A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment

The majority of vascular flowering plants are able to form symbiotic associations with arbuscular mycorrhizal fungi. These symbioses, termed arbuscular mycorrhizas, are mutually beneficial, and the fungus delivers phosphate to the plant while receiving carbon. In these symbioses, phosphate uptake by the arbuscular mycorrhizal fungus is the first step in the process of phosphate transport to the plant. Previously, we cloned a phosphate transporter gene involved in this process. Here, we analyze the expression and regulation of a phosphate transporter gene (GiPT) in the extra-radical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices during mycorrhizal association with carrot or Medicago truncatula roots. These analyses reveal that GiPT expression is regulated in response to phosphate concentrations in the environment surrounding the extra-radical hyphae and modulated by the overall phosphate status of the mycorrhiza. Phosphate concentrations, typical of those found in the soil solution, result in expression of GiPT. These data imply that G. intraradices can perceive phosphate levels in the external environment but also suggest the presence of an internal phosphate sensing mechanism.     

Symbiotic fungal associations in 'lower' land plants

An analysis of the current state of knowledge of symbiotic fungal associations in 'lower' plants is provided. Three fungal phyla, the Zygomycota, Ascomycota and Basidiomycota, are involved in forming these associations, each producing a distinctive suite of structural features in well-defined groups of 'lower' plants. Among the 'lower' plants only mosses and Equisetum appear to lack one or other of these types of association. The salient features of the symbioses produced by each fungal group are described and the relationships between these associations and those formed by the same or related fungi in 'higher' plants are discussed. Particular consideration is given to the question of the extent to which root fungus associations in 'lower' plants are analogous to 'mycorrhizas' of 'higher' plants and the need for analysis of the functional attributes of these symbioses is stressed. Zygomycetous fungi colonize a wide range of extant lower land plants (hornworts, many hepatics, lycopods, Ophioglossales, Psilotales and Gleicheniaceae), where they often produce structures analogous to those seen in the vesicular-arbuscular (VA) mycorrhizas of higher plants, which are formed by members of the order Glomales. A preponderance of associations of this kind is in accordance with palaeohbotanical and molecular evidence indicating that glomalean fungi produced the archetypal symbioses with the first plants to emerge on to land. It is shown, probably for the first time, that glomalean fungi forming typical VA mycorrhiza with a higher plant (Plantago lanceolata) can colonize a thalloid liverwort (Pellia epiphylla), producing arbuscules and vesicles in the hepatic. The extent to which these associations, which are structurally analogous to mycorrhizas, have similar functions remains to be evaluated. Ascomycetous associations are found in a relatively small number of families of leafy liverworts. The structural features of the fungal colonization of rhizoids and underground axes of these plants are similar to those seen in mycorrhizal associations of ericaceous plants like Vaccinium. Cross inoculation experiments have confirmed that a typical mycorrhizal endophyte of ericaceous plants, Hymenoscyphus ericae, will form associations in liverworts which are structurally identical to those seen in nature. Again, the functional significance of these associations remains to be examined. Some members of the Jungermanniales and Metzgeriales form associations with basidiomycetous fungi. These produce intracellular coils of hyphae, which are similar to the pelotons seen in orchid mycorrhizas, which also involve basidiomycetes. The fungal associates of the autotrophic Aneura and of its heterotrophic relative Cryptothallus mirabilis have been isolated. In the latter case it has been shown that the fungal symbiont is an ectomycorrhizal associate of Betula, suggesting that the apparently obligate nature of the association between the hepatic and Betula in nature is based upon requirement for this particular heterotroph.     

Non-host plants: Are they mycorrhizal networks players?

Common mycorrhizal networks (CMNs) that connect individual plants of the same or different species together play important roles in nutrient and signal transportation, and plant community organization. However, about 10% of land plants are non-mycorrhizal species with roots that do not form any well-recognized types of mycorrhizas; and each mycorrhizal fungus can only colonize a limited number of plant species, resulting in numerous non-host plants that could not establish typical mycorrhizal symbiosis with a specific mycorrhizal fungus. If and how non-mycorrhizal or non-host plants are able to involve in CMNs remains unclear. Here we summarize studies focusing on mycorrhizal-mediated host and non-host plant interaction. Evidence has showed that some host-supported both arbuscular mycorrhizal (AM) and ectomycorrhizal (EM) hyphae can access to non-host plant roots without forming typical mycorrhizal structures, while such non-typical mycorrhizal colonization often inhibits the growth but enhances the induced system resistance of non-host plants. Meanwhile, the host growth is also differentially affected, depending on plant and fungi species. Molecular analyses suggested that the AMF colonization to non-hosts is different from pathogenic and endophytic fungi colonization, and the hyphae in non-host roots may be alive and have some unknown functions. Thus we propose that non-host plants are also important CMNs players. Using non-mycorrhizal model species Arabidopsis, tripartite culture system and new technologies such as nanoscale secondary ion mass spectrometry and multi-omics, to study nutrient and signal transportation between host and non-host plants via CMNs may provide new insights into the mechanisms underlying benefits of intercropping and agro-forestry systems, as well as plant community establishment and stability.     

Diversity and classification of mycorrhizal associations

Most mycorrhizas are 'balanced' mutualistic associations in which the fungus and plant exchange commodities required for their growth and survival. Myco-heterotrophic plants have 'exploitative' mycorrhizas where transfer processes apparently benefit only plants. Exploitative associations are symbiotic (in the broad sense), but are not mutualistic. A new definition of mycorrhizas that encompasses all types of these associations while excluding other plant-fungus interactions is provided. This definition recognises the importance of nutrient transfer at an interface resulting from synchronised plant-fungus development. The diversity of interactions between mycorrhizal fungi and plants is considered. Mycorrhizal fungi also function as endophytes, necrotrophs and antagonists of host or non-host plants, with roles that vary during the lifespan of their associations. It is recommended that mycorrhizal associations are defined and classified primarily by anatomical criteria regulated by the host plant. A revised classification scheme for types and categories of mycorrhizal associations defined by these criteria is proposed. The main categories of vesicular-arbuscular mycorrhizal associations (VAM) are 'linear' or 'coiling', and of ectomycorrhizal associations (ECM) are 'epidermal' or 'cortical'. Subcategories of coiling VAM and epidermal ECM occur in certain host plants. Fungus-controlled features result in 'morphotypes' within categories of VAM and ECM. Arbutoid and monotropoid associations should be considered subcategories of epidermal ECM and ectendomycorrhizas should be relegated to an ECM morphotype. Both arbuscules and vesicles define mycorrhizas formed by glomeromycotan fungi. A new classification scheme for categories, subcategories and morphotypes of mycorrhizal associations is provided.     

Conservative ecological and evolutionary patterns in liverwort–fungal symbioses

Liverworts, the most ancient group of land plants, form a range of intimate associations with fungi that may be analogous to the mycorrhizas of vascular plants. Most thalloid liverworts contain arbuscular mycorrhizal glomeromycete fungi similar to most vascular plants. In contrast, a range of leafy liverwort genera and one simple thalloid liverwort family (the Aneuraceae) have switched to basidiomycete fungi. These liverwort switches away from glomeromycete fungi may be expected to parallel switches undergone by vascular plants that target diverse lineages of basidiomycete fungi to form ectomycorrhizas. To test this hypothesis, we used a cultivation-independent approach to examine the basidiomycete fungi associated with liverworts in varied worldwide locations by generating fungal DNA sequence data from over 200 field collections of over 30 species. Here we show that eight leafy liverwort genera predominantly and consistently associate with members of the Sebacina vermifera species complex and that Aneuraceae thalloid liverworts associate nearly exclusively with Tulasnella species. Furthermore, within sites where multiple liverwort species co-occur, they almost never share the same fungi. Our analyses reveal a strikingly conservative ecological and evolutionary pattern of liverwort symbioses with basidiomycete fungi that is unlike that of vascular plant mycorrhizas.     

Further advances in orchid mycorrhizal research

Orchid mycorrhizas are mutualistic interactions between fungi and members of the Orchidaceae, the world’s largest plant family. The majority of the world’s orchids are photosynthetic, a small number of species are myco-heterotrophic throughout their lifetime, and recent research indicates a third mode (mixotrophy) whereby green orchids supplement their photosynthetically fixed carbon with carbon derived from their mycorrhizal fungus. Molecular identification studies of orchid-associated fungi indicate a wide range of fungi might be orchid mycobionts, show common fungal taxa across the globe and support the view that some orchids have specific fungal interactions. Confirmation of mycorrhizal status requires isolation of the fungi and restoration of functional mycorrhizas. New methods may now be used to store orchid-associated fungi and store and germinate seed, leading to more efficient culture of orchid species. However, many orchid mycorrhizas must be synthesised before conservation of these associations can be attempted in the field. Further gene expression studies of orchid mycorrhizas are needed to better understand the establishment and maintenance of the interaction. These data will add to efforts to conserve this diverse and valuable association.     

Transport processes at the plant-fungus interface in mycorrhizal associations: physiological studies

The roots of most plants form symbiotic associations with mycorrhizal fungi. The net flux of nutrients, particularly phosphorus (P), from the soil into the plant is greater in mycorrhizal than in comparable non-mycorrhizal plants. However despite the widespread occurrence of mycorrhizal associations the processes controlling the transfer of solutes between the symbionts are poorly understood. To understand the mechanisms regulating the transfer of solutes information about conditions at the interface between plant and fungus is needed.Measurements of apoplastic and intracellular electrical potential difference in leek roots colonised by mycorrhizal fungi and estimates of cytosolic pH in fungal hyphae are presented. These and the implications for plant/fungal mineral nutrition in vesicular-arbuscular mycorrhizas are discussed.     

Fungi associated with terrestrial orchid mycorrhizas,seeds and protocorms

The identity and ecological role of fungi in the mycorrhizal roots of 25 species of mature terrestrial orchids and in 17 species of field incubated orchid seedlings were examined. Isolates of symbiotic fungi from mature orchid mycorrhizas were basidiomycetes primarily in the generaCeratorhiza, Epulorhiza andMoniliopsis; a few unidentified taxa with clamped hyphae were also recovered. More than one taxon of peloton-forming fungus was often observed in the cleared and stained mycorrhizas. AlthoughCeratorhiza andEpulorhiza strains were isolated from the developing protocorms, pelotons of clamped hyphae were often presents in the cleared protocorms of several orchid species. These basidiomycetes are difficult to isolate and may be symbionts of ectotrophic plants. The higher proportion of endophytes bearing clamp connections in developing seeds than in the mycorrhizas is attributed to differences in the nutritional requirements of the fully mycotrophic protocorms and partially autotrophic plants. Most isolates ofCeratorhiza differed enzymatically fromEpulorhiza in producing polyphenol oxidases. Dual cultures with thirteen orchid isolates and five non-orchid hosts showed that some taxa can form harmless associations with non-orchid hosts. It is suggested that most terrestrial orchid mycorrhizas are relatively non-specific and that the mycobionts can be saprophytes, parasites or mycorrhizal associates of other plants.     

Patterns of plant naturalization show that facultative mycorrhizal plants are more likely to succeed outside their native Eurasian ranges

The naturalization of an introduced species is a key stage during the invasion process. Therefore, identifying the traits that favor the naturalization of non-native species can help understand why some species are more successful when introduced to new regions. The ability and the requirement of a plant species to form a mutualism with mycorrhizal fungi, together with the types of associations formed may play a central role in the naturalization success of different plant species. To test the relationship between plant naturalization success and their mycorrhizal associations we analysed a database composed of mycorrhizal status and type for 1981 species, covering 155 families and 822 genera of plants from Europe and Asia, and matched it with the most comprehensive database of naturalized alien species across the world (GloNAF). In mainland regions, we found that the number of naturalized regions was highest for facultative mycorrhizal, followed by obligate mycorrhizal and lowest for non-mycorrhizal plants, suggesting that the ability of forming mycorrhizas is an advantage for introduced plants. We considered the following mycorrhizal types: arbuscular, ectomycorrhizal, ericoid and orchid mycorrhizal plants. Further, dual mycorrhizal species were those that included observations of arbuscular mycorrhizas as well as observations of ectomycorrhizas. Naturalization success (based on the number of naturalized regions) was highest for arbuscular mycorrhizal and dual mycorrhizal plants, which may be related to the low host specificity of arbuscular mycorrhizal fungi and the consequent high availability of arbuscular mycorrhizal fungal partners. However, these patterns of naturalization success were erased in islands, suggesting that the ability to form mycorrhizas may not be an advantage for establishing self-sustaining populations in isolated regions. Taken together our results show that mycorrhizal status and type play a central role in the naturalization process of introduced plants in many regions, but that their effect is modulated by other factors.     

Untangling above‐ and belowground mycorrhizal fungal networks in tropical orchids

Orchids typically depend on fungi for establishment from seeds, forming mycorrhizal associations with basidiomycete fungal partners in the polyphyletic group rhizoctonia from early stages of germination, sometimes with very high specificity. This has raised important questions about the roles of plant and fungal phylogenetics, and their habitat preferences, in controlling which fungi associate with which plants. In this issue of Molecular Ecology, Martos et al. (2012) report the largest network analysis to date for orchids and their mycorrhizal fungi, sampling a total of over 450 plants from nearly half the 150 tropical orchid species on Reunion Island, encompassing its main terrestrial and epiphytic orchid genera. The authors found a total of 95 operational taxonomic units of mycorrhizal fungi and investigated the architecture and nestedness of their bipartite networks with 73 orchid species. The most striking finding was a major ecological barrier between above‐ and belowground mycorrhizal fungal networks, despite both epiphytic and terrestrial orchids often associating with closely related taxa across all three major lineages of rhizoctonia fungi. The fungal partnerships of the epiphytes and terrestrial species involved a diversity of fungal taxa in a modular network architecture, with only about one in ten mycorrhizal fungi partnering orchids in both groups. In contrast, plant and fungal phylogenetics had weak or no effects on the network. This highlights the power of recently developed ecological network analyses to give new insights into controls on plant–fungal symbioses and raises exciting new hypotheses about the differences in properties and functioning of mycorrhiza in epiphytic and terrestrial orchids.     

Ericaceous plant–fungus network in a harsh alpine–subalpine environment

In terrestrial ecosystems, plant species and diverse root‐associated fungi form complex networks of host–symbiont associations. Recent studies have revealed that structures of those below‐ground plant–fungus networks differ between arbuscular mycorrhizal and ectomycorrhizal symbioses. Nonetheless, we still remain ignorant of how ericaceous plant species, which dominate arctic and alpine tundra, constitute networks with their root‐associated fungi. Based on a high‐throughput DNA sequencing data set, we characterized the statistical properties of a network involving 16 ericaceous plant species and more than 500 fungal taxa in the alpine–subalpine region of Mt. Tateyama, central Japan. While all the 16 ericaceous species were associated mainly with fungi in the order Helotiales, they varied remarkably in association with fungi in other orders such as Sebacinales, Atheliales, Agaricales, Russulales and Thelephorales. The ericaceous plant–fungus network was characterized by high symbiont/host preferences. Moreover, the network had a characteristic structure called ‘anti‐nestedness’, which has been previously reported in ectomycorrhizal plant–fungus networks. The results lead to the hypothesis that ericaceous plants in harsh environments can host unexpectedly diverse root‐associated fungal taxa, constituting networks whose structures are similar to those of previously reported ectomycorrhizal networks but not to those of arbuscular mycorrhizal ones.     

Functional compatibility in cucumber mycorrhizas in terms of plant growth performance and foliar nutrient composition

Functional compatibility in cucumber mycorrhizas in terms of plant and fungal growth, and foliar nutrient composition from all possible combinations of six cucumber varieties and three species of arbuscular mycorrhizal (AM) fungi was evaluated. Measurements of foliar nutrient composition included N, P, K, Mg, Ca, Na, Fe, Zn, Mn and Cu. Growth of AM fungi was measured in terms of root colonisation, as examined with microscopy and the AM fungus biomarker fatty acid 16:1ω5 from both phospholipids and neutral lipids. Different responses of plant growth and foliar nutrient profiles were observed for the different AM symbioses examined. The AM fungus Claroideoglomus claroideum caused growth depression in association with four out of six cucumber varieties; Rhizophagus irregularis caused growth promotion in one of six cucumber varieties; whereas Funneliformis mosseae had no effect on the growth performance of any of the cucumber varieties examined. All three AM fungi markedly altered host plant shoot nutrient composition, with the strongest contrast observed between cucumber–R. irregularis symbioses and non‐mycorrhizal cucumber plants, independent of cucumber variety. On the other hand, AM fungal growth in roots differed between the three AM fungi, but was unaffected by host genotype. Strong build‐up of storage lipids was observed for R. irregularis, which was more moderate in the two other AM fungi. In conclusion, strong differential responses of cucumber varieties to inoculation with different AM fungi in terms of growth and shoot nutrient composition revealed high functional diversity in AM symbioses in cucumber plants.     

Application of network theory to potential mycorrhizal networks

The concept of a common mycorrhizal network implies that the arrangement of plants and mycorrhizal fungi in a community shares properties with other networks. A network is a system of nodes connected by links. Here we apply network theory to mycorrhizas to determine whether the architecture of a potential common mycorrhizal network is random or scale-free. We analyzed mycorrhizal data from an oak woodland from two perspectives: the phytocentric view using trees as nodes and fungi as links and the mycocentric view using fungi as nodes and trees as links. From the phytocentric perspective, the distribution of potential mycorrhizal links, as measured by the number of ectomycorrhizal morphotypes on trees of Quercus garryana, was random with a short tail, implying that all the individuals of this species are more or less equal in linking to fungi in a potential network. From the mycocentric perspective, however, the distribution of plant links to fungi was scale-free, suggesting that certain fungus species may act as hubs with frequent connections to the network. Parallels exist between social networks and mycorrhizas that suggest future lines of study on mycorrhizal networks.     

Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis

A comprehensive appraisal of the mycorrhizal literature provides data for 336 plant families representing 99% of flowering plants, with regard to mycorrhizas and other nutritional adaptations. In total, arbuscular (AM), orchid, ectomycorrhizas (EM) and ericoid mycorrhizas and nonmycorrhizal (NM) roots occur in 74%, 9%, 2%, 1% and 6% of Angiosperm species respectively. Many families of NM plants have alternative nutritional strategies such as parasitism, carnivory, or cluster roots. The remaining angiosperms (8%) belong to families reported to have both AM and NM species. These are designated as NM-AM families here and tend to occur in habitats considered non-conducive to mycorrhizal fungi, such as epiphytic, aquatic, extremely cold, dry, disturbed, or saline habitats. Estimated numbers of species in each category of mycorrhizas is presented with lists of NM and EM families. Evolutionary trends are also summarised by providing data on all clades and orders of flowering and non-flowering vascular plants on a global scale. A case study of Western Australian plants revealed that plants with specialised nutritional modes such as carnivory, cluster roots, or EM were much more diverse in this ancient landscape with infertile soils than elsewhere. Detailed information on the mycorrhizal diversity of plants presented here is linked to a website (mycorrhizas.info) to allow data to remain current. Over a century of research effort has resulted in data on mycorrhizal associations of >10,000 plant species that are of great value, but also somewhat of a liability due to conflicting information about some families and genera. It is likely that these conflicts result in part from misdiagnosis of mycorrhizal associations resulting from a lack of standardisation in criteria used to define them. Families that contain both NM and AM species provide a second major source of inconsistency, but even when these are excluded there is a ～10% apparent error rate in published lists of mycorrhizal plants. Arbuscules are linked to AM misdiagnosis since they are used less often than vesicles to recognise AM associations in roots and apparently occur sporadically in NM plants. Key issues with the diagnosis of mycorrhizal plants are discussed using the Cyperaceae as a case study. Detailed protocols designed to consistently distinguish AM from endophytic Glomeromycotan Fungus Colonisation (GFC) are provided. This review aims to stimulate debate and provide advice to researchers delving into root biology.     

Highly diverse and spatially heterogeneous mycorrhizal symbiosis in a rare epiphyte is unrelated to broad biogeographic or environmental features

Symbiotic interactions are common in nature. In dynamic or degraded environments, the ability to associate with multiple partners (i.e. broad specificity) may enable species to persist through fluctuations in the availability of any particular partner. Understanding how species interactions vary across landscapes is necessary to anticipate direct and indirect consequences of environmental degradation on species conservation. We asked whether mycorrhizal symbiosis by populations of a rare epiphytic orchid (Epidendrum firmum) is related to geographic or environmental heterogeneity. The latter would suggest that interactions are governed by environmental conditions rather than historic isolation of populations and/or mycorrhizal fungi. We used DNA-based methods to identify mycorrhizal fungi from eleven E. firmum populations in Costa Rica. We used molecular and phylogenetic analyses to compare associations. Epidendrum firmum exhibited broad specificity, associating with diverse mycorrhizal fungi, including six Tulasnellaceae molecular operational taxonomic units (MOTUs), five Sebacinales MOTUs and others. Notably, diverse mycorrhizal symbioses formed in disturbed pasture and roadside habitats. Mycorrhizal fungi exhibited significant similarity within populations (spatial and phylogenetic autocorrelation) and significant differences among populations (phylogenetic community dissimilarity). However, mycorrhizal symbioses were not significantly associated with biogeographic or environmental features. Such unexpected heterogeneity among populations may result from complex combinations of fine-scale environmental factors and macro-evolutionary patterns of change in mycorrhizal specificity. Thus, E. firmum exhibits broad specificity and the potential for opportunistic associations with diverse fungi. We suggest that these characteristics could confer symbiotic assurance when mycorrhizal fungi are stochastically available, which may be crucial in dynamic or disturbed habitats such as tropical forest canopies.     

Mutualism and parasitism: the yin and yang of plant symbioses

Plants are solar-powered sugar factories that feed a multitude of other organisms. Many of these organisms associate directly with host plants to gain access to the plant's photosynthates. Such symbioses encompass a wide collection of styles ranging from mutualistic to commensal and parasitic. Among these, the mutualistic arbuscular mycorrhizal (AM) symbiosis is one of the evolutionarily oldest symbioses of plants, relying on the formation of an intimate relationship between fungi of the Glomeromycota and roots of the majority of vascular flowering plants. In this symbiosis, the fungus intracellularly colonizes living root cells, implying the existence of an extreme form of compatibility. Interestingly, molecular events that happen in the plant in response to mycorrhizal colonization also occur in other beneficial and, as recently shown, even antagonistic plant symbioses. Thus, basic 'compatibility modules' appear to be partially conserved between mutualism and parasitism.     

基于SCI文献分析我国菌根学研究现状和发展方向

基于美国科学情报研究所(ISI)科学引文索引(Science Citation Index, SCI)数据库, 对1989~2007年期间我国发表的菌根研究论文进行检索, 并采用文献计量方法对所获资料进行统计和趋势分析。结果表明, 1989~2007年间, 我国菌根学研究呈现不断上升趋势, 尤其是2000年之后, 增长速度明显加快。但只有5.22%的论文发表于影响因子大于5的刊物, 在研究深度上仍需进一步加强。半数以上的研究论文与丛枝菌根研究有关, 研究重点主要集中在菌根对植物的生理效应, 菌根与植物抗性     

Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis

Liverworts form endophytic associations with fungi that mirror mycorrhizal associations in tracheophytes. Here we report a worldwide survey of liverwort associations with glomeromycotean fungi (GAs), together with a comparative molecular and cellular analysis in representative species. Liverwort GAs are circumscribed by a basal assemblage embracing the Haplomitriopsida, the Marchantiopsida (except a few mostly derived clades), and part of the Metzgeriidae. Fungal endophytes from Haplomitrium, Conocephalum, Fossombronia, and Pellia were related to Glomus Group A, while the endophyte from Monoclea was related to Acaulospora. An isolate of G. mosseae colonized axenic thalli of Conocephalum, producing an association similar to that in the wild. Fungal colonization in marchantialean liverworts suppressed cell wall autofluorescence and elicited the deposition of a new wall layer that specifically bound the monoclonal antibody CCRC-M1 against fucosylated side groups associated with xyloglucan and rhamnogalacturonan I. The interfacial material covering the intracellular fungus contained the same epitopes present in host cell walls. The taxonomic distribution and cytology of liverwort GAs suggest an ancient origin and multiple more recent losses, but the occurence in widely separated liverwort taxa of fungi related to glomeromycotean lineages that form arbuscular mycorrhizas in tracheophytes, notably the Glomus Group A, is better explained by host shifting from tracheophytes to liverworts.     

Diversity and Spatial Structure of Belowground Plant–Fungal Symbiosis in a Mixed Subtropical Forest of Ectomycorrhizal and Arbuscular Mycorrhizal Plants

Plant–mycorrhizal fungal interactions are ubiquitous in forest ecosystems. While ectomycorrhizal plants and their fungi generally dominate temperate forests, arbuscular mycorrhizal symbiosis is common in the tropics. In subtropical regions, however, ectomycorrhizal and arbuscular mycorrhizal plants co-occur at comparable abundances in single forests, presumably generating complex community structures of root-associated fungi. To reveal root-associated fungal community structure in a mixed forest of ectomycorrhizal and arbuscular mycorrhizal plants, we conducted a massively-parallel pyrosequencing analysis, targeting fungi in the roots of 36 plant species that co-occur in a subtropical forest. In total, 580 fungal operational taxonomic units were detected, of which 132 and 58 were probably ectomycorrhizal and arbuscular mycorrhizal, respectively. As expected, the composition of fungal symbionts differed between fagaceous (ectomycorrhizal) and non-fagaceous (possibly arbuscular mycorrhizal) plants. However, non-fagaceous plants were associated with not only arbuscular mycorrhizal fungi but also several clades of ectomycorrhizal (e.g., Russula) and root-endophytic ascomycete fungi. Many of the ectomycorrhizal and root-endophytic fungi were detected from both fagaceous and non-fagaceous plants in the community. Interestingly, ectomycorrhizal and arbuscular mycorrhizal fungi were concurrently detected from tiny root fragments of non-fagaceous plants. The plant–fungal associations in the forest were spatially structured, and non-fagaceous plant roots hosted ectomycorrhizal fungi more often in the proximity of ectomycorrhizal plant roots. Overall, this study suggests that belowground plant–fungal symbiosis in subtropical forests is complex in that it includes “non-typical” plant–fungal combinations (e.g., ectomycorrhizal fungi on possibly arbuscular mycorrhizal plants) that do not fall within the conventional classification of mycorrhizal symbioses, and in that associations with multiple functional (or phylogenetic) groups of fungi are ubiquitous among plants. Moreover, ectomycorrhizal fungal symbionts of fagaceous plants may “invade” the roots of neighboring non-fagaceous plants, potentially influencing the interactions between non-fagaceous plants and their arbuscular-mycorrhizal fungal symbionts at a fine spatial scale.     

Micronutrient transport in mycorrhizal symbiosis; zinc steals the show

Mycorrhizas are mutually beneficial associations between soil-borne fungi and plant roots. Mycorrhizal fungi provide their host plant with essential nutrients in exchange for sugars and/or lipids. Traditionally, transport and translocation of macronutrients, including nitrogen and phosphorus, throughout the fungal mycelium and towards the host plant are well studied. However, the regulation of nutrient exchange and their contribution in the morphogenesis and development of mycorrhizas remains unclear. In this Opinion, we argue that adding micronutrients in the current models of symbiotic transport is essential to fully understand the establishment, maintenance, and functioning of mycorrhizal associations. Homeostatic mechanisms at the cellular level and the first transport proteins involved have been recently documented for zinc (Zn) in arbuscular mycorrhizal, ectomycorrhizal, and ericoid mycorrhizal fungi. Mycorrhizal plants benefit from an improved Zn status in control conditions and are better protected when environmental Zn availability fluctuates. These recent progresses are paving the way for a better understanding of micronutrient allocation in mycorrhizas. Revising our vision on the role of micronutrients, particularly of Zn, in these interactions will allow a better use of mycorrhizal fungi in sustainable agriculture and forestry, and will increase management practices in waste land, as well as in agricultural and natural ecosystems.