Soils contain a multitude of fungi with vastly divergent lifestyles ranging from saprotrophic to mutualistic and pathogenic. The recent release of many fungal genomes has led to comparative studies ...that consider the extent to which these lifestyles are encoded in the genome. The genomes of the symbiotic fungi Laccaria bicolor and Tuber melanosporum are proving especially useful in characterizing the genetic foundation of mutualistic symbiosis. New insights gleaned from these genomes, as compared to their saprotrophic and pathogenic cousins, have helped to redefine and shape our understanding of the nature of the symbiotic lifestyle. Here we detail the current state of research into this complex relationship and discuss avenues for future exploration.
Mycorrhiza helper bacteria (MHB) are known to increase host root colonization by mycorrhizal fungi but the molecular mechanisms and potential tripartite interactions are poorly understood. Through an ...effort to study Populus microbiome, we isolated 21 Pseudomonas strains from native Populus deltoides roots. These bacterial isolates were characterized and screened for MHB effectiveness on the Populus-Laccaria system. Two additional Pseudomonas strains (i.e., Pf-5 and BBc6R8) from existing collections were included for comparative purposes. We analyzed the effect of co-cultivation of these 23 individual Pseudomonas strains on Laccaria bicolor "S238N" growth rate, mycelial architecture and transcriptional changes. Nineteen of the 23 Pseudomonas strains tested had positive effects on L. bicolor S238N growth, as well as on mycelial architecture, with strains GM41 and GM18 having the most significant effect. Four of seven L. bicolor reporter genes, Tra1, Tectonin2, Gcn5, and Cipc1, thought to be regulated during the interaction with MHB strain BBc6R8, were induced or repressed, while interacting with Pseudomonas strains GM17, GM33, GM41, GM48, Pf-5, and BBc6R8. Strain GM41 promoted the highest roots colonization across three Populus species but most notably in P. deltoides, which is otherwise poorly colonized by L. bicolor. Here we report novel MHB strains isolated from native Populus that improve L. bicolor root colonization on Populus. This tripartite relationship could be exploited for Populus species/genotypes nursery production as a means of improving establishment and survival in marginal lands.
Plant growth is often limited by highly activated aluminum (Al) and low available phosphorus (P) in acidic soil. Ectomycorrhizal (ECM) fungi can improve their host plants' Al tolerance by increasing ...P availability while decreasing Al activity
or in hydroponic or sand culture systems. However, the effect of ECM fungi on inorganic P (IP) and labile Al in acidic soil in the field, particularly in conjunction with Al treatment, remains poorly understood. The present study aimed to determine the influence of ECM fungal association on the mobilization of IP and labile Al in rhizosphere soil of host plants grown in the field with external Al treatment and the underlying nutritional mechanism in plant Al tolerance. To do so, 4-week-old
seedlings were inoculated with three ECM isolates (
270,
S238A, and
S238N) and grown in a Haplic Alisol field with or without Al treatment for 12 weeks. Results showed that
association enhanced the available P depletion and facilitated the mobilization of IP and labile Al, in turn improving the capacity of host plant to use Al-bound P, Ca-bound P, and occluded P, particularly when
seedlings were inoculated with
S238A. Inoculation with
isolates also enhanced the solubility of labile Al and facilitated the conversion of acid-soluble Al into exchangeable Al. Our findings suggested that ECM inoculation could enhance plant Al tolerance in the field by mobilizing IP to improve the P bioavailability but not by decreasing Al activity.
Here, we reveal the underlying nutritional mechanism in plant Al tolerance conferred by ectomycorrhizal (ECM)-fungus inoculation in the field and report the screening of a promising ECM isolate to assist phytoremediation and afforestation using
in acidic soil in southern China. This study advances our understanding of the contribution of ECM fungi to plant-ECM-fungus symbiosis and highlights the vital role of ECM-fungus inoculation in plant Al tolerance. In addition, the results described in the present study confirm the importance of carrying out studies in the field rather than only
studies. Our findings strengthen our understanding of the role of ECM-fungus association in detecting, utilizing, and transporting unavailable nutrients in the soil to enhance host plant growth and adaptability in response to adverse habitats.
Summary
Soil‐borne microbes can establish compatible relationships with host plants, providing a large variety of nutritive and protective compounds in exchange for photosynthesized sugars. However, ...the molecular mechanisms mediating the establishment of these beneficial relationships remain unclear. Our previous genetic mapping and whole‐genome resequencing studies identified a gene deletion event of a Populus trichocarpa lectin receptor‐like kinase gene PtLecRLK1 in Populus deltoides that was associated with poor‐root colonization by the ectomycorrhizal fungus Laccaria bicolor. By introducing PtLecRLK1 into a perennial grass known to be a non‐host of L. bicolor, switchgrass (Panicum virgatum L.), we found that L. bicolor colonizes ZmUbipro‐PtLecRLK1 transgenic switchgrass roots, which illustrates that the introduction of PtLecRLK1 has the potential to convert a non‐host to a host of L. bicolor. Furthermore, transcriptomic and proteomic analyses on inoculated‐transgenic switchgrass roots revealed genes/proteins overrepresented in the compatible interaction and underrepresented in the pathogenic defence pathway, consistent with the view that pathogenic defence response is down‐regulated during compatible interaction. Metabolomic profiling revealed that root colonization in the transgenic switchgrass was associated with an increase in N‐containing metabolites and a decrease in organic acids, sugars, and aromatic hydroxycinnamate conjugates, which are often seen in the early steps of establishing compatible interactions. These studies illustrate that PtLecRLK1 is able to render a plant susceptible to colonization by the ectomycorrhizal fungus L. bicolor and shed light on engineering mycorrhizal symbiosis into a non‐host to enhance plant productivity and fitness on marginal lands.
The coordinated transcriptomic responses of both mutualistic ectomycorrhizal (ECM) fungi and their hosts during the establishment of symbiosis are not well-understood. This study characterizes the ...transcriptomic alterations of the ECM fungus Laccaria bicolor during different colonization stages on two hosts (Populus trichocarpa and Pseudotsuga menziesii) and compares this to the transcriptomic variations of P. trichocarpa across the same time-points. A large number of L. bicolor genes (≥ 8,000) were significantly regulated at the transcriptional level in at least one stage of colonization. From our data, we identify 1,249 genes that we hypothesize is the 'core' gene regulon necessary for the mutualistic interaction between L. bicolor and its host plants. We further identify a group of 1,210 genes that are regulated in a host-specific manner. This variable regulon encodes a number of genes coding for proteases and xenobiotic efflux transporters that we hypothesize act to counter chemical-based defenses simultaneously activated at the transcriptomic level in P. trichocarpa. The transcriptional response of the host plant P. trichocarpa consisted of differential waves of gene regulation related to signaling perception and transduction, defense response, and the induction of nutrient transfer in P. trichocarpa tissues. This study, therefore, gives fresh insight into the shifting transcriptomic landscape in both the colonizing fungus and its host and the different strategies employed by both partners in orchestrating a mutualistic interaction.
Effects of biodiversity on productivity are more likely to be expressed when there is greater potential for niche complementarity. In soil, chemically complex pools of nutrient resources should ...provide more opportunities for niche complementarity than chemically simple pools. Ectomycorrhizal (ECM) fungal genotypes can exhibit substantial variation in nutrient acquisition traits and are key components of soil biodiversity. Here, we tested the hypothesis that increasing the chemical complexity and forms of soil nutrients would enhance the effects of intraspecific ECM diversity on host plant and fungal productivity. In pure culture, we found substantial variation in growth of strains of the ECM fungus
on a range of inorganic and organic forms of nutrients. Subsequent experiments examined the effects of intraspecific identity and richness using Scots pine (
) seedlings colonized with different strains of
growing on substrates supplemented with either inorganic or organic forms of nitrogen and phosphorus. Intraspecific identity effects on plant productivity were only found under the inorganic nutrient amendment, whereas intraspecific identity affected fungal productivity to a similar extent under both nutrient treatments. Overall, there were no significant effects of intraspecific richness on plant and fungal productivity. Our findings suggest soil nutrient composition does not interact strongly with ECM intraspecific richness, at least under experimental conditions where mineral nutrients were not limiting. Under these conditions, intraspecific identity of ECM fungi becomes more important than richness in modulating plant and fungal performance.
Plants interact simultaneously with multiple organisms, including ectomycorrhizal (EM) fungal symbionts which benefit plants by facilitating resource acquisition. Yet, their role in induced plant ...defenses that rely on the allocation of plant resources has received little attention. We investigated whether EM fungi can affect the induction of defense-related monoterpenes in greenhouse-grown lodgepole pine (Pinus contorta var. latifolia) seedlings, and whether such effects differed between EM fungal species occurring alone or in combination. Fungal interactions on growth media were also assessed to complement the greenhouse study. Our study revealed that the production of certain monoterpenes is influenced by the fungal species colonizing pine roots. Furthermore, pine seedlings did not necessarily benefit from having associations with multiple EM fungi, as we found contrasting effects of single vs. multiple species of fungi on induced monoterpene responses. Finally, monoterpene responses were altered when early-colonizing species inhibited the colonization or development of later-arriving species. We conclude that the presence of EM fungi can impact host susceptibility to insect and pathogen attack, suggesting that seedlings establishing in areas lacking fungi that promote the induction of tree defense chemicals may suffer from increased susceptibility to future pest damage.
Currently ectomycorrhizal research suffers from a lack of molecular tools specifically adapted to study gene expression in fungal symbionts. Considering that, we designed pReNuK, a cloning vector for ...transcriptional promoter studies in the ectomycorrhizal basidiomycete Laccaria bicolor. The pReNuK vector offers the use of a nuclear localizing and chromatin incorporating histone H2B-mCherry fluorescent reporter protein and it is specifically optimized for efficient transgene expression in Laccaria. Moreover, pReNuK is designed to work in concert with Agrobacterium-mediated transformation under hygromycin B resistance selection. The functionality of the pReNuK reporter system was tested with the constitutive Laccaria glyceraldehyde 3-phosphate dehydrogenase gene promoter and further validated with the nitrogen source regulated nitrate reductase gene promoter. The expression of the nucleus-directed H2B-mCherry reporter is highly stable in time. Moreover, the transformation of Laccaria with pReNuK and the expression of the reporter do not have negative effects on the growth of the fungus. The pReNuK offers a novel tool for studying in vivo gene expression regulation in Laccaria, the leading fungal model for ectomycorrhizal research.
•Ectomycorrhizal research currently suffers from lack of molecular tools optimized for studies of the fungal partners•The pReNuK system presented here offers a nucleus-directed histone H2B-mCherry reporter optimized for studying promoter regulation in ECM model fungus Laccaria bicolor.•This fluorescent reporter is simple to detect, its expression is highly stable and non-toxic to fungal cells.•pReNuK is expected to be functional not only in Laccaria but also in other homobasidiomycetes
Within boreal and temperate forest ecosystems, the majority of trees and shrubs form beneficial relationships with mutualistic ectomycorrhizal (ECM) fungi that support plant health through increased ...access to nutrients as well as aiding in stress and pest tolerance. The intimate interaction between fungal hyphae and plant roots results in a new symbiotic "organ" called the ECM root tip. Little is understood concerning the metabolic reprogramming that favors the formation of this hybrid tissue in compatible interactions and what prevents the formation of ECM root tips in incompatible interactions. We show here that the metabolic changes during favorable colonization between the ECM fungus Laccaria bicolor and its compatible host, Populus trichocarpa, are characterized by shifts in aromatic acid, organic acid, and fatty acid metabolism. We demonstrate that this extensive metabolic reprogramming is repressed in incompatible interactions and that more defensive compounds are produced or retained. We also demonstrate that L. bicolor can metabolize a number of secreted defensive compounds and that the degradation of some of these compounds produces immune response metabolites (e.g., salicylic acid from salicin). Therefore, our results suggest that the metabolic responsiveness of plant roots to L. bicolor is a determinant factor in fungus-host interactions.
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