners. A key attribute of this symbiosis is the acquisition of soil nutrients by the fungus for the benefit of the plant in exchange for a carbon supply to the fungus. The interaction can range from mutualistic to parasitic depending on environmental and physiological contexts. This review considers current knowledge of the functionality of ectomycorrhizal (EM) symbiosis in the mobilisation and acquisition of soil nitrogen (N) in northern hemisphere forest ecosystems, highlighting the functional diversity of the fungi and the variation of symbiotic benefits, including the dynamics of N transfer to the plant. It provides an overview of recent advances in understanding ‘mycorrhizal decomposition’ for N release from organic or mineral-organic forms. Additionally, it emphasises the taxon-specific traits of EM fungi in soil N uptake. While the effects of EM communities on tree N are likely consistent across different communities regardless of species composition, the sink activities of various fungal taxa for tree carbon and N resources drive the dynamic continuum of mutualistic interactions. We posit that ectomycorrhizas contribute in a species-specific but complementary manner to benefit tree N nutrition. Therefore, alterations in diversity may impact fungal-plant resource exchange and, ultimately, the role of ectomycorrhizas in tree N nutrition. Understanding the dynamics of EM functions along the mutualism-parasitism continuum in forest ecosystems is essential for the effective management of ecosystem restoration and resilience amidst climate change.

Key points

• Mycorrhizal symbiosis spans a continuum from invested to appropriated benefits.

• Ectomycorrhizal fungal communities exhibit a high functional diversity.

• Tree nitrogen nutrition benefits from the diversity of ectomycorrhizal fungi.

Graphical abstract

Keywords

Ectomycorrhizal functional traits
Mutualistic spectrum
Decomposition
Nitrogen cycle
http://dx.doi.org/10.13039/501100000270 Natural Environment Research Council NE/W005816/1 Tibbett Mark http://dx.doi.org/10.13039/501100004406 Universitatea Transilvania din Brasov issue-copyright-statement© Springer-Verlag GmbH Germany, part of Springer Nature 2024
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pmcIntroduction

The holobiont concept, in which plants and their associated microbes are viewed not as independent entities but as a cohesive evolutionary unit, emphasises the vital roles that bacteria, fungi, and other microorganisms play in plant growth, health, and adaptation to various environments (Theis et al. 2016; Uroz et al. 2019). Terrestrial plants associate with mycorrhizal fungi to acquire nutrients (Moreau et al. 2019; Sun et al. 2021). They form a symbiotic relationship based on a nutritional exchange between the partners in a quid pro quo (‘giving and taking’) manner (Almario et al. 2022). Isotope tracing experiments have long demonstrated that there is a transfer of nutrients between partners (Finlay et al. 1989; Le Tacon et al. 2015; Schreider et al. 2022; Khokon et al. 2023; Pena et al. 2023). The mycorrhizal fungus obtains carbon (C) from the plant, which, in exchange, receives soil nutrients, mainly nitrogen (N) and phosphorus (P) from the fungus (Smith and Read 2010; Sun et al. 2021; Martin and van der Heijden 2024).

Mycorrhizal symbiosis is based on reciprocal invested benefits. Both partners invest and benefit from the symbiosis, and the benefit obtained from interaction exceeds the cost of the investment (Connor 1995). While diverse dynamics ranging from mutualism to parasitism can occur in certain contexts, such as early seedling development, high fertilisation conditions, or mismatched plant and fungal genotypes (Johnson et al. 1997), mycorrhizal symbiosis remains at the mutualistic end of the spectrum (Fig. 1a). It can sometimes be regarded as pseudo-reciprocity, where one partner does not invest directly but provides a by-product benefit to the other partner, such as when C is an excess resource for the plant (Corrêa et al. 2012), or when plants invest in the formation of new root tips, which are also utilised by mycorrhizal fungi (Ruotsalainen et al. 2022). In the case of appropriated (i.e. purloined) benefits (Connor 1995), the fungal partner may exploit the C resources of the plant without any direct investment (e.g. providing N). However, despite this parasitic interaction from the perspective of N nutrition, the fungus may also produce other benefits for the host plant (e.g. providing P) that exceed the costs of the appropriated benefits, maintaining a mutualistic symbiosis.Fig. 1 a Benefits of mutualistic ectomycorrhizal symbiosis: reciprocal invested benefits occur when both partners actively invest in each other; by-product benefits arise when one organism (the tree) incidentally benefits the other (the fungus); and appropriated benefits happen when one partner (the fungus) exploits the resources of the other (the plant). b The contribution of ectomycorrhizal (EM) fungi to tree nitrogen (N) nutrition in forest ecosystems: ectomycorrhizas formed with different fungal taxa vary in their abilities to retrieve N from diverse substrates, their mechanisms of organic matter decomposition and their preferences for specific N sources. The allocation of plant carbon (C) to different ectomycorrhizas is influenced by their C/N ratio. When soil N availability decreases, EM fungi may enhance decomposition activities to access N that requires higher C needs. Under severe N limitation, the mutualistic symbiosis may shift towards appropriated N benefits. The fungus optimises its N use efficiency to lower the C/N ratio, thereby securing more C from the plant without transferring the N to the plant. Created with BioRender.com

Of all vascular plant species on earth, approximately 2% (ca. 8500 species) form EM symbiosis and most temperate and boreal tree species, accounting for about 60% of tree stems on earth, may associate with some of the > 20,000 fungal species to form ectomycorrhizal (EM) symbioses (Brundrett and Tedersoo 2018; Steidinger et al. 2019). In this symbiosis, plant and fungal cells are reprogrammed to form a specialised root structure, the ectomycorrhiza, which facilitates the uptake and transfer of nutrients (Hacquard et al. 2013; Garcia et al. 2016; Nehls and Plassard 2018). The EM fungus forms a sheath around the colonised root tip (i.e. mantle) from which the mycelium extends bidirectionally into the root apoplastic space and surrounding soil. In the root, the fungus wraps around each cortical cell to create a ‘Hartig net’ (named after Theodor Hartig, who in 1842 described the net but wrongly interpreted it to be plant tissue, Hacskaylo 2017; Sportes et al. 2021). The Hartig net forms the symbiotic interface, where carbohydrate and nutrient exchange between plant and fungal cells take place via transporters. In the soil, the extraradical mycelium extends over varying distances, displaying a diverse range of morphologies depending on the fungal species. The EM extraradical mycelium has been classified into four main soil exploration types based on the extent, differentiation, and quantity of hyphae emanating from the mantle (Agerer 2001). The ‘contact’ exploration type features a smooth mantle, with only a few emanating hyphae primarily involved in nutrient exchange directly at the root interface. The ‘short-distance’ exploration type extends hyphae a short distance from the root surface, forming a compact network that enhances nutrient acquisition within the root depletion zone. The ‘medium-’ to ‘long-distance’ exploration types have hyphae that extend further, forming extensive networks, sometimes involving rhizomorphs that can spread considerably, accessing nutrients from a larger volume of soil beyond the root depletion zone. In natural forests, nearly all fine absorptive roots develop into ectomycorrhizas (Pena et al. 2010, 2017), making EM roots the primary nutrient-absorbing structures for these trees (Martin and van der Heijden 2024). They play a crucial role in major ecosystem functions by influencing tree nutrient acquisition under nutrient-limited conditions (Smith and Read 2010; Henriksson et al. 2021) and contributing to organic matter decomposition (Lindahl and Tunlid 2015; Fernandez and Kennedy 2016; Zak et al. 2019; Lindahl et al. 2021). Additionally, they aid in soil C stabilisation through their recalcitrant mycelium (Clemmensen et al. 2015; Fernandez and Kennedy 2018; Maillard et al. 2023a; Hagenbo et al. 2024).

Recent large-scale comparative genomics, coupled with gene expression studies and classical physiological assessments, have revealed significant differences in functional traits among EM taxa (Miyauchi et al. 2020; Khokon et al. 2023; Maillard et al. 2023b; Auer et al. 2024). Although mycorrhizal relationships predominantly remain mutualistic, Frank’s 1885 definition, which asserts that fungi provide host plants with nutrients (Frank 2005), requires refinement. This is necessary to account for functional variation among individual fungal species (Clemmensen et al. 2021; Lebreton et al. 2021; Lindahl et al. 2021) and differing growth conditions (Henriksson et al. 2021). This review synthesises recent advances in our understanding of the dynamics of EM symbiosis in terms of resource acquisition and exchange. It emphasises the role of EM in enhancing tree N nutrition in the large context of varying soil N availability.

Nitrogen is an essential element whose availability regulates primary productivity and organic matter decomposition in terrestrial ecosystems (LeBauer and Treseder 2008; Vitousek et al. 2010). In Northern Hemisphere forests, the low availability of biological N forms is a major factor limiting plant growth (LeBauer and Treseder 2008). In the short term, N availability is driven by the balance between supply and demand (von Sperber et al. 2017). Under low supply, strong plant and microbial demands result in rapid uptake and immobilisation of any available N, aggravating the limitation (von Sperber et al. 2017). Ectomycorrhizal fungi work as nutrient miners and scavengers-carriers (sensu Cao et al. 2024) and are involved in both the supply and demand chains. In the supply chain, they are mobilising N from organic matter as ‘mycorrhizal decomposers’(Lindahl and Tunlid 2015; Lindahl et al. 2021; Martin and van der Heijden 2024). In the demand chain, EM fungi acquire nutrients for the use of themselves and their host trees, becoming some of the strongest N competitors in the forest ecosystems (Wallenda and Read 1999; Pena et al. 2013; Bödeker et al. 2016; Auer et al. 2024).

In the following sections, we summarise the key findings on the EM fungal role in the mobilisation and acquisition of soil N, highlighting the functional diversity of EM fungi (Fig. 1b). Finally, we discuss the variation of mutualism benefits, including the dynamics of N transfer to the plant.

Contribution of ectomycorrhizas to organic N mobilisation

In most forest soils, up to 95% of N exists in organic form. Before stabilisation in the soil matrix and if not taken up by plants, organic N cycles between microbial biomass and residues, adsorption and desorption from soil mineral particles, and dissolution and precipitation from the soil solution, as described by Bingham and Cotrufo (2016). Organic N enters the soil through plant litter, and root, animal and microbial necromass, as well as dissolved organic N from root exudates and plant litter leachates. The labile N compounds, such as free amino acids or peptides, are rapidly immobilised by microorganisms and plants (Neff et al. 2003; Schimel and Bennett 2004). The remaining organic N, consisting of polymeric structures, is commonly complexed with degradation organic products or mineral particles and must undergo depolymerisation or mineralisation to become available to plants (Nannipieri and Paul 2009; Bingham and Cotrufo 2016; Jilling et al. 2018). In N-poor ecosystems, where organic N-use by plants is common, depolymerisation is the most limiting process in N accessibility (Schimel and Bennett 2004; Näsholm et al. 2009). Saprotrophic fungi and bacteria are recognised as efficient decomposers of organic biopolymers in the soil (López-Mondéjar et al. 2018, 2020). However, some EM basidiomycetes have the ability to secrete extracellular enzymes and low molecular weight (LMW) metabolites to solubilise a range of compounds from simple proteins to chitin, polymerised lignin, and mineral-protein complexes (Tibbett et al. 1999; Shah et al. 2013, 2016; Wang et al. 2020, 2021). In contrast with saprotrophs, which utilise soil organic matter as a source of metabolic C, ‘mycorrhizal decomposition’ results in N mobilisation (Lindahl and Tunlid 2015; Nicolás et al. 2019; Clemmensen et al. 2021). EM fungi use the plant C supply to carry out the co-metabolic decomposition of complexed organic N, releasing N (Hobbie et al. 2013; Lindahl and Tunlid 2015; Nicolás et al. 2019). Shah et al. (2016) propose that during EM evolution, the ancestral decay mechanisms used to obtain C have been changed to obtain N. Given that EM fungi evolved multiple times within different clades of saprotrophs, there are large variations in the genetic potential to decay soil organic matter among EM fungal lineages (Kohler et al. 2015; Miyauchi et al. 2020; Looney et al. 2022; Wu et al. 2022).

The genomes of many EM basidiomycetes retain a reduced set of genes encoding enzymes involved in organic matter decomposition, as compared to saprotrophs. These enzymes are commonly found in decaying mechanisms of white-rot and brown-rot saprotrophic fungi (reviewed in Lebreton et al. 2021). The white-rot fungi mainly degrade the exposed lignocellulose surfaces via extracellular oxidative enzymes, including phenol oxidases such as laccases and class II peroxidases (e.g. lignin peroxidases, manganese peroxidases, or versatile peroxidases) and various hydrolytic carbohydrate-active enzymes (CAZymes) (Janusz et al. 2017). Brown rot fungi evolved from white-rot fungi by losing many of their oxidoreductases and CAZymes as they have developed a less energy-demanding LMW catalytic mechanism based on a Fenton system for generation of hydroxyl radicals (Eastwood 2014; Goodell 2020). These hydroxyl radicals can rapidly depolymerise and then repolymerise lignin in a modified form, which is available for a delayed enzymatic attack (Goodell 2020).

Spectroscopic and genome-wide transcriptome analysis confirmed that EM fungi representing different origins of symbiosis within a white-rot (Agaricales), brown-rot (Boletales), or mixed (Atheliales–Amylocorticales) decomposer clades may retrieve N from soil organic matter extracts using oxidative mechanisms (Shah et al. 2016). Organic matter oxidation is possible as a co-metabolic process (Lindahl and Tunlid 2015) only when C is supplied (i.e. glucose) (Rineau et al. 2013; Shah et al. 2016; Nicolás et al. 2019). Ectomycorrhizal fungi also engage in Fenton-based decomposition of organic matter, similar to brown-rot fungi (Rineau et al. 2012; Shah et al. 2016, 2020). However, the specific mechanisms of Fenton chemistry may vary among different EM fungi (Shah et al. 2020). In an in vitro experiment involving five EM fungal species from different symbiotic origins, all species modified the organic extracts to varying extents, utilising different sets of transcripts (Shah et al. 2016). In a follow-up experiment, Nicolás et al. (2019) demonstrated that the mechanisms of N mobilisation from organic matter extracts differed significantly between Paxillus involutus (Boletales) and Laccaria bicolor (Agaricales), reflecting their evolutionary origins of brown-rot and litter-decomposing fungus, respectively. Paxillus involutus used a time-separated two-step mechanism consisting of oxidation and hydrolysis, whereas Laccaria bicolor employed a one-step mechanism that combined the activities of oxidative and hydrolytic enzymes (Nicolás et al. 2019). In both fungi, the availability of C and inorganic N in the culture media governed N mobilisation from the soil organic matter extracts. Decomposition and liberation of organic N decreased under C limitation and started only after the inorganic N (i.e. ammonium) was depleted (Nicolás et al. 2019). In P. involutus, oxidation was controlled by N limitation and hydrolysis by C limitation. In L. bicolor, the one-step mechanism was initiated by N limitation and sustained during C limitation. Based on the transcriptional pattern, where a gene encoding a sugar transporter and several plant cell wall-degrading enzyme (PCWDE) genes were upregulated, the authors suggested that L. bicolor may have the capacity to assimilate C released during organic matter decomposition (Nicolás et al. 2019). This capability is evident, at least when the fungus is not engaged in symbiosis (Martin et al. 2008). The role of N availability in triggering ‘mycorrhizal decomposition’ was also observed in the field, where ammonium addition led to the downregulation of manganese peroxidase genes in the genus Cortinarius (Bödeker et al. 2014; Pellitier and Zak 2021; Argiroff et al. 2022). Nevertheless, the control exerted by C availability on ‘mycorrhizal decomposition’ indicates that organic N mobilisation involves energetic costs that are commonly supported by trees on the reciprocal investment benefit mutualism. The benefits provided by the fungus should outweigh the cost of plant C investment to avoid a change leading to appropriated benefits or even parasitism (Näsholm et al. 2013; Baskaran et al. 2017; Ågren et al. 2019).

In contrast with the PCWDE gene copy number, which is higher in the saprotrophic than EM fungal genomes, the proportion of genes encoding for microbial cell wall degrading enzymes (MCWDEs) is similar between EM and saprotrophic fungi (Miyauchi et al. 2020). Recently, Auer et al. (2024) have shown that in situ EM fungi most strongly expressed the genes encoding for enzymes that act on chitin, such as GH18 (chitinases) and GH20 (b-N-acetylglucosaminidases). The ability of EM fungi to access N-containing polymers such as chitin or chitosan has been described for numerous species (Maillard et al. 2023b). Some species, such as Boletus edulis, Imleria badia, Suillus luteus, and Hebeloma cylindrosporum, are particularly efficient in mobilising N from chitin (Maillard et al. 2023b). This phenomenon is particularly important as fungal mycelium necromass is a large component of soil organic matter (Awad et al. 2019; Hagenbo et al. 2024).

A large fraction (e.g. 45% in boreal forest soil) of soil organic N exists as proteinaceous compounds associated with mineral particles (Jilling et al. 2018; Kramer and Chadwick 2018). Recent works indicate that EM fungi of different phylogeny and ecology can mobilise N from iron oxide mineral-associated proteins (Wang et al. 2020, 2021; Krumina et al. 2022). They use a proteolytic mechanism based on the formation of enzyme–substrate complexes at the mineral surfaces that enables protein hydrolysis without initial desorption of the proteins (Wang et al. 2020). Furthermore, reports from culture studies show that fungi assimilate about 30 to 50% of N from ferrihydrite- or goethite-associated bovine serum albumin (Wang et al. 2021). Although field studies are lacking, the ability of EM fungi to proliferate in deeper soil layers (Lindahl et al. 2007; McGuire et al. 2013; Clemmensen et al. 2021) where mineral-associated organic N is abundant (Jilling et al. 2018) and their high capacity to produce extracellular proteases (Shah et al. 2013; Nicolás et al. 2019) suggest that retrieving N from mineral-complexed proteins is important in N-limited forest ecosystems. Table 1 presents a comprehensive summary of recent findings on the abilities of distinct EM fungi to acquire N by decomposing organic substrates. Table 1 Ectomycorrhizal fungal capabilities in organic matter degradation for nitrogen (N) retrieval

Fungus	N source/involved mechanisms	Measurement methods	Reference	
Paxillus involutus	Soil organic matter/oxidative decomposition by Fenton chemistry	Infrared spectroscopy, chromatography,

mass spectrometry

	Rineau et al. (2012); Shah et al. (2016)	
Iron mineral-associated proteins/protein hydrolysation at the mineral surface without initial desorption	Isotopic analyses,

infrared spectroscopy

	Wang et al. (2020, 2021); Krumina et al. (2022)	
Suillus luteus	Soil organic matter/oxidative decomposition by Fenton chemistry	Infrared spectroscopy, chromatography,

mass spectrometry

	Shah et al. (2016)	
Cortinarius sp.	Lignin/Mn-peroxidase activity	Analysis of Mn-peroxidase activity	Bödeker et al. (2014)	
Laccaria bicolor	Soil organic matter/oxidative decomposition	Infrared spectroscopy	Shah et al. (2016)	
Piloderma croceum	Soil organic matter/oxidative decomposition	Infrared spectroscopy	Shah et al. (2016)	
Hebeloma cylindrosporum	Iron mineral-associated proteins/protein hydrolysation	Isotopic analyses,

infrared spectroscopy

	Wang et al. (2021)	
Imleria badia	Exogenous chitin/chitin hydrolysation	Measurements of 15N fungal enrichments, obtained by feeding the fungus with 15N labelled chitin	Maillard et al. (2023a, b)	
Boletus edulis	
Suillus luteus	
Hebeloma cylindrosporum	

The combination of fungi’s genetic potential for organic matter degradation with their ecological strategies explains the fungal functional traits of active EM fungi in mobilising N (Maillard et al. 2023b; Auer et al. 2024). While species may exhibit similar genetic patterns of genes involved in decomposition, their expression can vary depending on fungal ecology (Barbi et al. 2016). More versatile species that readily adapt to diverse decomposing substrates may possess a high number of decomposition-related genes but exhibit lower expression levels compared to more specialised species, which may show high expression of ‘keystone functional genes’ (Barbi et al. 2016). For example, some ‘long-distance-exploration type’ EM fungi oxidise organic matter and retrieve N more effectively than some ‘short-’ and ‘medium-distance-exploration’ types. This is despite all of them possessing genes encoding oxidative enzymes (Shah et al. 2016). Fungal decomposition capabilities, such as enzyme activities (Courty et al. 2010; Talbot et al. 2015) and accessing N from specific sources (Chen et al. 2019), vary less among phylogenetic lineages of fungi than among species with different ecologies (Tables 1 and 2). Additionally, Op De Beeck et al. (2020) demonstrated that genetically identical hyphal tips can exhibit differences in decomposition activity at the single-cell level within the mycelium. Thus, the environmental conditions, particularly the chemical properties and the availability of the substrates, are major drivers of EM fungal traits in N mobilisation (Shah et al. 2013). Table 2 Preferences of ectomycorrhizas (EM) for uptake of inorganic N from different sources

Fungus	N source preference	Methods	Reference	
Beech (Fagus sylvatica)	
  Clavulina cristata	NH4+	Measurements of 15N EM enrichments, obtained by feeding the plants with NH4NO3 labelled with either 15NH4+ or 15NO3−	Khokon et al. (2023)	
  Tomentella ramosissima,	
  Inosperma maculatum	
  Xerocomus chrysenteron	
  Genea hipidula	
  Helotiales	NO3−	
  Tomentella stuposa	
  Humaria hemisphaerica	
Douglas-fir (Pseudotsuga menziesii)	
  Lactarius rubrilacteus	NH4+	Microelectrode ion flux measures	Kranabetter et al. (2015)	
  Piloderma sp.	
  Tomentella sp.	
  Lactarius cf. hepaticus	
  Lactarius luculentus	
  Russula chloroides	
  Tomentella sublilacina	

Contribution of ectomycorrhizas to inorganic N acquisition

In symbiosis, the mechanism of nutrient uptake depends on both plant and fungal nutritional status and their reciprocal influence (Sa et al. 2019; Rivera Pérez et al. 2022). Similarly to plants, EM fungi take up N from the soil in its oxidised (NO3−) and reduced (NH4+) form or as soluble organic N mono- and oligomers (Talbot and Treseder 2010; Courty et al. 2015; Garcia et al. 2016). In a direct comparison between EM and non-mycorrhizal root tips, the uptake of NH4+, measured as N fluxes at the EM mantle surface, is consistently 10 to 60 times higher in the ectomycorrhiza of various EM fungal species compared to non-mycorrhizal root tips (Hawkins and Kranabetter 2017; Hawkins and Robbins 2022). However, variation may occur in NO3− uptake or when inorganic N availability is high (Hawkins and Kranabetter 2017; Xie et al. 2021). Nevertheless, the N fluxes measured in EM are generally higher than those in non-mycorrhizal roots (Gobert and Plassard 2002). The majority of EM fungi are particularly effective in accessing N from NH4+ (Kranabetter et al. 2015; Leberecht et al. 2016a, 2016b; Hawkins and Robbins 2022; Khokon et al. 2023), which is less mobile than NO3− due to its adsorption onto soil cation exchange sites (Tinker and Nye 2000). This role is crucial in more acidic, cold, or poorly aerated soils where NH4+ dominates, as these conditions do not favour nitrification (Marschner 2011).

In N-rich temperate forests, such as the coastal rainforests of North America, high rates of N mineralisation may lead to elevated levels of soil inorganic N. In these ecosystems, EM fungal communities are predominantly composed of species with high NH4+ uptake capacity (e.g. Lactarius hepaticus, Tomentella sublilacina, Tylospora sp., Kranabetter et al. 2015). The formation of ectomycorrhiza stimulates the expression of NO3− transporters and NH4+ transporters, as well as transporters for amino acids and peptides in both plant and fungi (Müller et al. 2020; Sun et al. 2021). While EM fungi possess only a limited number of high-affinity NO3− transporters, they are equipped with both low and high-affinity NH4+ transporters (Garcia et al. 2016). The combination of both enables effective regulation of NH4+ uptake in response to varying soil concentrations, which likely contributes to their adaptability in N-rich environments. In the fungus, the transcriptional profile related to nutrient acquisition and transport differed between compartments. The most upregulated genes are found in the EM extraradical mycelium and the mantle, which also plays a role in nutrient storage. In contrast, the most downregulated genes, including some that are completely switched off, are observed in the Hartig net at the plant-fungal interface. This complete downregulation may represent an efficient strategy to prevent the fungal reuptake of N (e.g. ammonia, amino acids) from the apoplastic space, ensuring that N remains available for transfer to the plant (Hacquard et al. 2013; Le Tacon et al. 2015).

One of the main contributions of EM fungi to N acquisition is their ability to extend the extraradical mycelium beyond the nutrient depletion zone surrounding the roots. This extension allows them to access nutrients from a larger soil volume, compensating for the plant’s limited ability to absorb nutrients at rates faster than their loss into the surrounding soil (Pena 2016). In boreal and temperate forest ecosystems, EM mycelium comprises one-third of microbial biomass (Awad et al. 2019; Hagenbo et al. 2024). Extraradical mycelium exploration types (Agerer 2001) have long been considered to be EM traits that explain spatial foraging patterns related to resource spatial availability and acquisition (Hobbie and Agerer 2009; Zak et al. 2019). However, a recent and comprehensive study by Jörgensen et al. (2023) demonstrated that there is little support for using the external mycelium exploration type to predict EM foraging strategy. Instead, the study, along with findings by Anthony et al. (2022), found that species exhibit preferences for nutritional substrates, which can be correlated with certain degrees of hyphal hydrophobicity and nitrophobicity. Taxa with high extraradical biomass, classified as the ‘medium- and long-distance-exploration’ type, are not necessarily the most prolific. Their biomass may be sustained by a lower turnover rate (Jörgensen et al. 2023). The majority of low-proliferating taxa are nitrophobic and hydrophobic, commonly associated with inorganic N-limited environments where N acquisition from organic sources is required (Pellitier and Zak 2021; Jörgensen et al. 2023). In contrast, in a temperate forest, under relatively high atmospheric N inputs (beech forest, 13.8–16.6 kg N ha−1 year−1, Khokon et al. 2023) or in an N-rich coastal rainforest (Kranabetter et al. 2015), EM fungal communities are dominated by neutrophilic species with contact and medium smooth exploration types. Some EM fungi, in beech communities, may contribute to the uptake of NO3−, reducing NO3− accumulation and preventing subsequent leaching (Mrak et al. 2024). Nevertheless, the species within these communities exhibited significant variation in N uptake of NH4+ or NO3− (Khokon et al. 2023), corroborating previous findings of substantial variability in fungal abilities for N acquisition. Table 2 highlights the diversity among ectomycorrhizas in N acquisition from various sources.

A recent metatranscriptomic study revealed that the impact of the EM community on tree N nutrition was similar and consistent across different fungal communities despite being composed of different taxa. The authors have suggested that functional redundancy exists among ectomycorrhizas (Auer et al. 2024). Evidence from other studies also suggests that communities, assembled through environmental filtering, are dominated by species best equipped to utilise the most available N source in their environment (Kranabetter et al. 2015). Moreover, endemic EM fungi are better adapted than cosmopolitan species at exploiting available N sources, indicating a high level of specialisation in enhancing tree access to available N (McPolin et al. 2024). On a global scale, the composition of EM fungal communities has been shown to account for a threefold variation in tree growth (Anthony et al. 2022). In contrast, Khokon et al. (2023) found that the positive relationship between EM fungal diversity and tree N acquisition does not correlate with any particular taxa, suggesting that specific traits of fungal species do not solely explain root N acquisition. This indicates that ectomycorrhizal communities contribute to tree N nutrition in a species-specific but complementary manner. A high EM functional diversity in abilities to access distinct or spatially scattered N sources forms the basis for improved N acquisition. We may consider physiological and functional flexibility, even within a single mycelial network, and adaptability to the edaphic environment to be within the limits of the reciprocal invested benefits (Cairney and Burke 1996). For example, in an EM assemblage, distinct EM taxa activate their N uptake abilities to benefit the tree when abiotic conditions are limiting, but not when the tree is unstressed (Pena and Polle 2014). Sustaining high EM fungal biodiversity is critical for tree N nutrition under current and future climate scenarios. However, maintaining the reciprocal investments and benefits of mutualistic interactions has sensitive limits. As EM fungal community size increases, this sensitivity may also rise, potentially leading to pseudo-reciprocity, appropriated benefits, or parasitism.

C and N resources in the ectomycorrhizas

The tree plays an intrinsic role in EM-mediated N nutrition, either by decoupling its N metabolism from fungal metabolism (Leberecht et al. 2016a; Rivera Pérez et al. 2022), or by modulating C allocation to ectomycorrhizas. The maintenance of diverse EM communities depends on the tree’s C supply (Pena et al. 2010). Furthermore, EM fungi that receive more C can colonise more root tips compared to those receiving less carbon (Pena et al. 2023). In other nutritional symbioses, such as the arbuscular mycorrhizal (Kiers et al. 2011) or legume–rhizobium (Simms et al. 2006) symbioses, the nutrient flux between partners follows the market exchange theory, with the plant allocating more C to the partner that provides the most nutrients. In ectomycorrhizas, at the cellular scale, the fungal-acquired soil N is spatially correlated with the plant photo-assimilated C transferred to the fungus (Mayerhofer et al. 2021). However, there is no quantitative correlation between the two fluxes (Valtanen et al. 2014; Hortal et al. 2017; Plett et al. 2024). Nevertheless, a strong relationship exists between the C supply and the taxon-specific C/N ratio of ectomycorrhiza, with the C supply decreasing as the C/N ratio increases. No C supply occurs when C/N is high (C/N > 24, Pena et al. 2023). This indicates that the plant-fungus exchange is not linear. The plant controls C allocation based on N content of the ectomycorrhiza, while fungal traits for N use efficiency, which determine N uptake and immobilisation in the fungus, provide feedback control on plant C allocation (Pena et al. 2023). EM feedback probably varies depending on environmental conditions and nutrient availability. A critical situation can arise under N-limitation when EM fungi take up and immobilise N in their biomass without supplying it to the trees, while continuously receiving C from them. Fungal-supplied N is correlated to the concentration of free amino acids in EM extraradical mycelium (Plett et al. 2024). In boreal forests, several studies suggest that high C allocation to symbionts enables greater fungal N immobilisation, negatively affecting soil N availability and forest N cycling (Hasselquist et al. 2016; Högberg et al. 2017; Henriksson et al. 2021).

According to Pena et al. (2023), different ectomycorrhizas form distinct plant-C sinks depending on their C/N ratio but also represent species-specific sinks of plant-assimilated N. In angiosperm plants, N absorbed from the soil is primarily assimilated into amino acids in the leaves. These amino acids are then redistributed to developing organs via the phloem, serving as the primary N source for root growth (Yoneyama et al. 2003). Internal N availability regulates tree N uptake (Rennenberg and Dannenmann 2015) and influences tree N-acquisition strategies, such as root proliferation to exploit soil N hotspots (Chen et al. 2018). In a recent study, using secondary ion mass spectrometry (SIMS) imaging combined with leaf labelling of young beech with 15NH4+, plant-derived N was found to be present in the fungal tissue within ectomycorrhizas (Pena et al. 2023). The 15N enrichment in the lateral rootlets was also correlated with the enrichment found in the attached ectomycorrhizas, which was further correlated with their C/N ratio. Ectomycorrhizal fungi can capture the plant-assimilated N either from the root apoplast at the symbiotic interface or by recapturing it after exudation. In the first scenario, EM fungal intervention is less likely because the presence of fungal amino acid transporters at the symbiotic interface could intercept the N influx, destabilising the symbiosis functionality (Martin & Nehls 2009, but see Garcia et al. 2016). Nevertheless, the second scenario is more probable, as EM fungi can uptake amino acids from the soil (Garcia et al. 2016). Given that the fungal mantle tightly encapsulates the EM root tip, EM fungi are favoured over other soil microorganisms in accessing plant-exuded N (Canarini et al. 2019). By intercepting the root N efflux, EM fungi reduce the supplementary N source available for rhizosphere microorganisms (Jones et al. 2004; Canarini et al. 2019). This functional trait of EM fungi, either creating a distinct sink for plant-assimilated N or recapturing the plant-exuded N, is crucial for tree N nutrition. It provides the basis for EM-regulated N fluxes within the root system and directly affects the plant’s priming capacity by modifying the exudate C/N stoichiometry. This latter aspect is important, as microorganism activity is commonly constrained by both C and N availability (Jones et al. 2004; Drake et al. 2013).

Ectomycorrhizal fungi enhance tree N nutrition via microbiome influence

The role of EM fungi in plant nutrition also includes an indirect component, as they positively influence other soil microorganisms (e.g. bacteria, archaea) involved in N cycling, thereby enhancing plant N uptake (Frey-Klett et al. 2007; Lladó et al. 2017; Uroz et al. 2019). Mycorrhizal symbiosis creates new niches for microorganisms by modifying the plant’s ecophysiological traits and local soil properties (Uroz et al. 2019). Specifically, EM fungi construct a unique compartment of the mycorrhizosphere—the immediate space surrounding the external EM hyphae influenced by root and hyphal exudates. This compartment provides space and nutrients for a range of microbial communities (Johansson et al. 2009; Bogar and Peay 2017; Gorka et al. 2019). For example, the mycorrhizospheres of Pinus sylvestris (Rinta-Kanto and Timonen 2020) and Pinus muricata (Nguyen and Bruns 2015) are populated with Actinobacteria and Planctomycetia, which can break down recalcitrant organic substrates (e.g. chitin) to retrieve N, and Burkholderiales, which are involved in N fixation (Elliott et al. 2007).

A much deeper analysis of Pinus sylvestris (Marupakula et al. 2016) or Fagus sylvatica (Dietrich et al. 2022) EM root tips revealed that distinct EM fungi harbour distinct communities of bacteria. Furthermore, rare fungal taxa play a role similar to that of the most abundant taxa in driving the assembly of new microbial communities (Dietrich et al. 2022). These findings highlight the importance of maintaining a high mycorrhizal diversity. High functional diversity is essential to foster the formation of diverse associated microbial communities that enhance N cycling and plant N nutrition. Further research is needed to understand how the functional benefits of EM fungi can remain unaffected by environmental changes and disturbances, ensuring sustained plant growth and soil health.

Future perspectives

Understanding the dynamics of EM functions along the mutualism-parasitism continuum in forest ecosystems is essential for the effective management of ecosystem restoration and resilience amidst climate change. Variation in mutualistic species interactions is common in nature, particularly in mycorrhizal symbiosis, which involves a bidirectional energy transfer –C from plants to fungi and N or other nutrients from fungi to plants. This variation is often described as context-dependent, influenced by changes in biotic factors, such as the involvement of additional species, and abiotic factors, such as resource availability or abiotic stress (Chamberlain et al. 2014) (Fig. 1b).

In the biotic context, the immediate functional groups that may influence EM symbioses through competition or cooperation with EM fungi include other fungi that occupy the same spatial niche and can transfer N to plants and access plant C resources. Tree roots host rich communities of dark septate endophytic (DSE) fungi that live in plant tissues, producing no symptoms or morphological modifications of their hosts (Hardoim et al. 2015). These ascomycetes have a strong enzymatic potential, enabling them to acquire N from organic sources, which is then transferred to the tree. There is a by-product mutualist interaction in which DSEs provide N without requiring any special structural investment from the host plant (Ruotsalainen et al. 2022). Tree C, which enters the soil as root exudates, or leaf and root litter, is a by-product benefitting the DSE fungi (Ruotsalainen et al. 2022). This interaction is considered a transitional phase in the evolution of mycorrhizal symbionts from saprotrophic fungi (Ruotsalainen et al. 2022). Reports on the interaction between DSE and EM fungi are currently limited and exhibit significant variability, ranging from neutral to competitive or facilitative interactions, largely depending on the fungal strains involved (Reininger and Sieber 2012; Berthelot et al. 2019). Notably, these findings are derived from in vitro experiments (Berthelot et al. 2019) and growth chamber studies with seedlings (Reininger and Sieber 2012), with no data available from field studies. Future research should prioritise field investigations to better understand the effects of DSEs on EM symbioses in natural settings and their implications for tree nutrition.

A special type of root endophyte involved in plant N acquisition is the soil ascomycetes fungi, such as Beauveria sp. (Cordycipitaceae) and Metarhizium sp. (Clavicipitaceae), which function as both endophyte and insect pathogens and can acquire N from soil insects and transfer it to the plant in exchange for C (Hu and Bidochka 2021; Bamisile et al. 2023). Their role in plant N nutrition was first described in 2012 (Behie et al. 2012). However, there are no reports on their interaction with other root fungi or whether their N-transfer abilities might affect the effectiveness and stability of mycorrhizal symbioses, which also deliver N to the plants.

Apart from fungi that reside in the same root with EM fungi, there are also feremycorrhizal fungi, meaning ‘nearly mycorrhizal.’ These fungi exhibit traits and functions similar to those of EM fungi but do not penetrate the roots (Kariman et al. 2014). Unlike EM symbiosis, no investment from the plant is required. Thus, feremycorrhiza is a by-product interaction that may interfere with mycorrhizas, potentially affecting their mutualistic relationship with the host plant.

In the abiotic context, EM mutualism can be influenced by current changes in soil nutrient levels. Historically, N has been a limiting factor in forest ecosystems of the Northern Hemisphere. However, due to anthropogenic activities, the global availability of N has increased to unprecedented levels, disrupting the context of low N supply and tight recycling (Galloway et al. 2008). Along natural fertility gradients, in boreal forests, increased N availability may have a positive effect on mycelium growth and species richness (Kranabetter et al. 2009a, 2009b; Högberg et al. 2021). In temperate N-rich forests, EM fungal communities remain diverse, with no apparent decline in diversity observed even under conditions of extreme native soil fertility compared to less fertile environments (Kranabetter et al. 2015). A recent study conducted in boreal forests found that moderate N deposition (5.8 kg N ha−1 year−1) had no impact on EM fungal biomass and community composition (Jörgensen et al. 2024). However, more severe N deposition (e.g. 11.1 kg N ha−1 year−1, Jörgensen et al. 2024) may lead to declines in fungal sporocarps, biomass, abundance, and community diversity. EM fungal communities tend to shift from nitrophobic taxa under moderate N deposition (5.8 kg N ha−1 year−1) to nitrophilic taxa at higher levels (15.5 kg N ha−1 year−1, van der Linde et al. 2018). This shift includes the loss of key functional species, particularly those with high enzymatic capabilities for releasing N from organic sources (reviewed by Lilleskov et al. 2019, 2024). Currently, it remains unclear whether the effects of N deposition on EM fungi differ between communities that are already more nitrophilic due to adaptation to N-rich soils and those from low-N environments. These observations related to N deposition are likely driven by either direct N toxicity stress or by alterations in EM symbiosis. This symbiosis is fundamentally based on the plant’s need for limited nutrients under an invested benefits mutualism. With no N limitation, the symbiosis may become a by-product benefit when plant C supply to fungi is at no expense for the plant or an appropriated benefit when the C supply is costly for the plant.

Changes in soil nutrient stoichiometry, such as P limitation induced by N saturation (Sardans et al. 2016), trigger changes from an N to a P-oriented acquisition strategy mediated by roots and ectomycorrhizas (Meeds et al. 2021; Zhang et al. 2023; Zhu et al. 2023). Averill et al. (2018), using a Bayesian multiple regression framework, found that across the USA, N deposition is linked to a decline in EM tree species, favouring their replacement with arbuscular mycorrhizal tree species. This shift is commonly explained by the fact that arbuscular mycorrhizal fungi primarily rely on inorganic N forms and possess significant abilities in P acquisition.

However, a recent finer-scale metanalysis in the tropics showed that the distribution and abundance of EM and arbuscular mycorrhizal trees are independent of soil nutrient availability (Medina-Vega et al. 2024). The results were supported by an empirical study of Chilian native forests (Lusk et al. 2024). At a plant level, research involving dual plants, capable of forming both arbuscular and EM symbioses, has revealed a certain plasticity in root symbioses to optimise nutrient acquisition under P limitation. However, a direct switch from EM to arbuscular mycorrhizal symbiosis was not apparent (Teste and Laliberté 2019). Under a higher N/P ratio and reduced pressure for N acquisition, EM fungi may benefit from the plant’s ability to allocate more energy toward increasing organic P acquisition through EM fungi or other mechanisms (McPolin et al. 2024), such as enhancing the activity of enzymes involved in P acquisition (Meeds et al. 2021).

Forests cover much of the Earth’s surface, providing crucial ecosystem services. With anthropogenic changes in temperature, precipitation, and N deposition, it is vital to understand the factors influencing the EM nutrient exchange and interactions with soil organisms affecting N supply to plants. Changes in plant-fungal mutualism within ectomycorrhizal symbiosis and reduced EM functional diversity are critical for forest productivity, soil carbon sequestration, nutrient cycling, and climate change feedback. Future studies should identify the factors and mechanisms driving these changes to mitigate their impacts and preserve forest ecosystem services.

Acknowledgements

We gratefully thank Barbara Hawkins for her invaluable assistance in reading and providing feedback on this manuscript. RP extends thanks to Transilvania University of Brașov for the Transilvania Fellowship for Visiting Professors. We thank the anonymous reviewers for their invaluable comments and suggestions, which significantly enhanced the quality and clarity of our manuscript.

Author contribution

RP was responsible for the conceptualisation, literature review, drafting, and manuscript revisions. MT provided critical feedback and assisted with revisions. Both authors approved the final version of the manuscript.

Funding

This work was supported by funding from the Natural Environment Research Council–UKRI (NE/W005816/1).

Data availability

This review paper does not contain associated laboratory data.

Declarations

Ethics approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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References

Agerer R Exploration types of ectomycorrhizae Mycorrhiza 2001 11 107 114 10.1007/s005720100108
Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114. 10.1007/s00572010010810.1007/s005720100108
Ågren GI Hyvönen R Baskaran P Ectomycorrhiza, friend or foe? Ecosystems 2019 22 1561 1572 10.1007/s10021-019-00356-y
Ågren GI, Hyvönen R, Baskaran P (2019) Ectomycorrhiza, friend or foe? Ecosystems 22:1561–1572. 10.1007/s10021-019-00356-y10.1007/s10021-019-00356-y
Almario J Fabiańska I Saridis G Bucher M Unearthing the plant–microbe quid pro quo in root associations with beneficial fungi New Phytol 2022 234 1967 1976 10.1111/nph.18061 35239199
Almario J, Fabiańska I, Saridis G, Bucher M (2022) Unearthing the plant–microbe quid pro quo in root associations with beneficial fungi. New Phytol 234:1967–1976. 10.1111/nph.1806135239199 10.1111/nph.18061
Anthony MA Crowther TW van der Linde S Suz LM Bidartondo MI Cox F Schaub M Rautio P Ferretti M Vesterdal L De Vos B Dettwiler M Eickenscheidt N Schmitz A Meesenburg H Andreae H Jacob F Dietrich H-P Waldner P Gessler A Frey B Schramm O van den Bulk P Hensen A Averill C Forest tree growth is linked to mycorrhizal fungal composition and function across Europe ISME J 2022 16 1327 1336 10.1038/s41396-021-01159-7 35001085
Anthony MA, Crowther TW, van der Linde S, Suz LM, Bidartondo MI, Cox F, Schaub M, Rautio P, Ferretti M, Vesterdal L, De Vos B, Dettwiler M, Eickenscheidt N, Schmitz A, Meesenburg H, Andreae H, Jacob F, Dietrich H-P, Waldner P, Gessler A, Frey B, Schramm O, van den Bulk P, Hensen A, Averill C (2022) Forest tree growth is linked to mycorrhizal fungal composition and function across Europe. ISME J 16:1327–1336. 10.1038/s41396-021-01159-735001085 10.1038/s41396-021-01159-7
Argiroff WA Zak DR Pellitier PT Upchurch RA Belke JP Decay by ectomycorrhizal fungi couples soil organic matter to nitrogen availability Ecol Lett 2022 25 391 404 10.1111/ele.13923 34787356
Argiroff WA, Zak DR, Pellitier PT, Upchurch RA, Belke JP (2022) Decay by ectomycorrhizal fungi couples soil organic matter to nitrogen availability. Ecol Lett 25:391–404. 10.1111/ele.1392334787356 10.1111/ele.13923
Auer L Buée M Fauchery L Lombard V Barry KW Clum A Copeland A Daum C Foster B LaButti K Singan V Yoshinaga Y Martineau C Alfaro M Castillo FJ Imbert JB Ramírez L Castanera R Pisabarro AG Finlay R Lindahl B Olson A Séguin A Kohler A Henrissat B Grigoriev IV Martin FM Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems New Phytol 2024 242 1676 1690 10.1111/nph.19471 38148573
Auer L, Buée M, Fauchery L, Lombard V, Barry KW, Clum A, Copeland A, Daum C, Foster B, LaButti K, Singan V, Yoshinaga Y, Martineau C, Alfaro M, Castillo FJ, Imbert JB, Ramírez L, Castanera R, Pisabarro AG, Finlay R, Lindahl B, Olson A, Séguin A, Kohler A, Henrissat B, Grigoriev IV, Martin FM (2024) Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems. New Phytol 242:1676–1690. 10.1111/nph.1947138148573 10.1111/nph.19471
Averill C Dietze MC Bhatnagar JM Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks Glob Change Biol 2018 24 4544 4553 10.1111/gcb.14368
Averill C, Dietze MC, Bhatnagar JM (2018) Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks. Glob Change Biol 24:4544–4553. 10.1111/gcb.1436810.1111/gcb.14368
Awad A Majcherczyk A Schall P Schröter K Schöning I Schrumpf M Ehbrecht M Boch S Kahl T Bauhus J Seidel D Ammer C Fischer M Kües U Pena R Ectomycorrhizal and saprotrophic soil fungal biomass are driven by different factors and vary among broadleaf and coniferous temperate forests Soil Biol Biochem 2019 131 9 18 10.1016/j.soilbio.2018.12.014
Awad A, Majcherczyk A, Schall P, Schröter K, Schöning I, Schrumpf M, Ehbrecht M, Boch S, Kahl T, Bauhus J, Seidel D, Ammer C, Fischer M, Kües U, Pena R (2019) Ectomycorrhizal and saprotrophic soil fungal biomass are driven by different factors and vary among broadleaf and coniferous temperate forests. Soil Biol Biochem 131:9–18. 10.1016/j.soilbio.2018.12.01410.1016/j.soilbio.2018.12.014
Bamisile BS Afolabi OG Siddiqui JA Xu Y Endophytic insect pathogenic fungi-host plant-herbivore mutualism: elucidating the mechanisms involved in the tripartite interactions World J Microbiol Biotechnol 2023 39 326 10.1007/s11274-023-03780-4 37776438
Bamisile BS, Afolabi OG, Siddiqui JA, Xu Y (2023) Endophytic insect pathogenic fungi-host plant-herbivore mutualism: elucidating the mechanisms involved in the tripartite interactions. World J Microbiol Biotechnol 39:326. 10.1007/s11274-023-03780-437776438 10.1007/s11274-023-03780-4
Barbi F Prudent E Vallon L Buée M Dubost A Legout A Marmeisse R Fraissinet-Tachet L Luis P Tree species select diverse soil fungal communities expressing different sets of lignocellulolytic enzyme-encoding genes Soil Biol Biochem 2016 100 149 159 10.1016/j.soilbio.2016.06.008
Barbi F, Prudent E, Vallon L, Buée M, Dubost A, Legout A, Marmeisse R, Fraissinet-Tachet L, Luis P (2016) Tree species select diverse soil fungal communities expressing different sets of lignocellulolytic enzyme-encoding genes. Soil Biol Biochem 100:149–159. 10.1016/j.soilbio.2016.06.00810.1016/j.soilbio.2016.06.008
Baskaran P Hyvönen R Berglund SL Clemmensen KE Ågren GI Lindahl BD Manzoni S Modelling the influence of ectomycorrhizal decomposition on plant nutrition and soil carbon sequestration in boreal forest ecosystems New Phytol 2017 213 1452 1465 10.1111/nph.14213 27748949
Baskaran P, Hyvönen R, Berglund SL, Clemmensen KE, Ågren GI, Lindahl BD, Manzoni S (2017) Modelling the influence of ectomycorrhizal decomposition on plant nutrition and soil carbon sequestration in boreal forest ecosystems. New Phytol 213:1452–1465. 10.1111/nph.1421327748949 10.1111/nph.14213
Behie SW Zelisko PM Bidochka MJ Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants Science 2012 336 1576 1577 10.1126/science.1222289 22723421
Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577. 10.1126/science.122228922723421 10.1126/science.1222289
Berthelot C Leyval C Chalot M Blaudez D Interactions between dark septate endophytes, ectomycorrhizal fungi and root pathogens in vitro FEMS Microbiol Lett 2019 366 fnz158 10.1093/femsle/fnz158 31295350
Berthelot C, Leyval C, Chalot M, Blaudez D (2019) Interactions between dark septate endophytes, ectomycorrhizal fungi and root pathogens in vitro. FEMS Microbiol Lett 366:fnz158. 10.1093/femsle/fnz15831295350 10.1093/femsle/fnz158
Bingham AH Cotrufo MF Organic nitrogen storage in mineral soil: implications for policy and management Sci Total Environ 2016 551–552 116 126 10.1016/j.scitotenv.2016.02.020 26874768
Bingham AH, Cotrufo MF (2016) Organic nitrogen storage in mineral soil: implications for policy and management. Sci Total Environ 551–552:116–126. 10.1016/j.scitotenv.2016.02.02026874768 10.1016/j.scitotenv.2016.02.020
Bödeker ITM Clemmensen KE de Boer W Martin F Olson Å Lindahl BD Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems New Phytol 2014 203 245 256 10.1111/nph.12791 24725281
Bödeker ITM, Clemmensen KE, de Boer W, Martin F, Olson Å, Lindahl BD (2014) Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytol 203:245–256. 10.1111/nph.1279124725281 10.1111/nph.12791
Bödeker ITM Lindahl BD Olson Å Clemmensen KE Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently Funct Ecol 2016 30 1967 1978 10.1111/1365-2435.12677
Bödeker ITM, Lindahl BD, Olson Å, Clemmensen KE (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol 30:1967–1978. 10.1111/1365-2435.1267710.1111/1365-2435.12677
Bogar LM Peay KG Tedersoo L Processes maintaining the coexistence of ectomycorrhizal fungi at a fine spatial scale Biogeography of Mycorrhizal Symbiosis 2017 Cham Springer International Publishing 79 105
Bogar LM, Peay KG (2017) Processes maintaining the coexistence of ectomycorrhizal fungi at a fine spatial scale. In: Tedersoo L (ed) Biogeography of Mycorrhizal Symbiosis. Springer International Publishing, Cham, pp 79–105
Brundrett MC Tedersoo L Evolutionary history of mycorrhizal symbioses and global host plant diversity New Phytol 2018 220 1108 1115 10.1111/nph.14976 29355963
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. 10.1111/nph.1497629355963 10.1111/nph.14976
Cairney JWG Burke RM Physiological heterogeneity within fungal mycelia: an important concept for a functional understanding of the ectomycorrhizal symbiosis New Phytol 1996 134 685 695 10.1111/j.1469-8137.1996.tb04934.x 33863201
Cairney JWG, Burke RM (1996) Physiological heterogeneity within fungal mycelia: an important concept for a functional understanding of the ectomycorrhizal symbiosis. New Phytol 134:685–695. 10.1111/j.1469-8137.1996.tb04934.x33863201 10.1111/j.1469-8137.1996.tb04934.x
Canarini A Kaiser C Merchant A Richter A Wanek W Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli Front Plant Sci 2019 10 157 10.3389/fpls.2019.00157 30881364
Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:15730881364 10.3389/fpls.2019.00157
Cao T Luo Y Shi M Tian X Kuzyakov Y Microbial interactions for nutrient acquisition in soil: miners, scavengers, and carriers Soil Biol Biochem 2024 188 109215 10.1016/j.soilbio.2023.109215
Cao T, Luo Y, Shi M, Tian X, Kuzyakov Y (2024) Microbial interactions for nutrient acquisition in soil: miners, scavengers, and carriers. Soil Biol Biochem 188:109215. 10.1016/j.soilbio.2023.10921510.1016/j.soilbio.2023.109215
Chamberlain SA Bronstein JL Rudgers JA How context dependent are species interactions? Ecol Lett 2014 17 881 890 10.1111/ele.12279 24735225
Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 17:881–890. 10.1111/ele.1227924735225 10.1111/ele.12279
Chen W Koide RT Eissenstat DM Nutrient foraging by mycorrhizas: from species functional traits to ecosystem processes Funct Ecol 2018 32 858 869 10.1111/1365-2435.13041
Chen W, Koide RT, Eissenstat DM (2018) Nutrient foraging by mycorrhizas: from species functional traits to ecosystem processes. Funct Ecol 32:858–869. 10.1111/1365-2435.1304110.1111/1365-2435.13041
Chen J Heikkinen J Hobbie EA Rinne-Garmston KT Penttilä R Mäkipää R Strategies of carbon and nitrogen acquisition by saprotrophic and ectomycorrhizal fungi in Finnish boreal Picea abies-dominated forests Fungal Biol 2019 123 456 464 10.1016/j.funbio.2019.03.005 31126422
Chen J, Heikkinen J, Hobbie EA, Rinne-Garmston KT, Penttilä R, Mäkipää R (2019) Strategies of carbon and nitrogen acquisition by saprotrophic and ectomycorrhizal fungi in Finnish boreal Picea abies-dominated forests. Fungal Biol 123:456–464. 10.1016/j.funbio.2019.03.00531126422 10.1016/j.funbio.2019.03.005
Clemmensen KE Finlay RD Dahlberg A Stenlid J Wardle DA Lindahl BD Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests New Phytol 2015 205 1525 1536 10.1111/nph.13208 25494880
Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205:1525–1536. 10.1111/nph.1320825494880 10.1111/nph.13208
Clemmensen KE Durling MB Michelsen A Hallin S Finlay RD Lindahl BD A tipping point in carbon storage when forest expands into tundra is related to mycorrhizal recycling of nitrogen Ecol Lett 2021 24 1193 1204 10.1111/ele.13735 33754469
Clemmensen KE, Durling MB, Michelsen A, Hallin S, Finlay RD, Lindahl BD (2021) A tipping point in carbon storage when forest expands into tundra is related to mycorrhizal recycling of nitrogen. Ecol Lett 24:1193–1204. 10.1111/ele.1373533754469 10.1111/ele.13735
Connor RC The benefits of mutualism: a conceptual framework Biol Rev 1995 70 427 457 10.1111/j.1469-185X.1995.tb01196.x
Connor RC (1995) The benefits of mutualism: a conceptual framework. Biol Rev 70:427–457. 10.1111/j.1469-185X.1995.tb01196.x10.1111/j.1469-185X.1995.tb01196.x
Corrêa A Gurevitch J Martins-Loução MA Cruz C C allocation to the fungus is not a cost to the plant in ectomycorrhizae Oikos 2012 121 449 463 10.1111/j.1600-0706.2011.19406.x
Corrêa A, Gurevitch J, Martins-Loução MA, Cruz C (2012) C allocation to the fungus is not a cost to the plant in ectomycorrhizae. Oikos 121:449–463. 10.1111/j.1600-0706.2011.19406.x10.1111/j.1600-0706.2011.19406.x
Courty PE Franc A Garbaye J Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community Soil Biol Biochem 2010 42 2022 2025 10.1016/j.soilbio.2010.07.014
Courty PE, Franc A, Garbaye J (2010) Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community. Soil Biol Biochem 42:2022–2025. 10.1016/j.soilbio.2010.07.01410.1016/j.soilbio.2010.07.014
Courty PE Smith P Koegel S Redecker D Wipf D Inorganic nitrogen uptake and transport in beneficial plant root-microbe interactions Crit Rev Plant Sci 2015 34 4 16 10.1080/07352689.2014.897897
Courty PE, Smith P, Koegel S, Redecker D, Wipf D (2015) Inorganic nitrogen uptake and transport in beneficial plant root-microbe interactions. Crit Rev Plant Sci 34:4–16. 10.1080/07352689.2014.89789710.1080/07352689.2014.897897
Dietrich M Montesinos-Navarro A Gabriel R Strasser F Meier DV Mayerhofer W Gorka S Wiesenbauer J Martin V Weidinger M Richter A Kaiser C Woebken D Both abundant and rare fungi colonizing Fagus sylvatica ectomycorrhizal root-tips shape associated bacterial communities Commun Biol 2022 5 1261 10.1038/s42003-022-04178-y 36396911
Dietrich M, Montesinos-Navarro A, Gabriel R, Strasser F, Meier DV, Mayerhofer W, Gorka S, Wiesenbauer J, Martin V, Weidinger M, Richter A, Kaiser C, Woebken D (2022) Both abundant and rare fungi colonizing Fagus sylvatica ectomycorrhizal root-tips shape associated bacterial communities. Commun Biol 5:1261. 10.1038/s42003-022-04178-y36396911 10.1038/s42003-022-04178-y
Drake JE Darby BA Giasson M-A Kramer MA Phillips RP Finzi AC Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest Biogeosciences 2013 10 821 838 10.5194/bg-10-821-2013
Drake JE, Darby BA, Giasson M-A, Kramer MA, Phillips RP, Finzi AC (2013) Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest. Biogeosciences 10:821–838. 10.5194/bg-10-821-201310.5194/bg-10-821-2013
Eastwood DC (2014) Evolution of fungal wood decay. In: Deterioration and Protection of Sustainable Biomaterials. American Chemical Society, pp 93–112
Elliott GN Chen W-M Chou J-H Wang H-C Sheu S-Y Perin L Reis VM Moulin L Simon MF Bontemps C Sutherland JM Bessi R De Faria SM Trinick MJ Prescott AR Sprent JI James EK Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta New Phytol 2007 173 168 180 10.1111/j.1469-8137.2006.01894.x 17176403
Elliott GN, Chen W-M, Chou J-H, Wang H-C, Sheu S-Y, Perin L, Reis VM, Moulin L, Simon MF, Bontemps C, Sutherland JM, Bessi R, De Faria SM, Trinick MJ, Prescott AR, Sprent JI, James EK (2007) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 173:168–180. 10.1111/j.1469-8137.2006.01894.x17176403 10.1111/j.1469-8137.2006.01894.x
Fernandez CW Kennedy PG Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 2016 209 1382 1394 10.1111/nph.13648 26365785
Fernandez CW, Kennedy PG (2016) Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394. 10.1111/nph.1364826365785 10.1111/nph.13648
Fernandez CW Kennedy PG Melanization of mycorrhizal fungal necromass structures microbial decomposer communities J Ecol 2018 106 468 479 10.1111/1365-2745.12920
Fernandez CW, Kennedy PG (2018) Melanization of mycorrhizal fungal necromass structures microbial decomposer communities. J Ecol 106:468–479. 10.1111/1365-2745.1292010.1111/1365-2745.12920
Finlay RD Ek H Odham G Süderström B Uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium and nitrate sources by intact ectomycorrhizal systems of Fagus sylvatica infected with Paxillus involutus New Phytol 1989 113 47 55 10.1111/j.1469-8137.1989.tb02394.x
Finlay RD, Ek H, Odham G, Süderström B (1989) Uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium and nitrate sources by intact ectomycorrhizal systems of Fagus sylvatica infected with Paxillus involutus. New Phytol 113:47–55. 10.1111/j.1469-8137.1989.tb02394.x10.1111/j.1469-8137.1989.tb02394.x
Frank B On the nutritional dependence of certain trees on root symbiosis with belowground fungi (an English translation of A.B. Frank’s classic paper of 1885) Mycorrhiza 2005 15 267 275 10.1007/s00572-004-0329-y 15549482
Frank B (2005) On the nutritional dependence of certain trees on root symbiosis with belowground fungi (an English translation of A.B. Frank’s classic paper of 1885). Mycorrhiza 15:267–275. 10.1007/s00572-004-0329-y15549482 10.1007/s00572-004-0329-y
Frey-Klett P Garbaye J Tarkka M The mycorrhiza helper bacteria revisited New Phytol 2007 176 22 36 10.1111/j.1469-8137.2007.02191.x 17803639
Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. 10.1111/j.1469-8137.2007.02191.x17803639 10.1111/j.1469-8137.2007.02191.x
Galloway JN Townsend AR Erisman JW Bekunda M Cai Z Freney JR Martinelli LA Seitzinger SP Sutton MA Transformation of the nitrogen cycle: recent trends, questions, and potential solutions Science 2008 320 889 892 10.1126/science.1136674 18487183
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. 10.1126/science.113667418487183 10.1126/science.1136674
Garcia K Doidy J Zimmermann SD Wipf D Courty P-E Take a trip through the plant and fungal transportome of mycorrhiza Trends Plant Sci 2016 21 937 950 10.1016/j.tplants.2016.07.010 27514454
Garcia K, Doidy J, Zimmermann SD, Wipf D, Courty P-E (2016) Take a trip through the plant and fungal transportome of mycorrhiza. Trends Plant Sci 21:937–950. 10.1016/j.tplants.2016.07.01027514454 10.1016/j.tplants.2016.07.010
Gobert A Plassard C Differential NO3− dependent patterns of NO3− uptake in Pinus pinaster, Rhizopogon roseolus and their ectomycorrhizal association New Phytol 2002 154 509 516 10.1046/j.1469-8137.2002.00378.x 33873433
Gobert A, Plassard C (2002) Differential NO3 − dependent patterns of NO3− uptake in Pinus pinaster, Rhizopogon roseolus and their ectomycorrhizal association. New Phytol 154:509–516. 10.1046/j.1469-8137.2002.00378.x33873433 10.1046/j.1469-8137.2002.00378.x
Goodell B (2020) Fungi involved in the biodeterioration and bioconversion of lignocellulose substrates. In: Benz JP, Schipper K (eds) Genetics and Biotechnology. The Mycota, vol 2. Springer, Cham. 10.1007/978-3-030-49924-2_15
Gorka S Dietrich M Mayerhofer W Gabriel R Wiesenbauer J Martin V Zheng Q Imai B Prommer J Weidinger M Schweiger P Eichorst SA Wagner M Richter A Schintlmeister A Woebken D Kaiser C Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability Front Microbiol 2019 10 168 10.3389/fmicb.2019.00168 30863368
Gorka S, Dietrich M, Mayerhofer W, Gabriel R, Wiesenbauer J, Martin V, Zheng Q, Imai B, Prommer J, Weidinger M, Schweiger P, Eichorst SA, Wagner M, Richter A, Schintlmeister A, Woebken D, Kaiser C (2019) Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability. Front Microbiol 10:168. 10.3389/fmicb.2019.0016830863368 10.3389/fmicb.2019.00168
Hacquard S Tisserant E Brun A Legué V Martin F Kohler A Laser microdissection and microarray analysis of Tuber melanosporum ectomycorrhizas reveal functional heterogeneity between mantle and Hartig net compartments Environ Microbiol 2013 15 1853 1869 10.1111/1462-2920.12080 23379715
Hacquard S, Tisserant E, Brun A, Legué V, Martin F, Kohler A (2013) Laser microdissection and microarray analysis of Tuber melanosporum ectomycorrhizas reveal functional heterogeneity between mantle and Hartig net compartments. Environ Microbiol 15:1853–1869. 10.1111/1462-2920.1208023379715 10.1111/1462-2920.12080
Hacskaylo E The Melin school: a personal memoir by Edward Hacskaylo Mycorrhiza 2017 27 75 80 10.1007/s00572-016-0728-x 27562508
Hacskaylo E (2017) The Melin school: a personal memoir by Edward Hacskaylo. Mycorrhiza 27:75–80. 10.1007/s00572-016-0728-x27562508 10.1007/s00572-016-0728-x
Hagenbo A, Fransson P, Menichetti L, Clemmensen KE, Olofsson MA, Ekblad A (2024) Ectomycorrhizal necromass turnover is one-third of biomass turnover in hemiboreal Pinus sylvestris forests. Plants People Planet 951–964. 10.1002/ppp3.10508
Hardoim PR van Overbeek LS Berg G Pirttilä AM Compant S Campisano A Döring M Sessitsch A The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes Microbiol Mol Biol Rev MMBR 2015 79 293 320 10.1128/MMBR.00050-14 26136581
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev MMBR 79:293–320. 10.1128/MMBR.00050-1426136581 10.1128/MMBR.00050-14
Hasselquist NJ Metcalfe DB Inselsbacher E Stangl Z Oren R Näsholm T Högberg P Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest Ecology 2016 97 1012 1022 10.1890/15-1222.1 27220217
Hasselquist NJ, Metcalfe DB, Inselsbacher E, Stangl Z, Oren R, Näsholm T, Högberg P (2016) Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest. Ecology 97:1012–1022. 10.1890/15-1222.127220217 10.1890/15-1222.1
Hawkins BJ Kranabetter JM Quantifying inorganic nitrogen uptake capacity among ectomycorrhizal fungal species using MIFE microelectrode ion flux measurements: theory and applications1 Botany 2017 10.1139/cjb-2017-0028
Hawkins BJ, Kranabetter JM (2017) Quantifying inorganic nitrogen uptake capacity among ectomycorrhizal fungal species using MIFE microelectrode ion flux measurements: theory and applications1. Botany. 10.1139/cjb-2017-002810.1139/cjb-2017-0028
Hawkins BJ Robbins S Comparison of ammonium, nitrate, and proton fluxes in mycorrhizal and nonmycorrhizal roots of lodgepole pine in contrasting nitrogen treatments Can J for Res 2022 52 1245 1253 10.1139/cjfr-2022-0066
Hawkins BJ, Robbins S (2022) Comparison of ammonium, nitrate, and proton fluxes in mycorrhizal and nonmycorrhizal roots of lodgepole pine in contrasting nitrogen treatments. Can J for Res 52:1245–1253. 10.1139/cjfr-2022-006610.1139/cjfr-2022-0066
Henriksson N Franklin O Tarvainen L Marshall J Lundberg-Felten J Eilertsen L Näsholm T The mycorrhizal tragedy of the commons Ecol Lett 2021 24 1215 1224 10.1111/ele.13737 33749095
Henriksson N, Franklin O, Tarvainen L, Marshall J, Lundberg-Felten J, Eilertsen L, Näsholm T (2021) The mycorrhizal tragedy of the commons. Ecol Lett 24:1215–1224. 10.1111/ele.1373733749095 10.1111/ele.13737
Hobbie EA Agerer R Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types Plant Soil 2009 327 71 83 10.1007/s11104-009-0032-z
Hobbie EA, Agerer R (2009) Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327:71–83. 10.1007/s11104-009-0032-z10.1007/s11104-009-0032-z
Hobbie EA Ouimette AP Schuur EAG Kierstead D Trappe JM Bendiksen K Ohenoja E Radiocarbon evidence for the mining of organic nitrogen from soil by mycorrhizal fungi Biogeochemistry 2013 114 381 389 10.1007/s10533-012-9779-z
Hobbie EA, Ouimette AP, Schuur EAG, Kierstead D, Trappe JM, Bendiksen K, Ohenoja E (2013) Radiocarbon evidence for the mining of organic nitrogen from soil by mycorrhizal fungi. Biogeochemistry 114:381–389. 10.1007/s10533-012-9779-z10.1007/s10533-012-9779-z
Högberg P Näsholm T Franklin O Högberg MN Tamm review: on the nature of the nitrogen limitation to plant growth in Fennoscandian boreal forests For Ecol Manag 2017 403 161 185 10.1016/j.foreco.2017.04.045
Högberg P, Näsholm T, Franklin O, Högberg MN (2017) Tamm review: on the nature of the nitrogen limitation to plant growth in Fennoscandian boreal forests. For Ecol Manag 403:161–185. 10.1016/j.foreco.2017.04.04510.1016/j.foreco.2017.04.045
Högberg MN Högberg P Wallander H Nilsson L-O Carbon–nitrogen relations of ectomycorrhizal mycelium across a natural nitrogen supply gradient in boreal forest New Phytol 2021 232 1839 1848 10.1111/nph.17701 34449884
Högberg MN, Högberg P, Wallander H, Nilsson L-O (2021) Carbon–nitrogen relations of ectomycorrhizal mycelium across a natural nitrogen supply gradient in boreal forest. New Phytol 232:1839–1848. 10.1111/nph.1770134449884 10.1111/nph.17701
Hortal S Plett KL Plett JM Cresswell T Johansen M Pendall E Anderson IC Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi ISME J 2017 11 2666 2676 10.1038/ismej.2017.116 28731478
Hortal S, Plett KL, Plett JM, Cresswell T, Johansen M, Pendall E, Anderson IC (2017) Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi. ISME J 11:2666–2676. 10.1038/ismej.2017.11628731478 10.1038/ismej.2017.116
Hu S Bidochka MJ Root colonization by endophytic insect-pathogenic fungi J Appl Microbiol 2021 130 570 581 10.1111/jam.14503 31667953
Hu S, Bidochka MJ (2021) Root colonization by endophytic insect-pathogenic fungi. J Appl Microbiol 130:570–581. 10.1111/jam.1450331667953 10.1111/jam.14503
Janusz G Pawlik A Sulej J Świderska-Burek U Jarosz-Wilkołazka A Paszczyński A Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution FEMS Microbiol Rev 2017 41 941 962 10.1093/femsre/fux049 29088355
Janusz G, Pawlik A, Sulej J, Świderska-Burek U, Jarosz-Wilkołazka A, Paszczyński A (2017) Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev 41:941–962. 10.1093/femsre/fux04929088355 10.1093/femsre/fux049
Jilling A Keiluweit M Contosta AR Frey S Schimel J Schnecker J Smith RG Tiemann L Grandy AS Minerals in the rhizosphere: overlooked mediators of soil nitrogen availability to plants and microbes Biogeochemistry 2018 139 103 122 10.1007/s10533-018-0459-5
Jilling A, Keiluweit M, Contosta AR, Frey S, Schimel J, Schnecker J, Smith RG, Tiemann L, Grandy AS (2018) Minerals in the rhizosphere: overlooked mediators of soil nitrogen availability to plants and microbes. Biogeochemistry 139:103–122. 10.1007/s10533-018-0459-510.1007/s10533-018-0459-5
Johansson EM Fransson PMA Finlay RD van Hees PAW Quantitative analysis of soluble exudates produced by ectomycorrhizal roots as a response to ambient and elevated CO2 Soil Biol Biochem 2009 41 1111 1116 10.1016/j.soilbio.2009.02.016
Johansson EM, Fransson PMA, Finlay RD, van Hees PAW (2009) Quantitative analysis of soluble exudates produced by ectomycorrhizal roots as a response to ambient and elevated CO2. Soil Biol Biochem 41:1111–1116. 10.1016/j.soilbio.2009.02.01610.1016/j.soilbio.2009.02.016
Johnson NC Graham J-H Smith FA Functioning of mycorrhizal associations along the mutualism–parasitism continuum New Phytol 1997 135 575 585 10.1046/j.1469-8137.1997.00729.x
Johnson NC, Graham J-H, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585. 10.1046/j.1469-8137.1997.00729.x10.1046/j.1469-8137.1997.00729.x
Jones DL Hodge A Kuzyakov Y Plant and mycorrhizal regulation of rhizodeposition New Phytol 2004 163 459 480 10.1111/j.1469-8137.2004.01130.x 33873745
Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480. 10.1111/j.1469-8137.2004.01130.x33873745 10.1111/j.1469-8137.2004.01130.x
Jörgensen K Clemmensen KE Wallander H Lindahl BD Do ectomycorrhizal exploration types reflect mycelial foraging strategies? New Phytol 2023 237 576 584 10.1111/nph.18566 36271619
Jörgensen K, Clemmensen KE, Wallander H, Lindahl BD (2023) Do ectomycorrhizal exploration types reflect mycelial foraging strategies? New Phytol 237:576–584. 10.1111/nph.1856636271619 10.1111/nph.18566
Jörgensen K Clemmensen KE Wallander H Lindahl BD Ectomycorrhizal fungi are more sensitive to high soil nitrogen levels in forests exposed to nitrogen deposition New Phytol 2024 242 1725 1738 10.1111/nph.19509 38213001
Jörgensen K, Clemmensen KE, Wallander H, Lindahl BD (2024) Ectomycorrhizal fungi are more sensitive to high soil nitrogen levels in forests exposed to nitrogen deposition. New Phytol 242:1725–1738. 10.1111/nph.1950938213001 10.1111/nph.19509
Kariman K Barker SJ Jost R Finnegan PM Tibbett M A novel plant–fungus symbiosis benefits the host without forming mycorrhizal structures New Phytol 2014 201 1413 1422 10.1111/nph.12600 24279681
Kariman K, Barker SJ, Jost R, Finnegan PM, Tibbett M (2014) A novel plant–fungus symbiosis benefits the host without forming mycorrhizal structures. New Phytol 201:1413–1422. 10.1111/nph.1260024279681 10.1111/nph.12600
Khokon AM Janz D Polle A Ectomycorrhizal diversity, taxon-specific traits and root N uptake in temperate beech forests New Phytol 2023 239 739 751 10.1111/nph.18978 37229659
Khokon AM, Janz D, Polle A (2023) Ectomycorrhizal diversity, taxon-specific traits and root N uptake in temperate beech forests. New Phytol 239:739–751. 10.1111/nph.1897837229659 10.1111/nph.18978
Kiers ET Duhamel M Beesetty Y Mensah JA Franken O Verbruggen E Fellbaum CR Kowalchuk GA Hart MM Bago A Palmer TM West SA Vandenkoornhuyse P Jansa J Bücking H Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis Science 2011 333 880 882 10.1126/science.1208473 21836016
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882. 10.1126/science.120847321836016 10.1126/science.1208473
Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A, Colpaert J, Copeland A, Costa MD, Doré J, Floudas D, Gay G, Girlanda M, Henrissat B, Herrmann S, Hess J, Högberg N, Johansson T, Khouja H-R, LaButti K, Lahrmann U, Levasseur A, Lindquist EA, Lipzen A, Marmeisse R, Martino E, Murat C, Ngan CY, Nehls U, Plett JM, Pringle A, Ohm RA, Perotto S, Peter M, Riley R, Rineau F, Ruytinx J, Salamov A, Shah F, Sun H, Tarkka M, Tritt A, Veneault-Fourrey C, Zuccaro A, Mycorrhizal Genomics Initiative Consortium, Tunlid A, Grigoriev IV, Hibbett DS, Martin F (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410–415. 10.1038/ng.3223
Kramer MG Chadwick OA Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale Nat Clim Change 2018 8 1104 1108 10.1038/s41558-018-0341-4
Kramer MG, Chadwick OA (2018) Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat Clim Change 8:1104–1108. 10.1038/s41558-018-0341-410.1038/s41558-018-0341-4
Kranabetter JM Durall DM MacKenzie WH Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest Mycorrhiza 2009 19 99 111 10.1007/s00572-008-0208-z 18941804
Kranabetter JM, Durall DM, MacKenzie WH (2009) Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest. Mycorrhiza 19:99–111. 10.1007/s00572-008-0208-z18941804 10.1007/s00572-008-0208-z
Kranabetter JM Friesen J Gamiet S Kroeger P Epigeous fruiting bodies of ectomycorrhizal fungi as indicators of soil fertility and associated nitrogen status of boreal forests Mycorrhiza 2009 19 535 548 10.1007/s00572-009-0255-0 19449039
Kranabetter JM, Friesen J, Gamiet S, Kroeger P (2009) Epigeous fruiting bodies of ectomycorrhizal fungi as indicators of soil fertility and associated nitrogen status of boreal forests. Mycorrhiza 19:535–548. 10.1007/s00572-009-0255-019449039 10.1007/s00572-009-0255-0
Kranabetter JM Hawkins BJ Jones MD Robbins S Dyer T Li T Species turnover (β-diversity) in ectomycorrhizal fungi linked to NH4+ uptake capacity Mol Ecol 2015 24 5992 6005 10.1111/mec.13435 26507980
Kranabetter JM, Hawkins BJ, Jones MD, Robbins S, Dyer T, Li T (2015) Species turnover (β-diversity) in ectomycorrhizal fungi linked to NH4 + uptake capacity. Mol Ecol 24:5992–6005. 10.1111/mec.1343526507980 10.1111/mec.13435
Krumina L Op De Beeck M Meklesh V Tunlid A Persson P Ectomycorrhizal fungal transformation of dissolved organic matter: consequences for reductive iron oxide dissolution and Fenton-based oxidation of mineral-associated organic matter Front Earth Sci 2022 10 763695 10.3389/feart.2022.763695
Krumina L, Op De Beeck M, Meklesh V, Tunlid A, Persson P (2022) Ectomycorrhizal fungal transformation of dissolved organic matter: consequences for reductive iron oxide dissolution and Fenton-based oxidation of mineral-associated organic matter. Front Earth Sci 10:76369510.3389/feart.2022.763695
Le Tacon F Zeller B Plain C Hossann C Bréchet C Martin F Kohler A Villerd J Robin C Study of nitrogen and carbon transfer from soil organic matter to Tuber melanosporum mycorrhizas and ascocarps using 15N and 13C soil labelling and whole-genome oligoarrays Plant Soil 2015 395 351 373 10.1007/s11104-015-2557-7
Le Tacon F, Zeller B, Plain C, Hossann C, Bréchet C, Martin F, Kohler A, Villerd J, Robin C (2015) Study of nitrogen and carbon transfer from soil organic matter to Tuber melanosporum mycorrhizas and ascocarps using 15N and 13C soil labelling and whole-genome oligoarrays. Plant Soil 395:351–373. 10.1007/s11104-015-2557-710.1007/s11104-015-2557-7
LeBauer DS Treseder KK Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed Ecology 2008 89 371 379 10.1890/06-2057.1 18409427
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. 10.1890/06-2057.118409427 10.1890/06-2057.1
Leberecht M, Dannenmann M, Tejedor J, Simon J, Rennenberg H, Polle A (2016a) Segregation of nitrogen use between ammonium and nitrate of ectomycorrhizas and beech trees. Plant Cell Environ 2691-2700. 10.1111/pce.12820
Leberecht M, Tu J, Polle A (2016b) Acid and calcareous soils affect nitrogen nutrition and organic nitrogen uptake by beech seedlings (Fagus sylvatica) under drought, and their ectomycorrhizal community structure. Plant Soil 1–15. 10.1007/s11104-016-2956-4
Lebreton A Zeng Q Miyauchi S Kohler A Dai Y-C Martin FM Evolution of the mode of nutrition in symbiotic and saprotrophic fungi in forest ecosystems Annu Rev Ecol Evol Syst 2021 52 385 404 10.1146/annurev-ecolsys-012021-114902
Lebreton A, Zeng Q, Miyauchi S, Kohler A, Dai Y-C, Martin FM (2021) Evolution of the mode of nutrition in symbiotic and saprotrophic fungi in forest ecosystems. Annu Rev Ecol Evol Syst 52:385–404. 10.1146/annurev-ecolsys-012021-11490210.1146/annurev-ecolsys-012021-114902
Lilleskov EA Kuyper TW Bidartondo MI Hobbie EA Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: A review Environ Pollut 2019 246 148 162 10.1016/j.envpol.2018.11.074 30543941
Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EA (2019) Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review. Environ Pollut 246:148–162. 10.1016/j.envpol.2018.11.07430543941 10.1016/j.envpol.2018.11.074
Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EA (2024) Chapter 6 - Impacts of nitrogen deposition on forest mycorrhizal communities. In: Du E, de Vries W (eds) Atmospheric Nitrogen Deposition to Global Forests. Academic Press, pp 95–118
Lindahl BD Tunlid A Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs New Phytol 2015 205 1443 1447 10.1111/nph.13201 25524234
Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447. 10.1111/nph.1320125524234 10.1111/nph.13201
Lindahl BD Ihrmark K Boberg J Trumbore SE Högberg P Stenlid J Finlay RD Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest New Phytol 2007 173 611 620 10.1111/j.1469-8137.2006.01936.x 17244056
Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620. 10.1111/j.1469-8137.2006.01936.x17244056 10.1111/j.1469-8137.2006.01936.x
Lindahl BD Kyaschenko J Varenius K Clemmensen KE Dahlberg A Karltun E Stendahl J A group of ectomycorrhizal fungi restricts organic matter accumulation in boreal forest Ecol Lett 2021 24 1341 1351 10.1111/ele.13746 33934481
Lindahl BD, Kyaschenko J, Varenius K, Clemmensen KE, Dahlberg A, Karltun E, Stendahl J (2021) A group of ectomycorrhizal fungi restricts organic matter accumulation in boreal forest. Ecol Lett 24:1341–1351. 10.1111/ele.1374633934481 10.1111/ele.13746
Lladó S López-Mondéjar R Baldrian P Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global change Microbiol Mol Biol Rev 2017 81 e00063 e116 10.1128/MMBR.00063-16 28404790
Lladó S, López-Mondéjar R, Baldrian P (2017) Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global change. Microbiol Mol Biol Rev 81:e00063-e116. 10.1128/MMBR.00063-1628404790 10.1128/MMBR.00063-16
Looney B Miyauchi S Morin E Drula E Courty PE Kohler A Kuo A LaButti K Pangilinan J Lipzen A Riley R Andreopoulos W He G Johnson J Nolan M Tritt A Barry KW Grigoriev IV Nagy LG Hibbett D Henrissat B Matheny PB Labbé J Martin FM Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom-forming fungi New Phytol 2022 233 2294 2309 10.1111/nph.17892 34861049
Looney B, Miyauchi S, Morin E, Drula E, Courty PE, Kohler A, Kuo A, LaButti K, Pangilinan J, Lipzen A, Riley R, Andreopoulos W, He G, Johnson J, Nolan M, Tritt A, Barry KW, Grigoriev IV, Nagy LG, Hibbett D, Henrissat B, Matheny PB, Labbé J, Martin FM (2022) Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom-forming fungi. New Phytol 233:2294–2309. 10.1111/nph.1789234861049 10.1111/nph.17892
López-Mondéjar R Brabcová V Štursová M Davidová A Jansa J Cajthaml T Baldrian P Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling ISME J 2018 12 1768 1778 10.1038/s41396-018-0084-2 29491492
López-Mondéjar R, Brabcová V, Štursová M, Davidová A, Jansa J, Cajthaml T, Baldrian P (2018) Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling. ISME J 12:1768–1778. 10.1038/s41396-018-0084-229491492 10.1038/s41396-018-0084-2
López-Mondéjar R Tláskal V Větrovský T Štursová M Toscan R Nunes da Rocha U Baldrian P Metagenomics and stable isotope probing reveal the complementary contribution of fungal and bacterial communities in the recycling of dead biomass in forest soil Soil Biol Biochem 2020 148 107875 10.1016/j.soilbio.2020.107875
López-Mondéjar R, Tláskal V, Větrovský T, Štursová M, Toscan R, Nunes da Rocha U, Baldrian P (2020) Metagenomics and stable isotope probing reveal the complementary contribution of fungal and bacterial communities in the recycling of dead biomass in forest soil. Soil Biol Biochem 148:107875. 10.1016/j.soilbio.2020.10787510.1016/j.soilbio.2020.107875
Lusk CH Godoy R Donoso PJ Dickie IA Soil nutrient availability and understorey composition beneath plantations of ecto- and arbuscular mycorrhizal Chilean native trees Plant Soil 2024 501 657 668 10.1007/s11104-024-06563-4
Lusk CH, Godoy R, Donoso PJ, Dickie IA (2024) Soil nutrient availability and understorey composition beneath plantations of ecto- and arbuscular mycorrhizal Chilean native trees. Plant Soil 501:657–668. 10.1007/s11104-024-06563-410.1007/s11104-024-06563-4
Maillard F Beatty B Park M Adamczyk S Adamczyk B See CR Cavender-Bares J Hobbie SE Kennedy PG Microbial community attributes supersede plant and soil parameters in predicting fungal necromass decomposition rates in a 12-tree species common garden experiment Soil Biol Biochem 2023 184 109124 10.1016/j.soilbio.2023.109124
Maillard F, Beatty B, Park M, Adamczyk S, Adamczyk B, See CR, Cavender-Bares J, Hobbie SE, Kennedy PG (2023) Microbial community attributes supersede plant and soil parameters in predicting fungal necromass decomposition rates in a 12-tree species common garden experiment. Soil Biol Biochem 184:109124. 10.1016/j.soilbio.2023.10912410.1016/j.soilbio.2023.109124
Maillard F Kohler A Morin E Hossann C Miyauchi S Ziegler-Devin I Gérant D Angeli N Lipzen A Keymanesh K Johnson J Barry K Grigoriev IV Martin FM Buée M Functional genomics gives new insights into the ectomycorrhizal degradation of chitin New Phytol 2023 238 845 858 10.1111/nph.18773 36702619
Maillard F, Kohler A, Morin E, Hossann C, Miyauchi S, Ziegler-Devin I, Gérant D, Angeli N, Lipzen A, Keymanesh K, Johnson J, Barry K, Grigoriev IV, Martin FM, Buée M (2023) Functional genomics gives new insights into the ectomycorrhizal degradation of chitin. New Phytol 238:845–858. 10.1111/nph.1877336702619 10.1111/nph.18773
Marschner H Marschner’s Mineral Nutrition of Higher Plants 2011 Academic Press
Marschner H (2011) Marschner’s Mineral Nutrition of Higher Plants. Academic Press
Martin F Nehls U Harnessing ectomycorrhizal genomics for ecological insights Curr Opin Plant Biol 2009 12 508 515 10.1016/j.pbi.2009.05.007 19540154
Martin F, Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Curr Opin Plant Biol 12:508–515. 10.1016/j.pbi.2009.05.00719540154 10.1016/j.pbi.2009.05.007
Martin FM van der Heijden MGA The mycorrhizal symbiosis: research frontiers in genomics, ecology, and agricultural application New Phytol 2024 242 1486 1506 10.1111/nph.19541 38297461
Martin FM, van der Heijden MGA (2024) The mycorrhizal symbiosis: research frontiers in genomics, ecology, and agricultural application. New Phytol 242:1486–1506. 10.1111/nph.1954138297461 10.1111/nph.19541
Martin F Aerts A Ahrén D Brun A Danchin EGJ Duchaussoy F Gibon J Kohler A Lindquist E Pereda V Salamov A Shapiro HJ Wuyts J Blaudez D Buée M Brokstein P Canbäck B Cohen D Courty PE Coutinho PM Delaruelle C Detter JC Deveau A DiFazio S Duplessis S Fraissinet-Tachet L Lucic E Frey-Klett P Fourrey C Feussner I Gay G Grimwood J Hoegger PJ Jain P Kilaru S Labbé J Lin YC Legué V Le Tacon F Marmeisse R Melayah D Montanini B Muratet M Nehls U Niculita-Hirzel H Secq MPO-L Peter M Quesneville H Rajashekar B Reich M Rouhier N Schmutz J Yin T Chalot M Henrissat B Kües U Lucas S Van de Peer Y Podila GK Polle A Pukkila PJ Richardson PM Rouzé P Sanders IR Stajich JE Tunlid A Tuskan G Grigoriev IV The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis Nature 2008 452 88 92 10.1038/nature06556 18322534
Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Secq MPO-L, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92. 10.1038/nature0655618322534 10.1038/nature06556
Marupakula S Mahmood S Finlay RD Analysis of single root tip microbiomes suggests that distinctive bacterial communities are selected by Pinus sylvestris roots colonized by different ectomycorrhizal fungi Environ Microbiol 2016 18 1470 1483 10.1111/1462-2920.13102 26521936
Marupakula S, Mahmood S, Finlay RD (2016) Analysis of single root tip microbiomes suggests that distinctive bacterial communities are selected by Pinus sylvestris roots colonized by different ectomycorrhizal fungi. Environ Microbiol 18:1470–1483. 10.1111/1462-2920.1310226521936 10.1111/1462-2920.13102
Mayerhofer W Schintlmeister A Dietrich M Gorka S Wiesenbauer J Martin V Gabriel R Reipert S Weidinger M Clode P Wagner M Woebken D Richter A Kaiser C Recently photoassimilated carbon and fungus-delivered nitrogen are spatially correlated in the ectomycorrhizal tissue of Fagus sylvatica New Phytol 2021 232 2457 2474 10.1111/nph.17591 34196001
Mayerhofer W, Schintlmeister A, Dietrich M, Gorka S, Wiesenbauer J, Martin V, Gabriel R, Reipert S, Weidinger M, Clode P, Wagner M, Woebken D, Richter A, Kaiser C (2021) Recently photoassimilated carbon and fungus-delivered nitrogen are spatially correlated in the ectomycorrhizal tissue of Fagus sylvatica. New Phytol 232:2457–2474. 10.1111/nph.1759134196001 10.1111/nph.17591
McGuire KL Allison SD Fierer N Treseder KK Ectomycorrhizal-dominated boreal and tropical forests have distinct fungal communities, but analogous spatial patterns across soil horizons PLoS ONE 2013 8 e68278 10.1371/journal.pone.0068278 23874569
McGuire KL, Allison SD, Fierer N, Treseder KK (2013) Ectomycorrhizal-dominated boreal and tropical forests have distinct fungal communities, but analogous spatial patterns across soil horizons. PLoS ONE 8:e68278. 10.1371/journal.pone.006827823874569 10.1371/journal.pone.0068278
McPolin MC Kranabetter JM Philpott TJ Hawkins BJ Sporocarp nutrition of ectomycorrhizal fungi indicates an important role for endemic species in a high productivity temperate rainforest New Phytol 2024 242 1603 1613 10.1111/nph.19280 37771241
McPolin MC, Kranabetter JM, Philpott TJ, Hawkins BJ (2024) Sporocarp nutrition of ectomycorrhizal fungi indicates an important role for endemic species in a high productivity temperate rainforest. New Phytol 242:1603–1613. 10.1111/nph.1928037771241 10.1111/nph.19280
Medina-Vega JA Zuleta D Aguilar S Alonso A Bissiengou P Brockelman WY Bunyavejchewin S Burslem DFRP Castaño N Chave J Dalling JW de Oliveira AA Duque Á Ediriweera S Ewango CEN Filip J Hubbell SP Itoh A Kiratiprayoon S Lum SKY Makana J-R Memiaghe H Mitre D Mohamad MB Nathalang A Nilus R Nkongolo NV Novotny V O’Brien MJ Pérez R Pongpattananurak N Reynolds G Russo SE Tan S Thompson J Uriarte M Valencia R Vicentini A Yao TL Zimmerman JK Davies SJ Tropical tree ectomycorrhiza are distributed independently of soil nutrients Nat Ecol Evol 2024 8 400 410 10.1038/s41559-023-02298-0 38200369
Medina-Vega JA, Zuleta D, Aguilar S, Alonso A, Bissiengou P, Brockelman WY, Bunyavejchewin S, Burslem DFRP, Castaño N, Chave J, Dalling JW, de Oliveira AA, Duque Á, Ediriweera S, Ewango CEN, Filip J, Hubbell SP, Itoh A, Kiratiprayoon S, Lum SKY, Makana J-R, Memiaghe H, Mitre D, Mohamad MB, Nathalang A, Nilus R, Nkongolo NV, Novotny V, O’Brien MJ, Pérez R, Pongpattananurak N, Reynolds G, Russo SE, Tan S, Thompson J, Uriarte M, Valencia R, Vicentini A, Yao TL, Zimmerman JK, Davies SJ (2024) Tropical tree ectomycorrhiza are distributed independently of soil nutrients. Nat Ecol Evol 8:400–410. 10.1038/s41559-023-02298-038200369 10.1038/s41559-023-02298-0
Meeds JA Marty Kranabetter J Zigg I Dunn D Miros F Shipley P Jones MD Phosphorus deficiencies invoke optimal allocation of exoenzymes by ectomycorrhizas ISME J 2021 15 1478 1489 10.1038/s41396-020-00864-z 33420298
Meeds JA, Marty Kranabetter J, Zigg I, Dunn D, Miros F, Shipley P, Jones MD (2021) Phosphorus deficiencies invoke optimal allocation of exoenzymes by ectomycorrhizas. ISME J 15:1478–1489. 10.1038/s41396-020-00864-z33420298 10.1038/s41396-020-00864-z
Miyauchi S, Kiss E, Kuo A, Drula E, Kohler A, Sánchez-García M, Morin E, Andreopoulos B, Barry KW, Bonito G, Buée M, Carver A, Chen C, Cichocki N, Clum A, Culley D, Crous PW, Fauchery L, Girlanda M, Hayes RD, Kéri Z, LaButti K, Lipzen A, Lombard V, Magnuson J, Maillard F, Murat C, Nolan M, Ohm RA, Pangilinan J, Pereira M de F, Perotto S, Peter M, Pfister S, Riley R, Sitrit Y, Stielow JB, Szöllősi G, Žifčáková L, Štursová M, Spatafora JW, Tedersoo L, Vaario L-M, Yamada A, Yan M, Wang P, Xu J, Bruns T, Baldrian P, Vilgalys R, Dunand C, Henrissat B, Grigoriev IV, Hibbett D, Nagy LG, Martin FM (2020) Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nat Commun 11:5125. 10.1038/s41467-020-18795-w
Moreau D Bardgett RD Finlay RD Jones DL Philippot L A plant perspective on nitrogen cycling in the rhizosphere Funct Ecol 2019 33 540 552 10.1111/1365-2435.13303
Moreau D, Bardgett RD, Finlay RD, Jones DL, Philippot L (2019) A plant perspective on nitrogen cycling in the rhizosphere. Funct Ecol 33:540–552. 10.1111/1365-2435.1330310.1111/1365-2435.13303
Mrak K Covre-Foltran E Lamersdorf N Elevated nitrate concentrations in soil solution under pure Douglas fir stands can be lowered by mixing with European beech and by site selection For Ecol Manag 2024 564 122004 10.1016/j.foreco.2024.122004
Mrak K, Covre-Foltran E, Lamersdorf N (2024) Elevated nitrate concentrations in soil solution under pure Douglas fir stands can be lowered by mixing with European beech and by site selection. For Ecol Manag 564:122004. 10.1016/j.foreco.2024.12200410.1016/j.foreco.2024.122004
Müller T Neuhäuser B Ludewig U Houdinet G Zimmermann SD Courty PE Wipf D New insights into HcPTR2A and HcPTR2B, two high-affinity peptide transporters from the ectomycorrhizal model fungus Hebeloma cylindrosporum Mycorrhiza 2020 30 735 747 10.1007/s00572-020-00983-7 32820366
Müller T, Neuhäuser B, Ludewig U, Houdinet G, Zimmermann SD, Courty PE, Wipf D (2020) New insights into HcPTR2A and HcPTR2B, two high-affinity peptide transporters from the ectomycorrhizal model fungus Hebeloma cylindrosporum. Mycorrhiza 30:735–747. 10.1007/s00572-020-00983-732820366 10.1007/s00572-020-00983-7
Nannipieri P Paul EA The chemical and functional characterization of soil N and its biotic components Soil Biol Biochem 2009 41 2357 2369 10.1016/j.soilbio.2009.07.013
Nannipieri P, Paul EA (2009) The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem 41:2357–2369. 10.1016/j.soilbio.2009.07.01310.1016/j.soilbio.2009.07.013
Näsholm T Kielland K Ganeteg U Uptake of organic nitrogen by plants New Phytol 2009 182 31 48 10.1111/j.1469-8137.2008.02751.x 19210725
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48. 10.1111/j.1469-8137.2008.02751.x19210725 10.1111/j.1469-8137.2008.02751.x
Näsholm T Högberg P Franklin O Metcalfe D Keel SG Campbell C Hurry V Linder S Högberg MN Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytol 2013 198 214 221 10.1111/nph.12139 23356503
Näsholm T, Högberg P, Franklin O, Metcalfe D, Keel SG, Campbell C, Hurry V, Linder S, Högberg MN (2013) Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytol 198:214–221. 10.1111/nph.1213923356503 10.1111/nph.12139
Neff JC Chapin FS III Vitousek PM Breaks in the cycle: dissolved organic nitrogen in terrestrial ecosystems Front Ecol Environ 2003 1 205 211 10.1890/1540-9295(2003)001[0205:BITCDO]2.0.CO;2
Neff JC, Chapin FS III, Vitousek PM (2003) Breaks in the cycle: dissolved organic nitrogen in terrestrial ecosystems. Front Ecol Environ 1:205–211. 10.1890/1540-9295(2003)001[0205:BITCDO]2.0.CO;210.1890/1540-9295(2003)001[0205:BITCDO]2.0.CO;2
Nehls U Plassard C Nitrogen and phosphate metabolism in ectomycorrhizas New Phytol 2018 220 1047 1058 10.1111/nph.15257 29888395
Nehls U, Plassard C (2018) Nitrogen and phosphate metabolism in ectomycorrhizas. New Phytol 220:1047–1058. 10.1111/nph.1525729888395 10.1111/nph.15257
Nguyen NH Bruns TD The microbiome of Pinus muricata ectomycorrhizae: community assemblages, fungal species effects, and Burkholderia as important bacteria in multipartnered symbioses Microb Ecol 2015 69 914 921 10.1007/s00248-015-0574-y 25687126
Nguyen NH, Bruns TD (2015) The microbiome of Pinus muricata ectomycorrhizae: community assemblages, fungal species effects, and Burkholderia as important bacteria in multipartnered symbioses. Microb Ecol 69:914–921. 10.1007/s00248-015-0574-y25687126 10.1007/s00248-015-0574-y
Nicolás C Martin-Bertelsen T Floudas D Bentzer J Smits M Johansson T Troein C Persson P Tunlid A The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen ISME J 2019 13 977 988 10.1038/s41396-018-0331-6 30538275
Nicolás C, Martin-Bertelsen T, Floudas D, Bentzer J, Smits M, Johansson T, Troein C, Persson P, Tunlid A (2019) The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen. ISME J 13:977–988. 10.1038/s41396-018-0331-630538275 10.1038/s41396-018-0331-6
Op De Beeck M Troein C Siregar S Gentile L Abbondanza G Peterson C Persson P Tunlid A Regulation of fungal decomposition at single-cell level ISME J 2020 14 896 905 10.1038/s41396-019-0583-9 31896790
Op De Beeck M, Troein C, Siregar S, Gentile L, Abbondanza G, Peterson C, Persson P, Tunlid A (2020) Regulation of fungal decomposition at single-cell level. ISME J 14:896–905. 10.1038/s41396-019-0583-931896790 10.1038/s41396-019-0583-9
Pellitier PT Zak DR Ectomycorrhizal fungal decay traits along a soil nitrogen gradient New Phytol 2021 232 2152 2164 10.1111/nph.17734 34533216
Pellitier PT, Zak DR (2021) Ectomycorrhizal fungal decay traits along a soil nitrogen gradient. New Phytol 232:2152–2164. 10.1111/nph.1773434533216 10.1111/nph.17734
Pena R Polle A Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress ISME J 2014 8 321 330 10.1038/ismej.2013.158 24030593
Pena R, Polle A (2014) Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress. ISME J 8:321–330. 10.1038/ismej.2013.15824030593 10.1038/ismej.2013.158
Pena R Offermann C Simon J Naumann PS Gessler A Holst J Dannenmann M Mayer H Kögel-Knabner I Rennenberg H Polle A Girdling affects ectomycorrhizal fungal (EMF) diversity and reveals functional differences in EMF community composition in a beech forest Appl Environ Microbiol 2010 76 1831 1841 10.1128/AEM.01703-09 20097809
Pena R, Offermann C, Simon J, Naumann PS, Gessler A, Holst J, Dannenmann M, Mayer H, Kögel-Knabner I, Rennenberg H, Polle A (2010) Girdling affects ectomycorrhizal fungal (EMF) diversity and reveals functional differences in EMF community composition in a beech forest. Appl Environ Microbiol 76:1831–1841. 10.1128/AEM.01703-0920097809 10.1128/AEM.01703-09
Pena R Tejedor J Zeller B Dannenmann M Polle A Interspecific temporal and spatial differences in the acquisition of litter-derived nitrogen by ectomycorrhizal fungal assemblages New Phytol 2013 199 520 528 10.1111/nph.12272 23594339
Pena R, Tejedor J, Zeller B, Dannenmann M, Polle A (2013) Interspecific temporal and spatial differences in the acquisition of litter-derived nitrogen by ectomycorrhizal fungal assemblages. New Phytol 199:520–528. 10.1111/nph.1227223594339 10.1111/nph.12272
Pena R Lang C Lohaus G Boch S Schall P Schöning I Ammer C Fischer M Polle A Phylogenetic and functional traits of ectomycorrhizal assemblages in top soil from different biogeographic regions and forest types Mycorrhiza 2017 27 233 245 10.1007/s00572-016-0742-z 27885418
Pena R, Lang C, Lohaus G, Boch S, Schall P, Schöning I, Ammer C, Fischer M, Polle A (2017) Phylogenetic and functional traits of ectomycorrhizal assemblages in top soil from different biogeographic regions and forest types. Mycorrhiza 27:233–245. 10.1007/s00572-016-0742-z27885418 10.1007/s00572-016-0742-z
Pena R Bluhm SL Ammerschubert S Agüi-Gonzalez P Rizzoli SO Scheu S Polle A Mycorrhizal C/N ratio determines plant-derived carbon and nitrogen allocation to symbiosis Commun Biol 2023 6 1230 10.1038/s42003-023-05591-7 38053000
Pena R, Bluhm SL, Ammerschubert S, Agüi-Gonzalez P, Rizzoli SO, Scheu S, Polle A (2023) Mycorrhizal C/N ratio determines plant-derived carbon and nitrogen allocation to symbiosis. Commun Biol 6:1230. 10.1038/s42003-023-05591-738053000 10.1038/s42003-023-05591-7
Pena R (2016) Nitrogen acquisition in ectomycorrhizal symbiosis. In: Molecular Mycorrhizal Symbiosis. John Wiley & Sons, Ltd, pp 179–196
Plett KL Wojtalewicz D Anderson IC Plett JM Fungal metabolism and free amino acid content may predict nitrogen transfer to the host plant in the ectomycorrhizal relationship between Pisolithus spp. and Eucalyptus grandis New Phytol 2024 242 1589 1602 10.1111/nph.19400 37974494
Plett KL, Wojtalewicz D, Anderson IC, Plett JM (2024) Fungal metabolism and free amino acid content may predict nitrogen transfer to the host plant in the ectomycorrhizal relationship between Pisolithus spp. and Eucalyptus grandis. New Phytol 242:1589–1602. 10.1111/nph.1940037974494 10.1111/nph.19400
Reininger V Sieber TN Mycorrhiza reduces adverse effects of dark septate endophytes (DSE) on growth of conifers PLoS ONE 2012 7 e42865 10.1371/journal.pone.0042865 22900058
Reininger V, Sieber TN (2012) Mycorrhiza reduces adverse effects of dark septate endophytes (DSE) on growth of conifers. PLoS ONE 7:e42865. 10.1371/journal.pone.004286522900058 10.1371/journal.pone.0042865
Rennenberg H Dannenmann M Nitrogen nutrition of trees in temperate forests—the significance of nitrogen availability in the pedosphere and atmosphere Forests 2015 6 2820 2835 10.3390/f6082820
Rennenberg H, Dannenmann M (2015) Nitrogen nutrition of trees in temperate forests—the significance of nitrogen availability in the pedosphere and atmosphere. Forests 6:2820–2835. 10.3390/f608282010.3390/f6082820
Rineau F Roth D Shah F Smits M Johansson T Canbäck B Olsen PB Persson P Grell MN Lindquist E Grigoriev IV Lange L Tunlid A The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry Environ Microbiol 2012 14 1477 1487 10.1111/j.1462-2920.2012.02736.x 22469289
Rineau F, Roth D, Shah F, Smits M, Johansson T, Canbäck B, Olsen PB, Persson P, Grell MN, Lindquist E, Grigoriev IV, Lange L, Tunlid A (2012) The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environ Microbiol 14:1477–1487. 10.1111/j.1462-2920.2012.02736.x22469289 10.1111/j.1462-2920.2012.02736.x
Rineau F Shah F Smits MM Persson P Johansson T Carleer R Troein C Tunlid A Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus ISME J 2013 7 2010 2022 10.1038/ismej.2013.91 23788332
Rineau F, Shah F, Smits MM, Persson P, Johansson T, Carleer R, Troein C, Tunlid A (2013) Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. ISME J 7:2010–2022. 10.1038/ismej.2013.9123788332 10.1038/ismej.2013.91
Rinta-Kanto JM Timonen S Spatial variations in bacterial and archaeal abundance and community composition in boreal forest pine mycorrhizospheres Eur J Soil Biol 2020 97 103168 10.1016/j.ejsobi.2020.103168
Rinta-Kanto JM, Timonen S (2020) Spatial variations in bacterial and archaeal abundance and community composition in boreal forest pine mycorrhizospheres. Eur J Soil Biol 97:103168. 10.1016/j.ejsobi.2020.10316810.1016/j.ejsobi.2020.103168
Rivera Pérez CA Janz D Schneider D Daniel R Polle A Transcriptional landscape of ectomycorrhizal fungi and their host provides insight into N uptake from forest soil mSystems 2022 7 e00957 21 10.1128/mSystems.00957-21 35089084
Rivera Pérez CA, Janz D, Schneider D, Daniel R, Polle A (2022) Transcriptional landscape of ectomycorrhizal fungi and their host provides insight into N uptake from forest soil. mSystems 7:e00957-21. 10.1128/mSystems.00957-2135089084 10.1128/mSystems.00957-21
Ruotsalainen AL Kauppinen M Wäli PR Saikkonen K Helander M Tuomi J Dark septate endophytes: mutualism from by-products? Trends Plant Sci 2022 27 247 254 10.1016/j.tplants.2021.10.001 34756535
Ruotsalainen AL, Kauppinen M, Wäli PR, Saikkonen K, Helander M, Tuomi J (2022) Dark septate endophytes: mutualism from by-products? Trends Plant Sci 27:247–254. 10.1016/j.tplants.2021.10.00134756535 10.1016/j.tplants.2021.10.001
Sa G Yao J Deng C Liu J Zhang Y Zhu Z Zhang Y Ma X Zhao R Lin S Lu C Polle A Chen S Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net New Phytol 2019 222 1951 1964 10.1111/nph.15740 30756398
Sa G, Yao J, Deng C, Liu J, Zhang Y, Zhu Z, Zhang Y, Ma X, Zhao R, Lin S, Lu C, Polle A, Chen S (2019) Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net. New Phytol 222:1951–1964. 10.1111/nph.1574030756398 10.1111/nph.15740
Sardans J Alonso R Janssens IA Carnicer J Vereseglou S Rillig MC Fernández-Martínez M Sanders TGM Peñuelas J Foliar and soil concentrations and stoichiometry of nitrogen and phosphorous across European Pinus sylvestris forests: relationships with climate, N deposition and tree growth Funct Ecol 2016 30 676 689 10.1111/1365-2435.12541
Sardans J, Alonso R, Janssens IA, Carnicer J, Vereseglou S, Rillig MC, Fernández-Martínez M, Sanders TGM, Peñuelas J (2016) Foliar and soil concentrations and stoichiometry of nitrogen and phosphorous across European Pinus sylvestris forests: relationships with climate, N deposition and tree growth. Funct Ecol 30:676–689. 10.1111/1365-2435.1254110.1111/1365-2435.12541
Schimel JP Bennett J Nitrogen mineralization: challenges of a changing paradigm Ecology 2004 85 591 602 10.1890/03-8002
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602. 10.1890/03-800210.1890/03-8002
Schreider K Hofmann D Boy J Andrino A FernandesFigueiredo A Sauheitl L Guggenberger G Mycorrhizal mediated partitioning of phosphorus: ectomycorrhizal (Populus x canescens x Paxillus involutus) potential to exploit simultaneously organic and mineral phosphorus sources Front Soil Sci 2022 2 865517 10.3389/fsoil.2022.865517
Schreider K, Hofmann D, Boy J, Andrino A, FernandesFigueiredo A, Sauheitl L, Guggenberger G (2022) Mycorrhizal mediated partitioning of phosphorus: ectomycorrhizal (Populus x canescens x Paxillus involutus) potential to exploit simultaneously organic and mineral phosphorus sources. Front Soil Sci 2:865517. 10.3389/fsoil.2022.86551710.3389/fsoil.2022.865517
Shah F Rineau F Canbäck B Johansson T Tunlid A The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus New Phytol 2013 200 875 887 10.1111/nph.12425 23902518
Shah F, Rineau F, Canbäck B, Johansson T, Tunlid A (2013) The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus. New Phytol 200:875–887. 10.1111/nph.1242523902518 10.1111/nph.12425
Shah F Nicolás C Bentzer J Ellström M Smits M Rineau F Canbäck B Floudas D Carleer R Lackner G Braesel J Hoffmeister D Henrissat B Ahrén D Johansson T Hibbett DS Martin F Persson P Tunlid A Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors New Phytol 2016 209 1705 1719 10.1111/nph.13722 26527297
Shah F, Nicolás C, Bentzer J, Ellström M, Smits M, Rineau F, Canbäck B, Floudas D, Carleer R, Lackner G, Braesel J, Hoffmeister D, Henrissat B, Ahrén D, Johansson T, Hibbett DS, Martin F, Persson P, Tunlid A (2016) Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol 209:1705–1719. 10.1111/nph.1372226527297 10.1111/nph.13722
Shah F Gressler M Nehzati S Op De Beeck M Gentile L Hoffmeister D Persson P Tunlid A Secretion of Iron(III)-reducing metabolites during protein acquisition by the ectomycorrhizal fungus Paxillus involutus Microorganisms 2020 9 E35 10.3390/microorganisms9010035
Shah F, Gressler M, Nehzati S, Op De Beeck M, Gentile L, Hoffmeister D, Persson P, Tunlid A (2020) Secretion of Iron(III)-reducing metabolites during protein acquisition by the ectomycorrhizal fungus Paxillus involutus. Microorganisms 9:E35. 10.3390/microorganisms901003510.3390/microorganisms9010035
Simms EL Taylor DL Povich J Shefferson RP Sachs J l, Urbina M, Tausczik Y, An empirical test of partner choice mechanisms in a wild legume–rhizobium interaction Proc R Soc B Biol Sci 2006 273 77 81 10.1098/rspb.2005.3292
Simms EL, Taylor DL, Povich J, Shefferson RP, Sachs J, l, Urbina M, Tausczik Y, (2006) An empirical test of partner choice mechanisms in a wild legume–rhizobium interaction. Proc R Soc B Biol Sci 273:77–81. 10.1098/rspb.2005.329210.1098/rspb.2005.3292
Smith SE Read DJ Mycorrhizal Symbiosis 2010 Academic Press
Smith SE, Read DJ (2010) Mycorrhizal Symbiosis. Academic Press
Sportes A Hériché M Boussageon R Noceto P-A van Tuinen D Wipf D Courty PE A historical perspective on mycorrhizal mutualism emphasizing arbuscular mycorrhizas and their emerging challenges Mycorrhiza 2021 31 637 653 10.1007/s00572-021-01053-2 34657204
Sportes A, Hériché M, Boussageon R, Noceto P-A, van Tuinen D, Wipf D, Courty PE (2021) A historical perspective on mycorrhizal mutualism emphasizing arbuscular mycorrhizas and their emerging challenges. Mycorrhiza 31:637–653. 10.1007/s00572-021-01053-234657204 10.1007/s00572-021-01053-2
Steidinger BS Crowther TW Liang J Nuland MEV Werner GDA Reich PB Nabuurs GJ de Miguel S Zhou M Picard N Herault B Zhao X Zhang C Routh D Peay KG Climatic controls of decomposition drive the global biogeography of forest-tree symbioses Nature 2019 569 404 408 10.1038/s41586-019-1128-0 31092941
Steidinger BS, Crowther TW, Liang J, Nuland MEV, Werner GDA, Reich PB, Nabuurs GJ, de Miguel S, Zhou M, Picard N, Herault B, Zhao X, Zhang C, Routh D, Peay KG (2019) Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569:404–408. 10.1038/s41586-019-1128-031092941 10.1038/s41586-019-1128-0
Sun Y Wang M Mur LAJ Shen Q Guo S The cross-kingdom roles of mineral nutrient transporters in plant-microbe relations Physiol Plant 2021 171 771 784 10.1111/ppl.13318 33341944
Sun Y, Wang M, Mur LAJ, Shen Q, Guo S (2021) The cross-kingdom roles of mineral nutrient transporters in plant-microbe relations. Physiol Plant 171:771–784. 10.1111/ppl.1331833341944 10.1111/ppl.13318
Talbot JM Treseder KK Controls over mycorrhizal uptake of organic nitrogen Pedobiologia 2010 53 169 179 10.1016/j.pedobi.2009.12.001
Talbot JM, Treseder KK (2010) Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 53:169–179. 10.1016/j.pedobi.2009.12.00110.1016/j.pedobi.2009.12.001
Talbot JM Martin F Kohler A Henrissat B Peay KG Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry Soil Biol Biochem 2015 88 441 456 10.1016/j.soilbio.2015.05.006
Talbot JM, Martin F, Kohler A, Henrissat B, Peay KG (2015) Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry. Soil Biol Biochem 88:441–456. 10.1016/j.soilbio.2015.05.00610.1016/j.soilbio.2015.05.006
Teste FP Laliberté E Plasticity in root symbioses following shifts in soil nutrient availability during long-term ecosystem development J Ecol 2019 107 633 649 10.1111/1365-2745.13103
Teste FP, Laliberté E (2019) Plasticity in root symbioses following shifts in soil nutrient availability during long-term ecosystem development. J Ecol 107:633–649. 10.1111/1365-2745.1310310.1111/1365-2745.13103
Theis KR Dheilly NM Klassen JL Brucker RM Baines JF Bosch TCG Cryan JF Gilbert SF Goodnight CJ Lloyd EA Sapp J Vandenkoornhuyse P Zilber-Rosenberg I Rosenberg E Bordenstein SR Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes mSystems 2016 1 e00028 16 10.1128/mSystems.00028-16 27822520
Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF, Bosch TCG, Cryan JF, Gilbert SF, Goodnight CJ, Lloyd EA, Sapp J, Vandenkoornhuyse P, Zilber-Rosenberg I, Rosenberg E, Bordenstein SR (2016) Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1:e00028-16. 10.1128/mSystems.00028-1627822520 10.1128/mSystems.00028-16
Tibbett M Sanders FE Cairney JWG Leake JR Temperature regulation of extracellular proteases in ectomycorrhizal fungi (Hebeloma spp.) grown in axenic culture Mycol Res 1999 103 707 714 10.1017/S0953756298007813
Tibbett M, Sanders FE, Cairney JWG, Leake JR (1999) Temperature regulation of extracellular proteases in ectomycorrhizal fungi (Hebeloma spp.) grown in axenic culture. Mycol Res 103:707–714. 10.1017/S095375629800781310.1017/S0953756298007813
Tinker PB Nye PH Solute movement in the rhizosphere 2000 Oxford University Press
Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press
Uroz S Courty PE Oger P Plant symbionts are engineers of the plant-associated microbiome Trends Plant Sci 2019 24 905 916 10.1016/j.tplants.2019.06.008 31288964
Uroz S, Courty PE, Oger P (2019) Plant symbionts are engineers of the plant-associated microbiome. Trends Plant Sci 24:905–916. 10.1016/j.tplants.2019.06.00831288964 10.1016/j.tplants.2019.06.008
Valtanen K Eissfeller V Beyer F Hertel D Scheu S Polle A Carbon and nitrogen fluxes between beech and their ectomycorrhizal assemblage Mycorrhiza 2014 24 645 650 10.1007/s00572-014-0581-8 24756632
Valtanen K, Eissfeller V, Beyer F, Hertel D, Scheu S, Polle A (2014) Carbon and nitrogen fluxes between beech and their ectomycorrhizal assemblage. Mycorrhiza 24:645–650. 10.1007/s00572-014-0581-824756632 10.1007/s00572-014-0581-8
van der Linde S Suz LM Orme CDL Cox F Andreae H Asi E Atkinson B Benham S Carroll C Cools N De Vos B Dietrich H-P Eichhorn J Gehrmann J Grebenc T Gweon HS Hansen K Jacob F Kristöfel F Lech P Manninger M Martin J Meesenburg H Merilä P Nicolas M Pavlenda P Rautio P Schaub M Schröck H-W Seidling W Šrámek V Thimonier A Thomsen IM Titeux H Vanguelova E Verstraeten A Vesterdal L Waldner P Wijk S Zhang Y Žlindra D Bidartondo MI Environment and host as large-scale controls of ectomycorrhizal fungi Nature 2018 558 243 248 10.1038/s41586-018-0189-9 29875410
van der Linde S, Suz LM, Orme CDL, Cox F, Andreae H, Asi E, Atkinson B, Benham S, Carroll C, Cools N, De Vos B, Dietrich H-P, Eichhorn J, Gehrmann J, Grebenc T, Gweon HS, Hansen K, Jacob F, Kristöfel F, Lech P, Manninger M, Martin J, Meesenburg H, Merilä P, Nicolas M, Pavlenda P, Rautio P, Schaub M, Schröck H-W, Seidling W, Šrámek V, Thimonier A, Thomsen IM, Titeux H, Vanguelova E, Verstraeten A, Vesterdal L, Waldner P, Wijk S, Zhang Y, Žlindra D, Bidartondo MI (2018) Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558:243–248. 10.1038/s41586-018-0189-929875410 10.1038/s41586-018-0189-9
Vitousek PM Porder S Houlton BZ Chadwick OA Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions Ecol Appl 2010 20 5 15 10.1890/08-0127.1 20349827
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15. 10.1890/08-0127.120349827 10.1890/08-0127.1
von Sperber C Chadwick OA Casciotti KL Peay KG Francis CA Kim AE Vitousek PM Controls of nitrogen cycling evaluated along a well-characterized climate gradient Ecology 2017 98 1117 1129 10.1002/ecy.1751 28130777
von Sperber C, Chadwick OA, Casciotti KL, Peay KG, Francis CA, Kim AE, Vitousek PM (2017) Controls of nitrogen cycling evaluated along a well-characterized climate gradient. Ecology 98:1117–1129. 10.1002/ecy.175128130777 10.1002/ecy.1751
Wallenda T Read DJ Kinetics of amino acid uptake by ectomycorrhizal roots Plant Cell Environ 1999 22 179 187 10.1046/j.1365-3040.1999.00385.x
Wallenda T, Read DJ (1999) Kinetics of amino acid uptake by ectomycorrhizal roots. Plant Cell Environ 22:179–187. 10.1046/j.1365-3040.1999.00385.x10.1046/j.1365-3040.1999.00385.x
Wang T Tian Z Tunlid A Persson P Nitrogen acquisition from mineral-associated proteins by an ectomycorrhizal fungus New Phytol 2020 228 697 711 10.1111/nph.16596 32279319
Wang T, Tian Z, Tunlid A, Persson P (2020) Nitrogen acquisition from mineral-associated proteins by an ectomycorrhizal fungus. New Phytol 228:697–711. 10.1111/nph.1659632279319 10.1111/nph.16596
Wang T Persson P Tunlid A A widespread mechanism in ectomycorrhizal fungi to access nitrogen from mineral-associated proteins Environ Microbiol 2021 23 5837 5849 10.1111/1462-2920.15539 33891367
Wang T, Persson P, Tunlid A (2021) A widespread mechanism in ectomycorrhizal fungi to access nitrogen from mineral-associated proteins. Environ Microbiol 23:5837–5849. 10.1111/1462-2920.1553933891367 10.1111/1462-2920.15539
Wu G Miyauchi S Morin E Kuo A Drula E Varga T Kohler A Feng B Cao Y Lipzen A Daum C Hundley H Pangilinan J Johnson J Barry K LaButti K Ng V Ahrendt S Min B Choi I-G Park H Plett JM Magnuson J Spatafora JW Nagy LG Henrissat B Grigoriev IV Yang Z-L Xu J Martin FM Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales New Phytol 2022 233 1383 1400 10.1111/nph.17858 34767630
Wu G, Miyauchi S, Morin E, Kuo A, Drula E, Varga T, Kohler A, Feng B, Cao Y, Lipzen A, Daum C, Hundley H, Pangilinan J, Johnson J, Barry K, LaButti K, Ng V, Ahrendt S, Min B, Choi I-G, Park H, Plett JM, Magnuson J, Spatafora JW, Nagy LG, Henrissat B, Grigoriev IV, Yang Z-L, Xu J, Martin FM (2022) Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales. New Phytol 233:1383–1400. 10.1111/nph.1785834767630 10.1111/nph.17858
Xie L Zhou X Liu Q Zhao C Yin C Inorganic nitrogen uptake rate of Picea asperata curtailed by fine root acclimation to water and nitrogen supply and further by ectomycorrhizae Physiol Plant 2021 173 2130 2141 10.1111/ppl.13562 34537962
Xie L, Zhou X, Liu Q, Zhao C, Yin C (2021) Inorganic nitrogen uptake rate of Picea asperata curtailed by fine root acclimation to water and nitrogen supply and further by ectomycorrhizae. Physiol Plant 173:2130–2141. 10.1111/ppl.1356234537962 10.1111/ppl.13562
Yoneyama T Ito O Engelaar WMHG Uptake, metabolism and distribution of nitrogen in crop plants traced by enriched and natural 15N: Progress over the last 30 years Phytochem Rev 2003 2 121 132 10.1023/B:PHYT.0000004198.95836.ad
Yoneyama T, Ito O, Engelaar WMHG (2003) Uptake, metabolism and distribution of nitrogen in crop plants traced by enriched and natural 15N: Progress over the last 30 years. Phytochem Rev 2:121–132. 10.1023/B:PHYT.0000004198.95836.ad10.1023/B:PHYT.0000004198.95836.ad
Zak DR Pellitier PT Argiroff W Castillo B James TY Nave LE Averill C Beidler KV Bhatnagar J Blesh J Classen AT Craig M Fernandez CW Gundersen P Johansen R Koide RT Lilleskov EA Lindahl BD Nadelhoffer KJ Phillips RP Tunlid A Exploring the role of ectomycorrhizal fungi in soil carbon dynamics New Phytol 2019 223 33 39 10.1111/nph.15679 30636276
Zak DR, Pellitier PT, Argiroff W, Castillo B, James TY, Nave LE, Averill C, Beidler KV, Bhatnagar J, Blesh J, Classen AT, Craig M, Fernandez CW, Gundersen P, Johansen R, Koide RT, Lilleskov EA, Lindahl BD, Nadelhoffer KJ, Phillips RP, Tunlid A (2019) Exploring the role of ectomycorrhizal fungi in soil carbon dynamics. New Phytol 223:33–39. 10.1111/nph.1567930636276 10.1111/nph.15679
Zhang Z Guo W Wang J Lambers H Yin H Extraradical hyphae alleviate nitrogen deposition-induced phosphorus deficiency in ectomycorrhiza-dominated forests New Phytol 2023 239 1651 1664 10.1111/nph.19078 37322611
Zhang Z, Guo W, Wang J, Lambers H, Yin H (2023) Extraradical hyphae alleviate nitrogen deposition-induced phosphorus deficiency in ectomycorrhiza-dominated forests. New Phytol 239:1651–1664. 10.1111/nph.1907837322611 10.1111/nph.19078
Zhu X Lambers H Guo W Chen D Liu Z Zhang Z Yin H Extraradical hyphae exhibit more plastic nutrient-acquisition strategies than roots under nitrogen enrichment in ectomycorrhiza-dominated forests Glob Change Biol 2023 29 4605 4619 10.1111/gcb.16768
Zhu X, Lambers H, Guo W, Chen D, Liu Z, Zhang Z, Yin H (2023) Extraradical hyphae exhibit more plastic nutrient-acquisition strategies than roots under nitrogen enrichment in ectomycorrhiza-dominated forests. Glob Change Biol 29:4605–4619. 10.1111/gcb.1676810.1111/gcb.16768
