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e Spatial topology of Rhizopogon genets and Douglasfir trees. A 30 3 30 m plot (square outline) contained 67 trees of various ages (green shapes, sized relative to tree diameter). Small black dots mark sampling locations of Rhizopogon EM (n [ 401), 338 of which were associated with a specific tree and fungal genet based on microsatellite DNA analysis. Samples representative of each fungal genet are outlined in colours: Rhizopogon visiculosus genets (n [ 14), blue, and Rhizopogon vinicolor genets (n [ 13), pink. Lines link tree roots encountered by Rhizopogon EM with corresponding trees aboveground and are coloured according to tree genotype. The most highly connected tree (arrow) was linked to 47 other trees through eight R. vesiculosus genets and three R. vinicolor genets. Reproduced, with permission, from Beiler et al. (2010).
Source publication
Mycorrhizal networks, defined as a common mycorrhizal mycelium linking the roots of at least two plants, occur in all major terrestrial ecosystems. This review discusses the recent progress and challenges in our understanding of the characteristics, functions, ecology and models of mycorrhizal networks, with the goal of encouraging future research...
Context in source publication
Context 1
... and resilience to disturbance from studies of MN architecture in forest ecosystems (see Section 2). In Beiler et al. (2010), multi-locus, microsatellite DNA markers were used to show that most trees in an uneven-aged forest of P. menziesii var. glauca were interconnected by a complex MN of the EM fungi Rhizopogon ves- iculosus and R. vinicolor (Fig. 5). The MN had a scale-free network structure (Box 7), where most of the young trees were linked to large, old hub trees, suggesting the network played a role in facilitating the self-regeneration of these Douglas-fir forests. Likewise, seedling establishment success in this forest type was 26% greater where seedlings had full access to ...
Citations
... In forest ecosystems, MX plants occur in the understory, and their associated fungi are shared with neighbouring plants, forming common mycorrhizal networks (CMNs) (Selosse et al. 2006;Beiler et al. 2010;Simard et al. 2012;Simard 2018). CMNs have been suggested to transport carbon, nutrients, and water (Simard et al. 1997(Simard et al. , 2003(Simard et al. , 2012Selosse et al. 2006), and despite recent claims that CMNs are overstated (Karst et al. 2023), mycoheterotrophic and MX plants are likely the strongest evidence that CMNs can be functional. ...
... In forest ecosystems, MX plants occur in the understory, and their associated fungi are shared with neighbouring plants, forming common mycorrhizal networks (CMNs) (Selosse et al. 2006;Beiler et al. 2010;Simard et al. 2012;Simard 2018). CMNs have been suggested to transport carbon, nutrients, and water (Simard et al. 1997(Simard et al. , 2003(Simard et al. , 2012Selosse et al. 2006), and despite recent claims that CMNs are overstated (Karst et al. 2023), mycoheterotrophic and MX plants are likely the strongest evidence that CMNs can be functional. A MX orchid whose CMN connections are disturbed, such as by killing the fungus, is driven to be more autotrophic by the reduction of its mycorrhizal resources (Bellino et al. 2014); this trend is reflected in its fruits, as expected since in MX orchids the resources for fruiting come mostly from the plant's own photosynthesis Gonneau et al. 2014;Tĕšitel et al. 2018). ...
Pyrola japonica, a member of the family Ericaceae, is a mixotroph that grows on forest floors and obtains carbon (C) from both its photosynthesis and its mycorrhizal fungi. Its mycorrhizal community is dominated by Russulaceae. However, the mechanism of its C acquisition and its flexibility are not well understood. Our aim was to assess the impact of disturbance of the mycorrhizal fungal communities on C acquisition by P. japonica. We repeatedly applied a fungicide (Benomyl) to soils around P. japonica plants in a broad-leaved forest of central Japan, in order to disturb fungal associates near roots. After fungicide treatment, P. japonica roots were collected and subjected to barcoding by next-generation sequencing, focusing on the ITS2 region. The rate of mycorrhizal formation and α-diversity did not significantly change upon fungicide treatments. Irrespective of the treatments, Russulaceae represented more than 80% of the taxa. Leaves and seeds of the plants were analysed for ¹³C stable isotope ratios that reflect fungal C gain. Leaf and seed δ¹³C values with the fungicide treatment were significantly lower than those with the other treatments. Thus the fungicide did not affect mycorrhizal communities in the roots, but disturbed mycorrhizal fungal pathways via extraradical hyphae, and resulted in a more photosynthetic behaviour of P. japonica for leaves and seeds.
... The ability of mycorrhizal fungi to access water and nutrients from distant soil areas increases plant resistance to various abiotic stresses, such as drought and salinity. Moreover, mycorrhizal fungi provide a protective barrier against soil-borne pathogens, enhancing the plants' defense mechanisms [17,19]. ...
... In return, mycorrhizal fungi benefit from their symbiotic relationship with plants by gaining access to carbohydrates produced through photosynthesis, which are essential for their growth and development. The plant roots also offer a stable and protected environment for the fungi to colonize and thrive, ensuring a reliable habitat [17,19]. ...
Biological entities in nature have developed sophisticated communication methods over millennia to facilitate cooperation. Among these entities, plants are some of the most intricate communicators. They interact with each other through various communication modalities, creating networks that enable the exchange of information and nutrients. In this paper, we explore this collective behavior and its components. We then introduce the concept of agent plants, outlining their architecture and detailing the tasks of each unit. Additionally, we investigate the mycorrhizal fungi-plant symbiosis to extract glucose for energy harvesting. We propose an architecture that converts the chemical energy stored in these glucose molecules into electrical energy. We conduct comprehensive analyses of the proposed architecture to validate its effectiveness.
... Mediterranean terrestrial plant production is generally more P-limited than N-limited (Du et al., 2020), which suggests that P may be a more important nutrient trader than N in these ecosystems (Adamo et al., 2021). It has been suggested that plants allocate more resources to P uptake as their P limitation increases (Simard et al., 2012); however, Frank (Frank, 2008) reported that grazing had no influence on plant P uptake. Therefore, it cannot be assumed that the presence of ungulates will affect different elements in the same way (Sitters and Andriuzzi, 2019). ...
The effect of wild ungulate density on ecosystems varies according to different factors: climate and physiography conditions, forest type, management history, and herbivore identity. In this study, we evaluated the effect of historically high densities of red deer (Cervus elaphus L.) on the soil fungal communities in Mediterranean ecosystems using 30 paired plots, open on the one hand and exclosure plots on the other one. Plots were established at the end of 2020 in a perimeter-fenced hunting estate of 6600 ha in Toledo, Spain. Three months after plots were established, we analysed fungal communities in 60 soil samples using Illumina 250-bp paired-end sequencing. We estimated changes in total fungal richness and in the richness of trophic groups through Linear Mixed Effects models using fenced/unfenced type and deer habitat use as fixed variables and the location of the plots and the main tree host species as random variables. Fungal composition was analysed using non-metric multidimensional scaling and permutational multivariate ANOVA; edaphic characteristics were incorporated to explain differences. Soil fungal communities were not differentially affected by excluding ungulates for three months. Areas with high deer densities had a richer saprotrophic community and where lowland environments were dominated by the main tree hosts Quercus faginea and Quercus ilex. Arbutus unedo was found in mountain areas where there was less herbivore pressure, a greater richness of ectomycorrhizal and lichenized fungi and soils positively associated to nitrogen, phosphorus, potassium and organic matter levels.
... Quindi il Wood-Wide Web permette agli alberi più sviluppati di aiutare quelli più giovani che altrimenti non sopravvivrebbero. Attraverso la stessa via, le piante possono scambiarsi altri elementi quali azoto e fosforo (Simard et al., 2012). Un'altra evidenza arriva dall'altra parte del mondo, tra i pendii scoscesi della Nuova Zelanda. ...
In questo saggio approfondiremo il comportamento di uno dei principali elementi che caratterizza i nostri paesaggi: le piante. La comprensione di un paesaggio non può esimersi da una profonda conoscenza del mondo vegetale e dalle dinamiche che intercorrono tra le comunità di piante che lo compongono. Lo scopo è di andare oltre la visione del verde come mero sfondo e linguaggio compositivo per considerarlo, più propriamente, come il principale attore del paesaggio, con i suoi bisogni, le sue peculiarità e la sua… intelligenza. Dopo un breve excursus sulle straordinarie abilità cognitive delle piante, ci soffermeremo sulle complesse relazioni che le piante sanno tessere al fine della sopravvivenza. Concluderemo, con una riflessione sull’importanza del verde non solo per la progettazione dei nostri paesaggi ma anche per la salvaguardia della biodiversità e gli ecosistemi.
... In pulse-chase experiments on trees and tree saplings, only relatively small gains have been detected in aboveground plant tissue (<10% of the carbon acquired in plant tissue during the experiment [97][98][99] (but see ref. 100)), although factors such as low labelling intensity, the duration of the experiment and the heterogeneity of carbon partitioning may lead to considerable underestimates of net carbon gain 101 . A pulse-chase experiment on Cephalanthera damasonium, a partially mycoheterotrophic orchid, highlighted the importance of the latter process; even though the investigated plants perform photosynthesis, the resulting photosynthates are not used for the growth of perennial underground organs 54 . ...
... In the ectomycorrhizal symbiosis, it has been suggested that small amounts of carbon gain might be a by-product of nitrogen uptake 97 . But several studies indicate that nitrogen is transferred from the fungus to the plant in a non-organic form [102][103][104][105] . ...
... Carbon uptake is therefore unlikely to be solely a by-product of nutrient uptake. Yet, it is clear that carbon uptake by plants from mycorrhizal fungi may constitute only a minute fraction of the total plant biomass in forest ecosystems or even in individual plants 97 . Also, because no study has reported a positive effect on plant growth or performance due to carbon gain from common mycorrhizal networks, this phenomenon has been considered 'physiologically insignificant' 14 . ...
The prevalence and potential functions of common mycorrhizal networks, or the ‘wood-wide web’, resulting from the simultaneous interaction of mycorrhizal fungi and roots of different neighbouring plants have been increasingly capturing the interest of science and society, sometimes leading to hyperbole and misinterpretation. Several recent reviews conclude that popular claims regarding the widespread nature of these networks in forests and their role in the transfer of resources and information between plants lack evidence. Here we argue that mycoheterotrophic plants associated with ectomycorrhizal or arbuscular mycorrhizal fungi require resource transfer through common mycorrhizal networks and thus are natural evidence for the occurrence and function of these networks, offering a largely overlooked window into this methodologically challenging underground phenomenon. The wide evolutionary and geographic distribution of mycoheterotrophs and their interactions with a broad phylogenetic range of mycorrhizal fungi indicate that common mycorrhizal networks are prevalent, particularly in forests, and result in net carbon transfer among diverse plants through shared mycorrhizal fungi. On the basis of the available scientific evidence, we propose a continuum of carbon transfer options within common mycorrhizal networks, and we discuss how knowledge on the biology of mycoheterotrophic plants can be instrumental for the study of mycorrhizal-mediated transfers between plants.
... Generalist fungi, colonizing the roots of several different tree species, and specialist fungi, specific to individual tree species, may colonize P. cembra roots [9]. In alpine and subalpine habitats, specialists often dominate the ectomycorrhizal community, possibly, because in high altitude areas with extreme conditions, they provide the benefit of efficient nutrient and water transfer between both symbionts and exclude mycoheterotrophy [10]. Some fungal genera, such as Suillus, Rhizopogon, Russula, and Tomentella, are well known for mycorrhizing P. cembra roots [11]. ...
Background
In Europe, Pinus cembra forests cover subalpine and alpine areas and they are of high conservational and ecological relevance. These forests experience strong seasonality with alternating snow-free and snow covered periods. Although P. cembra is known for mycorrhization and mycorrhizae usually involve fungi, plants and bacteria, the community compositions of fungi and bacteria and their associations in (sub-)alpine P. cembra forests remain vastly understudied. Here, we studied the fungal and bacterial community compositions in three independent (sub-)alpine P. cembra forests and inferred their microbial associations using marker gene sequencing and network analysis. We asked about the effect of snow cover on microbial compositions and associations. In addition, we propose inferring microbial associations across a range of filtering criteria, based on which we infer well justified, concrete microbial associations with high potential for ecological relevance that are typical for P. cembra forests and depending on snow cover.
Results
The overall fungal and bacterial community structure was comparable with regards to both forest locations and snow cover. However, occurrence, abundance, and diversity patterns of several microbial taxa typical for P. cembra forests differed among snow-free and snow covered soils, e.g. Russula, Tetracladium and Phenoliphera. Moreover, network properties and microbial associations were influenced by snow cover. Here, we present concrete microbial associations on genus and species level that were repeatedly found across microbial networks, thereby confirming their ecological relevance. Most importantly, ectomycorrhizal fungi, such as Basidioascus, Pseudotomentella and Rhizopogon, as well as saprobic Mortierella changed their bacterial association partners depending on snow cover.
Conclusion
This is the first study researching fungal-bacterial associations across several (sub-)alpine P. cembra forests. The poorly investigated influence of snow cover on soil fungi and bacteria, especially those mycorrhizing P. cembra roots, but also saprobic soil organisms, underlines the relevance of forest seasonality. Our findings highlight that the seasonal impact of snow cover has significant consequences for the ecology of the ecosystem, particularly in relation to mycorrhization and nutrient cycling. It is imperative to consider such effects for a comprehensive understanding of the functioning resilience and responsiveness of an ecosystem.
... на уровне демоценозов, пока не осознается, в том числе и при обращении к публикациям по этому вопросу (Savinov, 2011;Савинов, 2012) ряда отечественных и зарубежных исследователей (Русина, 2015;Дмитриева и др., 2016;Протасов, 2016;Theis et al., 2012;Gilbert, 2014;Voss et al., 2015;Salvucci, 2016Salvucci, , 2019Stepanova et al., 2021). А на биоценотическом и экосистемном уровнях зарубежными исследователями развиваются представления о микоризной сети («mycorrhizal network», «Wood Wide Web») (Simard et al., 2004(Simard et al., , 2012Castro-Delgado et al., 2020;Figueiredo et al., 2021), лишь частично аналогичные концепции геосимбиоза (Савинов, 2014а,б). ...
In modern conditions, it is advisable to base the study of biological sciences, especially integrative ones – the theory of evolution and ecology – on the methodology of a systemic cybernetic approach. Based on this, the book outlines the issues of organization, functioning and evolution of biological systems at different levels (organismal, population, biocenotic) in groups of organisms of various ranks and kingdoms of wildlife in terms of their activity. The book describes in detail and summarizes modern ideas about methods of studying the activity of biosystems using examples of real species of organisms and their groupings. The applied aspects of biosystemology (systemic aspects of bioindication and environmental monitoring in the light of methods for studying the activity of biosystems) are considered. The book is intended for students, teachers of biology, as well as for students and teachers of faculties where the theory of systems and control, cybernetics are studied.
... AMF are important mutualistic microorganisms that can connect the roots of plants to form CMNs. In plant-plant interactions, CMNs play a major role by interlinking the root systems of two or more host plants (Simard et al., 2012;Hoeksema, 2015). It allows distant plant individuals to communicate and help each other (Gilbert and Johnson, 2017). ...
... It is believed that interplant resource exchanges are regulated by source-sink; as such, they can form the relationship between donor and receiver. For instance, the nutrient-rich plants provide minerals to the neighboring plants, which are nutrient deficient (Simard et al., 2012). ...
Plants engage in a variety of interactions, including sharing nutrients through common mycorrhizal networks (CMNs), which are facilitated by arbuscular mycorrhizal fungi (AMF). These networks can promote the establishment, growth, and distribution of limited nutrients that are important for plant growth, which in turn benefits the entire network of plants. Interactions between plants and microbes in the rhizosphere are complex and can either be socialist or capitalist in nature, and the knowledge of these interactions is equally important for the progress of sustainable agricultural practice. In the socialist network, resources are distributed more evenly, providing benefits for all connected plants, such as symbiosis. For example, direct or indirect transfer of nutrients to plants, direct stimulation of growth through phytohormones, antagonism toward pathogenic microorganisms, and mitigation of stresses. For the capitalist network, AMF would be privately controlled for the profit of certain groups of plants, hence increasing competition between connected plants. Such plant interactions invading by microbes act as saprophytic and cause necrotrophy in the colonizing plants. In the first case, an excess of the nutritional resources may be donated to the receiver plants by direct transfer. In the second case, an unequal distribution of resources occurs, which certainly favor individual groups and increases competition between interactions. This largely depends on which of these responses is predominant (“socialist” or “capitalist”) at the moment plants are connected. Therefore, some plant species might benefit from CMNs more than others, depending on the fungal species and plant species involved in the association. Nevertheless, benefits and disadvantages from the interactions between the connected plants are hard to distinguish in nature once most of the plants are colonized simultaneously by multiple fungal species, each with its own cost-benefits. Classifying plant–microbe interactions based on their habitat specificity, such as their presence on leaf surfaces (phyllospheric), within plant tissues (endophytic), on root surfaces (rhizospheric), or as surface-dwelling organisms (epiphytic), helps to highlight the dense and intricate connections between plants and microbes that occur both above and below ground. In these complex relationships, microbes often engage in mutualistic interactions where both parties derive mutual benefits, exemplifying the socialistic or capitalistic nature of these interactions. This review discusses the ubiquity, functioning, and management interventions of different types of plant–plant and plant–microbe interactions in CMNs, and how they promote plant growth and address environmental challenges for sustainable agriculture.
... Amino acids which were found labelled across tissues here, like alanine, glutamate and leucine, have already been reported in Sullius (Ribeiro et al., 2008). Importantly, we bring preliminary evidence for amino acid transport from tree roots to EMF, as noted earlier (Simard et al., 2012). This supports the notion that, under certain conditions, plants and fungi exchange organic nitrogen, rather than importing it in alternative pathways (Henriksson et al., 2023). ...
Ectomycorrhizal fungi (EMF) are common belowground tree symbionts, supplying trees with water and nutrients. In return, large amounts of C assimilated by trees can be allocated into EMF. However, the chemical forms in which the C is transferred from trees to fungi under field conditions are mostly unknown.
In this study, we aimed to unravel the fate of tree‐derived C in EMF. We conducted ¹³ CO 2 pulse labelling of Pinus halepensis trees in two forest sites with adjacent EMF sporocarps, combined with a non‐targeted metabolomics profiling of root and sporocarp tissues. ¹³ C was measured in sporocarps of Tricholoma terreum and Suillus collinitus up to 3 m from pine stems.
C was assimilated in the labelled trees' needles and transferred to their roots. Starting from Day 2 after labelling, the C was transferred to adjacent sporocarps, peaking on Day 5. We identified more than 100 different labelled metabolites of different chemical groups present in roots and sporocarps. Of them, 17 were common to pine roots and both EMF species, and additional eight common to roots and one of the two EMF. The major labelled metabolites in the root tips were amino acids and tricarboxylic acid intermediates. The major labelled metabolites in sporocarps were amino acids, nucleotides, and fatty acids. We also identified labelled carbohydrates in all tissues. Labelling patterns diverged across different tissues, which can hint at how the C was transferred.
Considering the young tree as a sole C source for these sporocarps, and with a diurnal assimilation of 5.4 g C, the total monthly C source is ~165 g C. On average, there were 10 sporocarps around each tree, each requiring ~1 g C. Therefore, a 10 g C investment would make 6% of total tree C allocation, and about 12% of net primary productivity. Overall, we found that this significant and ubiquitous transfer of metabolites from tree roots to EMF sporocarps is more rapid and chemically diverse than once thought.
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... EM fungi exhibit higher levels of host specificity compared to AM fungi, leading to the lower competitive ability of EM trees for heterospecific in mixed forests (Schroeder et al., 2020). In addition, EM trees show a greater reliance on mycorrhizal hyphae when competing for nutrients (Chen et al., 2018;Shah et al., 2016) and benefit from the common mycorrhizal network in forest ecosystems (McGuire, 2007;Simard et al., 2012). However, the increased proportion of AM trees in the EM tree community hampers the formation of EM networks, leading to a decrease in the enzyme activity associated with N and P in the rhizosphere of EM trees (Averill et al., 2022;Cheeke et al., 2017;Liang et al., 2020;Zheng et al., 2023). ...
Plant nutrient stoichiometry is of critical importance to productivity and nutrient cycling in terrestrial ecosystems. The impacts of tree species diversity on productivity have been well studied at the stand level. However, it is unclear how neighbourhood interactions impact the foliar nutrient stoichiometry of trees at the neighbourhood scale and how plant mycorrhizal associations can mediate such effects.
We randomly selected eight tree species from a large‐scale biodiversity experiment with mixtures up to 32 tree species in subtropical China to assess the effects of species richness, phylogenetic and trait dissimilarities and competition on the foliar nutrient stoichiometry of focal trees associated with either arbuscular mycorrhizal (AM) or ectomycorrhizal (EM) fungi. We further investigated whether neighbourhood diversity can alter focal tree growth by regulating C:N:P stoichiometry.
Neighbourhood species richness had no significant impact on the foliar C:N, N:P or C:P for both AM and EM trees. Increased neighbourhood phylogenetic dissimilarity significantly decreased the foliar N:P and C:P of AM trees but did not affect those of EM tree species. Foliar C:N, N:P and C:P of AM trees decreased with increasing neighbour trait (specific leaf area, root diameter, wood density dissimilarity, total trait) dissimilarities, while those of EM trees increased or remained unchanged. The increase of the neighbourhood competition index resulted in an increase in the foliar C:N of AM tree species but not EM tree species. The structural equation model analysis revealed that the increase of neighbourhood phylogenetic dissimilarity and functional trait dissimilarity indirectly enhanced tree growth of AM trees by decreasing foliar C:N. Conversely, the increase of neighbourhood‐specific root length and wood density dissimilarity indirectly reduced the growth of EM trees by increasing foliar N:P.
Synthesis . Our results indicate that neighbourhood trait dissimilarity regulated tree foliar stoichiometry and growth performance, but the effects depended on the mycorrhizal type of trees. Our findings highlight the importance of tree mycorrhizal associations for better understanding the relationship between plant diversity and ecosystem functions.
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