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Polle, A.

Publications and source records attributed to Polle, A..

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Forest tree species composition and abiotic site conditions drive soil fungal communities and functional groups

Soil fungi, especially the functional guilds of saprotrophic and mycorrhizal fungi, play a central role in ecosystem processes by degrading litter, mining for mineral nutrients and linking above- and belowground nutrient fluxes. Fungal community structures are influenced by abiotic habitat filters and management decisions such as tree species selection. Yet, the implications of the enrichment of temperate forests consisting of tree species in their natural range with non-native tree species on soil fungal diversity and their functional groups are unknown. Here, we studied fungal communities in 40 plots located in two regions differing in site conditions (nutrient content and soil moisture) in forests composed of European beech, Norway spruce and Douglas-fir (non-native) and mixtures of beech with either spruce or Douglas-fir. We hypothesized that fungal community structures are driven by soil resources and tree species composition, generally resulting in higher fungal diversity in mixed than in mono-specific forests. We further hypothesized that Douglas-fir has a negative effect on ectomycorrhizal fungal species richness compared to native species, whereas saprotrophic fungal richness is unaffected. We found strong separation of fungal communities between nutrient-rich and nutrient-poor sites and taxonomic divergence between beech and conifer fungal communities and an intermediate pattern in mixed forests. Mycorrhizal species richness did not vary with forest type, but the relative abundance of mycorrhizal species was lower in Douglas-fir and in mixed beech-Douglas-fir forests than in spruce or beech- spruce mixture. Conifer forests contained higher relative abundances of saprotrophic fungi than mono-specific beech forests. Among 16 abundant fungal orders in soil, two containing saprotrophic fungi (Tremellales, Hymenochaetales) were enriched in conifer forests, regardless of site conditions and tree species mixture. The other fungal orders, including those dominated by mycorrhizal fungi (Russulales, Boletales, Atheliales, Cantharellales) showed variable patterns depending on site conditions and tree species. In conclusion, Douglas-fir mono-specific or mixed forests show no loss of fungal species richness, but a shift in functional composition towards saprotrophic fungi.

ecology↗

Transcriptional Landscape of Ectomycorrhizal Fungi and Their Host Provide Insight into N Uptake from Forest Soil

Mineral nitrogen (N) is a major nutrient showing strong fluctuations in the environment due to anthropogenic activities. Acquisition and translocation of N to forest trees is achieved by highly diverse ectomycorrhizal fungi (EMF) living in symbioses with their host roots. Here, we examined colonized root tips to characterize the entire root-associated fungal community by DNA metabarcoding-Illumina sequencing of the fungal ITS2 molecular marker and used RNA sequencing to target metabolically active fungi and the plant transcriptome after N application. The study was conducted with beech (Fagus sylvatica L), a dominant tree species in central Europe, grown in native forest soil. We demonstrate strong enrichment of 15N from nitrate or ammonium in the ectomycorrhizal roots by stable isotope labeling. The relative abundance of the EMF members in the fungal community was correlated with their transcriptional abundances. The fungal metatranscriptome covered KEGG and KOG categories similar to model fungi and did not reveal significant changes related to N metabolization but species-specific transcription patterns, supporting trait stability. In contrast to the resistance of the fungal metatranscriptome, the transcriptome of the host exhibited dedicated nitrate- or ammonium-responsive changes with upregulation of transporters and enzymes required for nitrate reduction and drastic enhancement of glutamine synthetase transcript levels, indicating channeling of ammonium into the pathway for plant protein biosynthesis. Our results support that self-composed fungal communities associated with tree roots buffer nutritional signals in their own metabolism but do not shield plants from high environmental N. IMPORTANCEAlthough EMF are well known for their role in supporting tree N nutrition, the molecular mechanisms underlying N flux from the soil solution into the host through the ectomycorrhizal pathway remain widely unknown. Furthermore, ammonium and nitrate availability in the soil solution is subject to constant oscillations that create a dynamic environment for the tree roots and associated microbes during N acquisition. Therefore, it is important to understand how root-associated mycobiomes and the tree roots handle these fluctuations. We studied the response of the symbiotic partners by screening their transcriptomes after a sudden environmental flux of nitrate or ammonium. We show that the fungi and the host respond asynchronously, with the fungi displaying resistance to increased nitrate or ammonium, and the host dynamically metabolizing the supplied N sources. This study provides insights into the molecular mechanisms of the symbiotic partners operating under N enrichment in a multidimensional symbiotic system.

microbiology↗

Multi-omics analysis of xylem sap uncovers dynamic modulation of poplar defenses by ammonium and nitrate

Xylem sap is the major transport route for nutrients from roots to shoots. Here, we investigated how variations in nitrogen (N) nutrition affected the metabolome and proteome of xylem sap, growth of the xylem endophyte Brennaria salicis and report transcriptional re-wiring of leaf defenses in poplar (Populus x canescens). We supplied poplars with high, intermediate or low concentrations of ammonium or nitrate. We identified 288 unique proteins in xylem sap. About 85% of the xylem sap proteins were shared among ammonium- and nitrate-supplied plants. The number of proteins increased with increasing N supply but the major functional categories (catabolic processes, cell wall-related enzymes, defense) were unaffected. Ammonium nutrition caused higher abundances of amino acids and carbohydrates, while nitrate caused higher malate levels in xylem sap. Pipecolic acid and N-hydroxy-pipecolic acid increased whereas salicylic acid and jasmonoyl-isoleucine decreased with increasing N nutrition. Untargeted metabolome analyses revealed 2179 features in xylem sap, of which 863 were differentially affected by N treatments. We identified 122 metabolites, mainly from specialized metabolism of the groups of salicinoids, phenylpropanoids, phenolics, flavonoids, and benzoates. Their abundances increased with decreasing N. Endophyte growth was stimulated in xylem sap of high N- and suppressed in that of low N-fed plants. The drastic changes in xylem sap composition caused massive changes in the transcriptional landscape of leaves and recruited defense pathways against leaf feeding insects and biotrophic fungi, mainly under low nitrate. Our study uncovers unexpected complexity and variability of xylem composition with consequences for plant defenses. Significance statementThis study reports the largest, currently available plant xylem sap proteome and metabolome databases and highlights novel discoveries of specialized metabolites and phytohormones in the xylem sap. This is the first multi-omics study linking differences in nitrogen supply with changes xylem sap composition, endophyte growth and transcriptional defenses in leaves.

plant biology↗

Impact of nitrogen and phosphorus addition on resident soil and root mycobiomes in beech forests

In forest soils, the pools of N and P available for microbes and plants are strongly dependent on soil properties. Here, we conducted a P and N fertilization experiment to disentangle the effects of nutrient availability on soil-residing, root-associated and ectomycorrhizal fungi in beech (Fagus sylvativa) forests differing in P availability. We tested the hypothesis that in P-poor forests, P fertilization leads to enhanced fungal diversity in soil and roots, resulting in enhanced P nutrition of beech and that N fertilization aggravates P shortage, shifting the fungal communities towards nitrophilic species. In response to fertilizer treatments (1x 50 kg ha-1 P, 5x 30 kg ha-1 N within 2 years), the labile P fractions increased in soil and roots, regardless of plant-available P in soil. Root total P decreased in response to N fertilization and root total P increased at the low P site in response to P addition. The relative abundances of ectomycorrhizal fungi, but not their species richness, increased in response to P or N addition in comparison with that of saprotrophic fungi. While some fungal orders (Trechisporales, Atheliales, Cantharellales) were moderately decreased in response to fertilizer treatments, Boletales increased in response to P and Russulaes to N addition. N or P fertilization resulted in functional trade-off, shifting away from saprotrophic towards symbiotrophic potential. Our results suggest that chronic exposure of forest ecosystems to increased nutrient inputs may overcome the resistance of the resident mycobiome structures resulting in nutritional imbalance and loss of forest ecosystem services.

ecology↗

Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Below-ground microbes can induce systemic resistance (ISR) against foliar pests and pathogens on diverse plant hosts. The prevalence of ISR among plant-microbe-pest systems raises the question of host specificity in microbial induction of ISR. To test whether ISR is limited by plant host range, we tested the ISR-inducing ectomycorrhizal (ECM) fungus Laccaria bicolor on the non-mycorrhizal plant Arabidopsis. We found that root inoculation with L. bicolor triggered ISR against the insect herbivore Trichoplusia ni and induced systemic susceptibility (ISS) against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Pto). We found that L. bicolor-triggered ISR against T. ni was dependent on jasmonic acid (JA) signaling and salicylic acid (SA) biosynthesis and signaling. We found that heat killed L. bicolor and chitin are sufficient to trigger ISR against T. ni and ISS against Pto and that the chitin receptor CERK1 is necessary for L. bicolor-mediated effects on systemic immunity. Collectively our findings suggest that some ISR responses might not require intimate co-evolution of host and microbe, but rather might be the result of root perception of conserved microbial signals.

plant biology↗