Tree islands enhance biodiversity and functioning in oil palm landscapes.

In the United Nations Decade on Ecosystem Restoration1, large knowledge gaps persist on how to increase biodiversity and ecosystem functioning in cash crop-dominated tropical landscapes2. Here, we present findings from a large-scale, 5-year ecosystem restoration experiment in an oil palm landscape enriched with 52 tree islands, encompassing assessments of ten indicators of biodiversity and 19 indicators of ecosystem functioning. Overall, indicators of biodiversity and ecosystem functioning, as well as multidiversity and ecosystem multifunctionality, were higher in tree islands compared to conventionally managed oil palm. Larger tree islands led to larger gains in multidiversity through changes in vegetation structure. Furthermore, tree enrichment did not decrease landscape-scale oil palm yield. Our results demonstrate that enriching oil palm-dominated landscapes with tree islands is a promising ecological restoration strategy, yet should not replace the protection of remaining forests.

Balancing economic and ecological functions in smallholder and industrial oil palm plantations.

The expansion of the oil palm industry in Indonesia has improved livelihoods in rural communities, but comes at the cost of biodiversity and ecosystem degradation. Here, we investigated ways to balance ecological and economic outcomes of oil palm cultivation. We compared a wide range of production systems, including smallholder plantations, industrialized company estates, estates with improved agronomic management, and estates with native tree enrichment. Across all management types, we assessed multiple indicators of biodiversity, ecosystem functions, management, and landscape structure to identify factors that facilitate economic-ecological win-wins, using palm yields as measure of economic performance. Although, we found that yields in industrialized estates were, on average, twice as high as those in smallholder plantations, ecological indicators displayed substantial variability across systems, regardless of yield variations, highlighting potential for economic-ecological win-wins. Reducing management intensity (e.g., mechanical weeding instead of herbicide application) did not lower yields but improved ecological outcomes at moderate costs, making it a potential measure for balancing economic and ecological demands. Additionally, maintaining forest cover in the landscape generally enhanced local biodiversity and ecosystem functioning within plantations. Enriching plantations with native trees is also a promising strategy to increase ecological value without reducing productivity. Overall, we recommend closing yield gaps in smallholder cultivation through careful intensification, whereas conventional plantations could reduce management intensity without sacrificing yield. Our study highlights various pathways to reconcile the economics and ecology of palm oil production and identifies management practices for a more sustainable future of oil palm cultivation.

Ectomycorrhizal fungi of Douglas-fir retain newly assimilated carbon derived from neighboring European beech.

Ectomycorrhizal (ECM) fungi distribute tree-derived carbon (C) via belowground hyphal networks in forest ecosystems. Here, we asked the following: (1) Is C transferred belowground to a neighboring tree retained in fungal structures or transported within the recipient tree? (2) Is the overlap of ectomycorrhizal fungi in mycorrhizal networks related to the amount of belowground C transfer? We used potted sapling pairs of European beech (Fagus sylvatica) and North-American Douglas-fir (Pseudotsuga menziesii) for 13CO2 pulse-labeling. We compared 13C transfer from beech (donor) to either beech or Douglas-fir (recipient) and identified the ECM species. We measured the 13C enrichment in soil, plant tissues, and ECM fractions of fungal-containing parts and plant transport tissues. In recipients, only fungal-containing tissue of ectomycorrhizas was significantly enriched in 13C and not the plant tissue. Douglas-fir recipients shared on average one ECM species with donors and had a lower 13C enrichment than beech recipients, which shared on average three species with donors. Our results support that recently assimilated C transferred belowground is shared among fungi colonizing tree roots but not among trees. In mixed forests with beech and Douglas-fir, the links for C movement might be hampered due to low mycorrhizal overlap with consequences for soil C cycling.

Formation of mineral-associated organic matter in temperate soils is primarily controlled by mineral type and modified by land use and management intensity.

Formation of mineral-associated organic matter (MAOM) supports the accumulation and stabilization of carbon (C) in soil, and thus, is a key factor in the global C cycle. Little is known about the interplay of mineral type, land use and management intensity in MAOM formation, especially on subdecadal time scales. We exposed mineral containers with goethite or illite, the most abundant iron oxide and phyllosilicate clay in temperate soils, for 5 years in topsoils of 150 forest and 150 grassland sites in three regions across Germany. Results show that irrespective of land use and management intensity, more C accumulated on goethite than illite (on average 0.23 ± 0.10 and 0.06 ± 0.03 mg m-2 mineral surface respectively). Carbon accumulation across regions was consistently higher in coniferous forests than in deciduous forests and grasslands. Structural equation models further showed that thinning and harvesting reduced MAOM formation in forests. Formation of MAOM in grasslands was not affected by grazing. Fertilization had opposite effects on MAOM formation, with the positive effect being mediated by enhanced plant productivity and the negative effect by reduced plant species richness. This highlights the caveat of applying fertilizers as a strategy to increase soil C stocks in temperate grasslands. Overall, we demonstrate that the rate and amount of MAOM formation in soil is primarily driven by mineral type, and can be modulated by land use and management intensity even on subdecadal time scales. Our results suggest that temperate soils dominated by oxides have a higher capacity to accumulate and store C than those dominated by phyllosilicate clays, even under circumneutral pH conditions. Therefore, adopting land use and management practices that increase C inputs into oxide-rich soils that are under their capacity to store C may offer great potential to enhance near-term soil C sequestration.

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. In the present study, we investigated how variations in nitrogen (N) nutrition affected the metabolome and proteome of xylem sap and the growth of the xylem endophyte Brennaria salicis, and we also report transcriptional re-wiring of leaf defenses in poplar (Populus × canescens). We supplied poplars with high, intermediate or low concentrations of ammonium or nitrate. We identified 288 unique proteins in xylem sap. Approximately 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, whereas 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 124 metabolites, mainly from specialized metabolism of the groups of salicinoids, phenylpropanoids, phenolics, flavonoids, and benzoates. Their abundances increased with decreasing N, except coumarins. Brennaria salicis growth was reduced in nutrient-supplemented xylem sap of low- and high- NO3- -fed plants compared to that of NH4+ -fed plants. The drastic changes in xylem sap composition caused massive changes in the transcriptional landscape of leaves and recruited defenses related to systemic acquired and induced systemic resistance. Our study uncovers unexpected complexity and variability of xylem composition with consequences for plant defenses.

Predicting functions of putative fungal sesquiterpene synthase genes based on multiomics data analysis.

Sesquiterpenes (STs) are secondary metabolites, which mediate biotic interactions between different organisms. Predicting the species-specific ST repertoires can contribute to deciphering the language of communication between organisms of the same or different species. High biochemical plasticity and catalytic promiscuity of sesquiterpene synthases (STSs), however, challenge the homology-based prediction of the STS functions. Using integrated analyses of genomic, transcriptomic, volatilomic, and metabolomic data, we predict product profiles for 116 out of 146 putative STS genes identified in the genomes of 30 fungal species from different trophic groups. Our prediction method is based on the observation that STSs encoded by genes closely related phylogenetically are likely to share the initial enzymatic reactions of the ST biosynthesis pathways and, therefore, produce STs via the same reaction route. The classification by reaction routes allows to assign STs known to be emitted by a particular species to the putative STS genes from this species. Gene expression information helps to further specify these ST-to-STS assignments. Validation of the computational predictions of the STS functions using both in silico and experimental approaches shows that integrated multiomic analyses are able to correctly link cyclic STs of non-cadalane type to genes. In the process of the experimental validation, we characterized catalytic properties of several putative STS genes from the mycorrhizal fungus Laccaria bicolor. We show that the STSs encoded by the L.bicolor mycorrhiza-induced genes emit either nerolidol or α-cuprenene and α-cuparene, and discuss the possible roles of these STs in the mycorrhiza formation.

Ectomycorrhizal diversity, taxon-specific traits and root N uptake in temperate beech forests.

Roots of forest trees are colonized by a diverse spectrum of ectomycorrhizal (EM) fungal species differing in their nitrogen (N) acquisition abilities. Here, we hypothesized that root N gain is the result of EM fungal diversity or related to taxon-specific traits for N uptake. To test our hypotheses, we traced 15 N enrichment in fine roots, coarse roots and taxon-specific ectomycorrhizas in temperate beech forests in two regions and three seasons, feeding 1 mM NH4 NO3 labelled with either 15 NH4 + or 15 NO3 - . We morphotyped > 45 000 vital root tips and identified 51 of 53 detected EM species by sequencing. EM root tips exhibited strong, fungal taxon-specific variation in 15 N enrichment with higher NH4 + than NO3 - enrichment. The translocation of N into the upper parts of the root system increased with increasing EM fungal diversity. Across the growth season, influential EM species predicting root N gain were not identified, probably due to high temporal dynamics of the species composition of EM assemblages. Our results support that root N acquisition is related to EM fungal community-level traits and highlight the importance of EM diversity for tree N nutrition.

Re-examining the evidence for the mother tree hypothesis - resource sharing among trees via ectomycorrhizal networks.

Seminal scientific papers positing that mycorrhizal fungal networks can distribute carbon (C) among plants have stimulated a popular narrative that overstory trees, or 'mother trees', support the growth of seedlings in this way. This narrative has far-reaching implications for our understanding of forest ecology and has been controversial in the scientific community. We review the current understanding of ectomycorrhizal C metabolism and observations on forest regeneration that make the mother tree narrative debatable. We then re-examine data and conclusions from publications that underlie the mother tree hypothesis. Isotopic labeling methods are uniquely suited for studying element fluxes through ecosystems, but the complexity of mycorrhizal symbiosis, low detection limits, and small carbon discrimination in biological processes can cause researchers to make important inferences based on miniscule shifts in isotopic abundance, which can be misleading. We conclude that evidence of a significant net C transfer via common mycorrhizal networks that benefits the recipients is still lacking. Furthermore, a role for fungi as a C pipeline between trees is difficult to reconcile with any adaptive advantages for the fungi. Finally, the hypothesis is neither supported by boreal forest regeneration patterns nor consistent with the understanding of physiological mechanisms controlling mycorrhizal symbiosis.

Carbohydrate depletion in roots impedes phosphorus nutrition in young forest trees.

Nutrient imbalances cause the deterioration of tree health in European forests, but the underlying physiological mechanisms are unknown. Here, we investigated the consequences of decreasing root carbohydrate reserves for phosphorus (P) mobilisation and uptake by forest trees. In P-rich and P-poor beech (Fagus sylvatica) forests, naturally grown, young trees were girdled and used to determine root, ectomycorrhizal and microbial activities related to P mobilisation in the organic layer and mineral topsoil in comparison with those in nongirdled trees. After girdling, root carbohydrate reserves decreased. Root phosphoenolpyruvate carboxylase activities linking carbon and P metabolism increased. Root and ectomycorrhizal phosphatase activities and the abundances of bacterial genes catalysing major steps in P turnover increased, but soil enzymes involved in P mobilisation were unaffected. The physiological responses to girdling were stronger in P-poor than in P-rich forests. P uptake was decreased after girdling. The soluble and total P concentrations in roots were stable, but fine root biomass declined after girdling. Our results support that carbohydrate depletion results in reduced P uptake, enhanced internal P remobilisation and root biomass trade-off to compensate for the P shortage. As reductions in root biomass render trees more susceptible to drought, our results link tree deterioration with disturbances in the P supply as a consequence of decreased belowground carbohydrate allocation.

Wood Formation under Severe Drought Invokes Adjustment of the Hormonal and Transcriptional Landscape in Poplar.

Drought is a severe environmental stress that exerts negative effects on plant growth. In trees, drought leads to reduced secondary growth and altered wood anatomy. The mechanisms underlying wood stress adaptation are not well understood. Here, we investigated the physiological, anatomical, hormonal, and transcriptional responses of poplar to strong drought. Drought-stressed xylem was characterized by higher vessel frequencies, smaller vessel lumina, and thicker secondary fiber cell walls. These changes were accompanied by strong increases in abscisic acid (ABA) and antagonistic changes in salicylic acid in wood. Transcriptional evidence supported ABA biosynthesis and signaling in wood. Since ABA signaling activates the fiber-thickening factor NST1, we expected upregulation of the secondary cell wall (SCW) cascade under stress. By contrast, transcription factors and biosynthesis genes for SCW formation were down-regulated, whereas a small set of cellulose synthase-like genes and a huge array of genes involved in cell wall modification were up-regulated in drought-stressed wood. Therefore, we suggest that ABA signaling monitors normal SCW biosynthesis and that drought causes a switch from normal to "stress wood" formation recruiting a dedicated set of genes for cell wall biosynthesis and remodeling. This proposition implies that drought-induced changes in cell wall properties underlie regulatory mechanisms distinct from those of normal wood.

Ectomycorrhizal Fungal Strains Facilitate Cd2+ Enrichment in a Woody Hyperaccumulator under Co-Existing Stress of Cadmium and Salt.

Cadmium (Cd2+) pollution occurring in salt-affected soils has become an increasing environmental concern in the world. Fast-growing poplars have been widely utilized for phytoremediation of soil contaminating heavy metals (HMs). However, the woody Cd2+-hyperaccumulator, Populus × canescens, is relatively salt-sensitive and therefore cannot be directly used to remediate HMs from salt-affected soils. The aim of the present study was to testify whether colonization of P. × canescens with ectomycorrhizal (EM) fungi, a strategy known to enhance salt tolerance, provides an opportunity for affordable remediation of Cd2+-polluted saline soils. Ectomycorrhization with Paxillus involutus strains facilitated Cd2+ enrichment in P. × canescens upon CdCl2 exposures (50 µM, 30 min to 24 h). The fungus-stimulated Cd2+ in roots was significantly restricted by inhibitors of plasmalemma H+-ATPases and Ca2+-permeable channels (CaPCs), but stimulated by an activator of plasmalemma H+-ATPases. NaCl (100 mM) lowered the transient and steady-state Cd2+ influx in roots and fungal mycelia. Noteworthy, P. involutus colonization partly reverted the salt suppression of Cd2+ uptake in poplar roots. EM fungus colonization upregulated transcription of plasmalemma H+-ATPases (PcHA4, 8, 11) and annexins (PcANN1, 2, 4), which might mediate Cd2+ conductance through CaPCs. EM roots retained relatively highly expressed PcHAs and PcANNs, thus facilitating Cd2+ enrichment under co-occurring stress of cadmium and salinity. We conclude that ectomycorrhization of woody hyperaccumulator species such as poplar could improve phytoremediation of Cd2+ in salt-affected areas.

Soil and root nutrient chemistry structure root-associated fungal assemblages in temperate forests.

Root-associated fungi (RAF) link nutrient fluxes between soil and roots and thus play important roles in ecosystem functioning. To enhance our understanding of the factors that control RAF, we fitted statistical models to explain variation in RAF community structure using data from 150 temperate forest sites covering a broad range of environmental conditions and chemical root traits. We found that variation in RAF communities was related to both root traits (e.g., cations, carbohydrates, NO3 - ) and soil properties (pH, cations, moisture, C/N). The identified drivers were the combined result of distinct response patterns of fungal taxa (determined at the rank of orders) to biotic and abiotic factors. Our results support that RAF community variation is related to evolutionary adaptedness of fungal lineages and consequently, drivers of RAF communities are context-dependent.

Ectomycorrhizal fungi induce systemic resistance against insects on a nonmycorrhizal plant in a CERK1-dependent manner.

Below-ground microbes can induce systemic resistance against foliar pests and pathogens on diverse plant hosts. The prevalence of induced systemic resistance (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 fungus Laccaria bicolor on the nonmycorrhizal plant Arabidopsis thaliana. We used the cabbage looper Trichoplusia ni and bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Pto) as readouts for ISR on Arabidopsis. We found that root inoculation with L. bicolor triggered ISR against T. ni and induced systemic susceptibility (ISS) against the bacterial pathogen Pto. We found that L. bicolor-triggered ISR against T. ni was dependent on jasmonic acid signaling and salicylic acid biosynthesis and signaling. Heat-killed L. bicolor and chitin were sufficient to trigger ISR against T. ni and ISS against Pto. The chitin receptor CERK1 was necessary for L. bicolor-mediated effects on systemic immunity. Collectively our findings suggest that some ISR responses might not require intimate symbiotic association, but rather might be the result of root perception of conserved microbial signals.

Root isoprene formation alters lateral root development.

Isoprene is a C5 volatile organic compound, which can protect aboveground plant tissue from abiotic stress such as short-term high temperatures and accumulation of reactive oxygen species (ROS). Here, we uncover new roles for isoprene in the plant belowground tissues. By analysing Populus x canescens isoprene synthase (PcISPS) promoter reporter plants, we discovered PcISPS promoter activity in certain regions of the roots including the vascular tissue, the differentiation zone and the root cap. Treatment of roots with auxin or salt increased PcISPS promoter activity at these sites, especially in the developing lateral roots (LR). Transgenic, isoprene non-emitting poplar roots revealed an accumulation of O2- in the same root regions where PcISPS promoter activity was localized. Absence of isoprene emission, moreover, increased the formation of LRs. Inhibition of NAD(P)H oxidase activity suppressed LR development, suggesting the involvement of ROS in this process. The analysis of the fine root proteome revealed a constitutive shift in the amount of several redox balance, signalling and development related proteins, such as superoxide dismutase, various peroxidases and linoleate 9S-lipoxygenase, in isoprene non-emitting poplar roots. Together our results indicate for isoprene a ROS-related function, eventually co-regulating the plant-internal signalling network and development processes in root tissue.

Specialisation and diversity of multiple trophic groups are promoted by different forest features.

While forest management strongly influences biodiversity, it remains unclear how the structural and compositional changes caused by management affect different community dimensions (e.g. richness, specialisation, abundance or completeness) and how this differs between taxa. We assessed the effects of nine forest features (representing stand structure, heterogeneity and tree composition) on thirteen above- and belowground trophic groups of plants, animals, fungi and bacteria in 150 temperate forest plots differing in their management type. Canopy cover decreased light resources, which increased community specialisation but reduced overall diversity and abundance. Features increasing resource types and diversifying microhabitats (admixing of oaks and conifers) were important and mostly affected richness. Belowground groups responded differently to those aboveground and had weaker responses to most forest features. Our results show that we need to consider forest features rather than broad management types and highlight the importance of considering several groups and community dimensions to better inform conservation.

Competing Endogenous RNA Networks Underlying Anatomical and Physiological Characteristics of Poplar Wood in Acclimation to Low Nitrogen Availability.

Although poplar plantations are often established on nitrogen (N)-poor soil, the physiological and molecular mechanisms underlying wood properties of poplars in acclimation to low N availability remain largely unknown. To investigate wood properties of poplars in acclimation to low N, Populus � canescens saplings were exposed to either 50 (low N) or 500 (normal N) �M NH4NO3 for 2 months. Low N resulted in decreased xylem width and cell layers of the xylem (the number of cells counted along the ray parenchyma on the stem cross section), narrower lumina of vessels and fibers, greater thickness of double fiber walls (the walls between two adjacent fiber cells), more hemicellulose and lignin deposition, and reduced cellulose accumulation in poplar wood. Consistently, concentrations of gibberellins involved in cell size determination and the abundance of various metabolites including amino acids, carbohydrates and precursors for cell wall biosynthesis were decreased in low N-supplied wood. In line with these anatomical and physiological changes, a number of mRNAs, long noncoding RNAs (lncRNAs) and microRNAs (miRNAs) were significantly differentially expressed. Competing endogenous RNA regulatory networks were identified in the wood of low N-treated poplars. Overall, these results indicate that miRNAs-lncRNAs-mRNAs networks are involved in regulating wood properties and physiological processes of poplars in acclimation to low N availability.

Abscisic acid signalling mediates biomass trade-off and allocation in poplar.

Abscisic acid (ABA) is a well known stress hormone regulating drought adaptation of plants. Here, we hypothesised that genetic engineering of genes involved in ABA stress signalling and photoperiodic regulation affected drought resistance by trade-off with biomass production in perennial poplar trees. We grew Populus tremula × tremuloides wild-type (T89) and various transgenic lines (two transformation events of 35S::abi1-1, 35S::RCAR, RCAR:RNAi, 35S::ABI3, 35S::AREB3, 35S::FDL1, FDL1:RNAi, 35S::FDL2 and FDL2:RNAi) outdoors and exposed them to drought in the second growth period. After the winter, the surviving lines showed a huge variation in stomatal conductance, leaf size, whole-plant leaf area, tree height, stem diameter, and biomass. Whole-plant leaf area was a strong predictor for woody biomass production. The 35S::AREB3 lines were compromised in biomass production under well irrigated conditions compared with wild-type poplars but were resilient to drought. ABA signalling regulated FDL1 and FDL2 expression under stress. Poplar lines overexpressing FDL1 or FDL2 were drought-sensitive; they shed leaves and lost root biomass, whereas the FDL RNAi lines showed higher biomass allocation to roots under drought. These results assign a new function in drought acclimation to FDL genes aside from photoperiodic regulation. Our results imply a critical role for ABA-mediated processes in balancing biomass production and climate adaptation.

Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net.

Salt stress is an important environmental cue impeding poplar nitrogen nutrition. Here, we characterized the impact of salinity on proton-driven nitrate fluxes in ectomycorrhizal roots and the importance of a Hartig net for nitrate uptake. We employed two Paxillus involutus strains for root colonization: MAJ, which forms typical ectomycorrhizal structures (mantle and Hartig net), and NAU, colonizing roots with a thin, loose hyphal sheath. Fungus-colonized and noncolonized Populus × canescens were exposed to sodium chloride and used to measure root surface pH, nitrate (NO3- ) flux and transcription of NO3- transporters (NRTs; PcNRT1.1, -1.2, -2.1), and plasmalemma proton ATPases (HAs; PcHA4, -8, -11). Paxillus colonization enhanced root NO3- uptake, decreased surface pH, and stimulated NRTs and HA4 of the host regardless the presence or absence of a Hartig net. Under salt stress, noncolonized roots exhibited strong net NO3- efflux, whereas beneficial effects of fungal colonization on surface pH and HAs prevented NO3- loss. Inhibition of HAs abolished NO3- influx under all conditions. We found that stimulation of HAs was crucial for the beneficial influence of ectomycorrhiza on NO3- uptake, whereas the presence of a Hartig net was not required for improved NO3- translocation. Mycorrhizas may contribute to host adaptation to salt-affected environments by keeping up NO3- nutrition.

Assembly processes of trophic guilds in the root mycobiome of temperate forests.

Root-associated mycobiomes (RAMs) link plant and soil ecological processes, thereby supporting ecosystem functions. Understanding the forces that govern the assembly of RAMs is key to sustainable ecosystem management. Here, we dissected RAMs according to functional guilds and combined phylogenetic and multivariate analyses to distinguish and quantify the forces driving RAM assembly processes. Across large biogeographic scales (>1,000 km) in temperate forests (>100 plots), RAMs were taxonomically highly distinct but composed of a stable trophic structure encompassing symbiotrophic, ectomycorrhizal (55%), saprotrophic (7%), endotrophic (3%) and pathotrophic fungi (<1%). Taxonomic community composition of RAMs is explained by abiotic factors, forest management intensity, dominant tree family (Fagaceae, Pinaceae) and root resource traits. Local RAM assemblies are phylogenetically clustered, indicating stronger habitat filtering on roots in dry, acid soils and in conifer stands than in other forest types. The local assembly of ectomycorrhizal communities is driven by forest management intensity. At larger scales, root resource traits and soil pH shift the assembly process of ectomycorrhizal fungi from deterministic to neutral. Neutral or weak deterministic assembly processes are prevalent in saprotrophic and endophytic guilds. The remarkable consistency of the trophic composition of the RAMs suggests that temperate forests attract fungal assemblages that afford functional resilience under the current range of climatic and edaphic conditions. At local scales, the filtering processes that structure symbiotrophic assemblies can be influenced by forest management and tree selection, but at larger scales, environmental cues and host resource traits are the most prevalent forces.

Mycorrhiza-Triggered Transcriptomic and Metabolomic Networks Impinge on Herbivore Fitness.

Symbioses between plants and mycorrhizal fungi are ubiquitous in ecosystems and strengthen the plants' defense against aboveground herbivores. Here, we studied the underlying regulatory networks and biochemical mechanisms in leaves induced by ectomycorrhizae that modify herbivore interactions. Feeding damage and oviposition by the widespread poplar leaf beetle Chrysomela populi were reduced on the ectomycorrhizal hybrid poplar Populus × canescens Integration of transcriptomics, metabolomics, and volatile emission patterns via mass difference networks demonstrated changes in nitrogen allocation in the leaves of mycorrhizal poplars, down-regulation of phenolic pathways, and up-regulation of defensive systems, including protease inhibitors, chitinases, and aldoxime biosynthesis. Ectomycorrhizae had a systemic influence on jasmonate-related signaling transcripts. Our results suggest that ectomycorrhizae prime wounding responses and shift resources from constitutive phenol-based to specialized protective compounds. Consequently, symbiosis with ectomycorrhizal fungi enabled poplars to respond to leaf beetle feeding with a more effective arsenal of defense mechanisms compared with nonmycorrhizal poplars, thus demonstrating the importance of belowground plant-microbe associations in mitigating aboveground biotic stress.