During the diversification of Fungi and the rise of conifer-dominated and angiosperm- dominated forests, mutualistic symbioses developed between certain trees and ectomycorrhizal fungi that enabled ...these trees to colonize boreal and temperate regions. The evolutionary success of these symbioses is evident from phylogenomic analyses that suggest that ectomycorrhizal fungi have arisen in approximately 60 independent saprotrophic lineages, which has led to the wide range of ectomycorrhizal associations that exist today. In this Review, we discuss recent genomic studies that have revealed the adaptations that seem to be fundamental to the convergent evolution of ectomycorrhizal fungi, including the loss of some metabolic functions and the acquisition of effectors that facilitate mutualistic interactions with host plants. Finally, we consider how these insights can be integrated into a model of the development of ectomycorrhizal symbioses.
The roots of Arabidopsis thaliana host diverse fungal communities that affect plant health and disease states. Here, we sequence the genomes of 41 fungal isolates representative of the A. thaliana ...root mycobiota for comparative analysis with other 79 plant-associated fungi. Our analyses indicate that root mycobiota members evolved from ancestors with diverse lifestyles and retain large repertoires of plant cell wall-degrading enzymes (PCWDEs) and effector-like small secreted proteins. We identify a set of 84 gene families associated with endophytism, including genes encoding PCWDEs acting on xylan (family GH10) and cellulose (family AA9). Transcripts encoding these enzymes are also part of a conserved transcriptional program activated by phylogenetically-distant mycobiota members upon host contact. Recolonization experiments with individual fungi indicate that strains with detrimental effects in mono-association with the host colonize roots more aggressively than those with beneficial activities, and dominate in natural root samples. Furthermore, we show that the pectin-degrading enzyme family PL1_7 links aggressiveness of endophytic colonization to plant health.
Linking community composition to ecosystem function is a challenge in complex microbial communities. We tested the hypothesis that key biological features of fungi - evolutionary history, functional ...guild, and abundance of functional genes – can predict the biogeochemical activity of fungal species during decay. We measured the activity of 10 different enzymes produced by 48 model fungal species on leaf litter in laboratory microcosms. Taxa included closely related species with different ecologies (i.e. species in different “functional guilds”) and species with publicly available genomes. Decomposition capabilities differed less among phylogenetic lineages of fungi than among different functional guilds. Activity of carbohydrases and acid phosphatase was significantly higher in litter colonized by saprotrophs compared to ectomycorrhizal species. By contrast, oxidoreductase activities per unit fungal biomass were statistically similar across functional guilds, with white rot fungi having highest polyphenol oxidase activity and ectomycorrhizal fungi having highest peroxidase activity. On the ecosystem level, polyphenol oxidase activity in soil correlated with the abundance of white rot fungi, while soil peroxidase activity correlated with the abundance of ectomycorrhizal fungi in soil. Copy numbers of genes coding for different enzymes explained the activity of some carbohydrases and polyphenol oxidase produced by fungi in culture, but were not significantly better predictors of activity than specific functional guild. Collectively, our data suggest that quantifying the specific functional guilds of fungi in soil, potentially through environmental sequencing approaches, allows us to predict activity of enzymes that drive soil biogeochemical cycles.
•We tested which biological features of fungi predict their enzyme activities.•Functional guild (saprotrophs vs. ectomycorrhizal) best predicted enzyme activity.•Functional gene abundance predicted functional guild of fungi.•Ectomycorrhizal fungi produced peroxidase activity equal to white rots.•Functional guilds predicted enzyme activities in field soil across the U.S.
Ectomycorrhizal fungi, such as Laccaria bicolor, support forest growth and sustainability by providing growth-limiting nutrients to their plant host through a mutualistic symbiotic relationship with ...host roots. We have previously shown that the effector protein MiSSP7 (Mycorrhiza-induced Small Secreted Protein 7) encoded by L. bicolor is necessary for the establishment of symbiosis with host trees, although the mechanistic reasoning behind this role was unknown. We demonstrate here that MiSSP7 interacts with the host protein PtJAZ6, a negative regulator of jasmonic acid (JA)-induced gene regulation in Populus. As with other characterized JASMONATE ZIM-DOMAIN (JAZ) proteins, PtJAZ6 interacts with PtCOI1 in the presence of the JA mimic coronatine, and PtJAZ6 is degraded in plant tissues after JA treatment. The association between MiSSP7 and PtJAZ6 is able to protect PtJAZ6 from this JA-induced degradation. Furthermore, MiSSP7 is able to block—or mitigate—the impact of JA on L. bicolor colonization of host roots. We show that the loss of MiSSP7 production by L. bicolor can be complemented by transgenically varying the transcription of PtJAZ6 or through inhibition of JA-induced gene regulation. We conclude that L. bicolor, in contrast to arbuscular mycorrhizal fungi and biotrophic pathogens, promotes mutualism by blocking JA action through the interaction of MiSSP7 with PtJAZ6.
Despite the pivotal role of jasmonic acid in the outcome of plant-microorganism interactions, JA-signaling components in roots of perennial trees like western balsam poplar (Populus trichocarpa) are ...poorly characterized. Here we decipher the poplar-root JA-perception complex centered on PtJAZ6, a co-repressor of JA-signaling targeted by the effector protein MiSSP7 from the ectomycorrhizal basidiomycete Laccaria bicolor during symbiotic development. Through protein-protein interaction studies in yeast we determined the poplar root proteins interacting with PtJAZ6. Moreover, we assessed via yeast triple-hybrid how the mutualistic effector MiSSP7 reshapes the association between PtJAZ6 and its partner proteins. In the absence of the symbiotic effector, PtJAZ6 interacts with the transcription factors PtMYC2s and PtJAM1.1. In addition, PtJAZ6 interacts with it-self and with other Populus JAZ proteins. Finally, MiSSP7 strengthens the binding of PtJAZ6 to PtMYC2.1 and antagonizes PtJAZ6 homo-/heterodimerization. We conclude that a symbiotic effector secreted by a mutualistic fungus may promote the symbiotic interaction through altered dynamics of a JA-signaling-associated protein-protein interaction network, maintaining the repression of PtMYC2.1-regulated genes.
Orchids are highly dependent on their mycorrhizal fungal partners for nutrient supply, especially during early developmental stages. In addition to organic carbon, nitrogen (N) is probably a major ...nutrient transferred to the plant because orchid tissues are highly N-enriched. We know almost nothing about the N form preferentially transferred to the plant or about the key molecular determinants required for N uptake and transfer.
We identified, in the genome of the orchid mycorrhizal fungus Tulasnella calospora, two functional ammonium transporters and several amino acid transporters but found no evidence of a nitrate assimilation system, in agreement with the N preference of the free-living mycelium grown on different N sources.
Differential expression in symbiosis of a repertoire of fungal and plant genes involved in the transport and metabolism of N compounds suggested that organic N may be the main form transferred to the orchid host and that ammonium is taken up by the intracellular fungus from the apoplatic symbiotic interface.
This is the first study addressing the genetic determinants of N uptake and transport in orchid mycorrhizas, and provides a model for nutrient exchanges at the symbiotic interface, which may guide future experiments.
Soil-borne mutualistic fungi, such as the ectomycorrhizal fungi, have helped shape forest communities worldwide over the last 180 million years through a mutualistic relationship with tree roots in ...which the fungal partner provides a large array of nutrients to the plant host in return for photosynthetically derived sugars 1, 2. This exchange is essential for continued growth and productivity of forest trees, especially in nutrient-poor soils. To date, the signals from the two partners that mediate this symbiosis have remained uncharacterized. Here we demonstrate that MYCORRHIZAL iNDUCED SMALL SECRETED PROTEIN 7 (MiSSP7), the most highly symbiosis-upregulated gene from the ectomycorrhizal fungus Laccaria bicolor 3, encodes an effector protein indispensible for the establishment of mutualism. MiSSP7 is secreted by the fungus upon receipt of diffusible signals from plant roots, imported into the plant cell via phosphatidylinositol 3-phosphate-mediated endocytosis, and targeted to the plant nucleus where it alters the transcriptome of the plant cell. L. bicolor transformants with reduced expression of MiSSP7 do not enter into symbiosis with poplar roots. MiSSP7 resembles effectors of pathogenic fungi, nematodes, and bacteria that are similarly targeted to the plant nucleus to promote colonization of the plant tissues 4–9 and thus can be considered a mutualism effector.
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► Identification of MiSSP7 as the first symbiotic effector protein critical to symbiosis ► MiSSP7 is actively taken up into plant cells without the need of fungal machinery ► MiSSP7 localizes to host nuclei upon cell entry where it alters host transcription ► Nuclear localization of MiSSP7 is necessary for its role in promoting symbiosis
Root systems of host trees are known to establish ectomycorrhizae (ECM) interactions with rhizospheric fungi. This mutualistic association leads to dramatic developmental modifications in root ...architecture, with the formation of numerous short and swollen lateral roots ensheathed by a fungal mantle. Knowing that auxin plays a crucial role in root development, we investigated how auxin metabolism, signaling, and response are affected in poplar (Populus spp.)-Laccaria bicolor ECM roots. The plant-fungus interaction leads to the arrest of lateral root growth with simultaneous attenuation of the synthetic auxin response element DR5. Measurement of auxin-related metabolites in the free-living partners revealed that the mycelium of L. bicolor produces high concentrations of the auxin indole-3-acetic acid (IAA). Metabolic profiling showed an accumulation of IAA and changes in the indol-3-pyruvic acid-dependent IAA biosynthesis and IAA conjugation and degradation pathways during ECM formation. The global analysis of auxin response gene expression and the regulation of AUXIN SIGNALING F-BOX PROTEIN5, AUXIN/IAA, and AUXIN RESPONSE FACTOR expression in ECM roots suggested that symbiosis-dependent auxin signaling is activated during the colonization by L. bicolor. Taking all this evidence into account, we propose a model in which auxin signaling plays a crucial role in the modification of root growth during ECM formation.
The plant hormones ethylene, jasmonic acid and salicylic acid have interconnecting roles during the response of plant tissues to mutualistic and pathogenic symbionts. We used morphological studies of ...transgenic‐ or hormone‐treated Populus roots as well as whole‐genome oligoarrays to examine how these hormones affect root colonization by the mutualistic ectomycorrhizal fungus Laccaria bicolor S238N. We found that genes regulated by ethylene, jasmonic acid and salicylic acid were regulated in the late stages of the interaction between L. bicolor and poplar. Both ethylene and jasmonic acid treatments were found to impede fungal colonization of roots, and this effect was correlated to an increase in the expression of certain transcription factors (e.g. ETHYLENE RESPONSE FACTOR1) and a decrease in the expression of genes associated with microbial perception and cell wall modification. Further, we found that ethylene and jasmonic acid showed extensive transcriptional cross‐talk, cross‐talk that was opposed by salicylic acid signaling. We conclude that ethylene and jasmonic acid pathways are induced late in the colonization of root tissues in order to limit fungal growth within roots. This induction is probably an adaptive response by the plant such that its growth and vigor are not compromised by the fungus.
Boreal peatlands play a crucial role in global carbon cycling, acting as an important carbon reservoir. However, little information is available on how peatland microbial communities are influenced ...by natural variability or human-induced disturbances. In this study, we have investigated the fungal diversity and community structure of both the organic soil layer and buried wood in boreal forest soils using high-throughput sequencing of the internal transcribed spacer (ITS) region. We have also compared the fungal communities during the primary colonization of wood with those of the surrounding soils. A permutational multivariate analysis of variance (PERMANOVA) confirmed that the community composition significantly differed between soil types (P< 0.001) and tree species (P< 0.001). The distance-based linear models analysis showed that environmental variables were significantly correlated with community structure (P< 0.04). The availability of soil nutrients (Ca P= 0.002, Fe P= 0.003, and P P= 0.003) within the site was an important factor in the fungal community composition. The species richness in wood was significantly lower than in the corresponding soil (P< 0.004). The results of the molecular identification were supplemented by fruiting body surveys. Seven of the genera of Agaricomycotina identified in our surveys were among the top 20 genera observed in pyrosequencing data. Our study is the first, to our knowledge, fungal high-throughput next-generation sequencing study performed on peatlands; it further provides a baseline for the investigation of the dynamics of the fungal community in the boreal peatlands.
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