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The mechanisms underlying interspecific variation in conspecific negative density dependence (CNDD) are poorly understood. Using a multilevel modeling approach, we combined long-term seedling demographic data from a subtropical forest plot with soil fungal community data by means of DNA sequencing to address the feedback of various guilds of soil fungi on the density dependence of trees. We show that mycorrhizal type mediates tree neighborhood interactions at the community level, and much of the interspecific variation in CNDD is explained by how tree species differ in their fungal density accumulation rates as they grow. Species with higher accumulation rates of pathogenic fungi suffered more from CNDD, whereas species with lower CNDD had higher accumulation rates of ectomycorrhizal fungi, suggesting that mutualistic and pathogenic fungi play important but opposing roles.

Photosynthesis by leaves and acquisition of water and minerals by roots are required for plant growth, which is a key component of many ecosystem functions. Although the role of leaf functional traits in photosynthesis is generally well understood, the relationship of root functional traits to nutrient uptake is not. In particular, predictions of nutrient acquisition strategies from specific root traits are often vague. Roots of nearly all plants cooperate with mycorrhizal fungi in nutrient acquisition. Most tree species form symbioses with either arbuscular mycorrhizal (AM) or ectomycorrhizal (EM) fungi. Nutrients are distributed heterogeneously in the soil, and nutrient-rich “hotspots” can be a key source for plants. Thus, predicting the foraging strategies that enable mycorrhizal root systems to exploit these hotspots can be critical to the understanding of plant nutrition and ecosystem carbon and nutrient cycling. Here, we show that in 13 sympatric temperate tree species, when nutrient availability is patchy, thinner root species alter their foraging to exploit patches, whereas thicker root species do not. Moreover, there appear to be two distinct pathways by which thinner root tree species enhance foraging in nutrient-rich patches: AM trees produce more roots, whereas EM trees produce more mycorrhizal fungal hyphae. Our results indicate that strategies of nutrient foraging are complementary among tree species with contrasting mycorrhiza types and root morphologies, and that predictable relationships between below-ground traits and nutrient acquisition emerge only when both roots and mycorrhizal fungi are considered together.

Background Soil microbiomes play an important role in the services and functioning of terrestrial ecosystems. However, little is known of their vertical responses to restoration process and their contributions to soil nutrient cycling in the subsurface profiles. Here, we investigated the community assembly of soil bacteria, archaea, and fungi along vertical (i.e., soil depths of 0–300 cm) and horizontal (i.e., distance from trees of 30–90 cm) profiles in a chronosequence of reforestation sites that represent over 30 years of restoration. Results In the superficial layers (0–80 cm), bacterial and fungal diversity decreased, whereas archaeal diversity increased with increasing soil depth. As reforestation proceeded over time, the vertical spatial variation in bacterial communities decreased, while that in archaeal and fungal communities increased. Vertical distributions of the soil microbiomes were more related to the variation in soil properties, while their horizontal distributions may be driven by a gradient effect of roots extending from the tree. Bacterial and archaeal beta-diversity were strongly related to multi-nutrient cycling in the soil, respectively, playing major roles in deep and superficial layers. Conclusions Taken together, these results reveal a new perspective on the vertical and horizontal spatial variation in soil microbiomes at the fine scale of single trees. Distinct response patterns underpinned the contributions of soil bacteria, archaea, and fungi as a function of subsurface nutrient cycling during the reforestation of ex-arable land.

The identification of plant functional traits that can be linked to ecosystem processes is of wide interest, especially for predicting vegetational responses to climate change. Root diameter of the finest absorptive roots may be one plant trait that has wide significance. Do species with relatively thick absorptive roots forage in nutrient-rich patches differently from species with relatively fine absorptive roots? We measured traits related to nutrient foraging (root morphology and architecture, root proliferation, and mycorrhizal colonization) across six coexisting arbuscular mycorrhizal (AM) temperate tree species with and without nutrient addition. Root traits such as root diameter and specific root length were highly correlated with root branching intensity, with thin-root species having higher branching intensity than thick-root species. In both fertilized and unfertilized soil, species with thin absorptive roots and high branching intensity showed much greater root length and mass proliferation but lower mycorrhizal colonization than species with thick absorptive roots. Across all species, fertilization led to increased root proliferation and reduced mycorrhizal colonization. These results suggest that thin-root species forage more by root proliferation, whereas thick-root species forage more by mycorrhizal fungi. In mineral nutrient-rich patches, AM trees seem to forage more by proliferating roots than by mycorrhizal fungi.

Most trees form symbioses with ectomycorrhizal fungi (EMF) which influence access to growth-limiting soil resources. Mesocosm experiments repeatedly show that EMF species differentially affect plant development, yet whether these effects ripple up to influence the growth of entire forests remains unknown. Here we tested the effects of EMF composition and functional genes relative to variation in well-known drivers of tree growth by combining paired molecular EMF surveys with high-resolution forest inventory data across 15 European countries. We show that EMF composition was linked to a three-fold difference in tree growth rate even when controlling for the primary abiotic drivers of tree growth. Fast tree growth was associated with EMF communities harboring high inorganic but low organic nitrogen acquisition gene proportions and EMF which form contact versus medium-distance fringe exploration types. These findings suggest that EMF composition is a strong bio-indicator of underlying drivers of tree growth and/or that variation of forest EMF communities causes differences in tree growth. While it may be too early to assign causality or directionality, our study is one of the first to link fine-scale variation within a key component of the forest microbiome to ecosystem functioning at a continental scale.

Feedback with soil biota is an important determinant of terrestrial plant diversity. However, the factors regulating plant-soil feedback, which varies from positive to negative among plant species, remain uncertain. In a large-scale study involving 55 species and 550 populations of North American trees, the type of mycorrhizal association explained much of the variation in plant-soil feedbacks. In soil collected beneath conspecifics, arbuscular mycorrhizal trees experienced negative feedback, whereas ectomycorrhizal trees displayed positive feedback. Additionally, arbuscular mycorrhizal trees exhibited strong conspecific inhibition at multiple spatial scales, whereas ectomycorrhizal trees exhibited conspecific facilitation locally and less severe conspecific inhibition regionally. These results suggest that mycorrhizal type, through effects on plant-soil feedbacks, could be an important contributor to population regulation and community structure in temperate forests.

Canker caused by ascomycetous Valsa species are among the most destructive diseases of woody plants worldwide. These pathogens are distinct from other pathogens because they only effectively attack tree bark in the field. To unravel the potential adaptation mechanism of bark colonization, we examined the genomes of Valsa mali and Valsa pyri that preferentially infect apple and pear, respectively. We reported the 44.7 and 35.7 Mb genomes of V. mali and V. pyri, respectively. We also identified the potential genomic determinants of wood colonization by comparing them with related cereal pathogens. Both genomes encode a plethora of pathogenicity‐related genes involved in plant cell wall degradation and secondary metabolite biosynthesis. In order to adapt to the nutrient limitation and low pH environment in bark, they seem to employ membrane transporters associated with nitrogen uptake and secrete proteases predominantly with acidic pH optima. Remarkably, both Valsa genomes are especially suited for pectin decomposition, but are limited in lignocellulose and cutin degradation. Besides many similarities, the two genomes show distinct variations in many secondary metabolism gene clusters. Our results show a potential adaptation of Valsa canker pathogens to colonize woody bark. Secondary metabolism gene clusters are probably responsible for this host specificity.

The mechanisms regulating community composition and local dominance of trees in species-rich forests are poorly resolved, but the importance of interactions with soil microbes is increasingly acknowledged. Here, we show that tree seedlings that interact via root-associated fungal hyphae with soils beneath neighbouring adult trees grow faster and have greater survival than seedlings that are isolated from external fungal mycelia, but these effects are observed for species possessing ectomycorrhizas (ECM) and not arbuscular mycorrhizal (AM) fungi. Moreover, survival of naturally-regenerating AM seedlings over ten years is negatively related to the density of surrounding conspecific plants, while survival of ECM tree seedlings displays positive density dependence over this interval, and AM seedling roots contain greater abundance of pathogenic fungi than roots of ECM seedlings. Our findings show that neighbourhood interactions mediated by beneficial and pathogenic soil fungi regulate plant demography and community structure in hyperdiverse forests. Associations with mycorrhizal fungi can affect the outcome of plant competition in complex ways. Here the authors use a decade-long field survey and two hyphal exclusion experiments to reveal a critical role of underground fungal networks in facilitating seedling growth and fitness of ectomycorrhizal plants but not arbuscular mycorrhizal plants.

Outbreaks of the Eurasian spruce bark beetle ( Ips typographus ) have decimated millions of hectares of conifer forests in Europe in recent years. The ability of these 4.0 to 5.5 mm long insects to kill mature trees over a short period has been sometimes ascribed to two main factors: (1) mass attacks on the host tree to overcome tree defenses and (2) the presence of fungal symbionts that support successful beetle development in the tree. While the role of pheromones in coordinating mass attacks has been well studied, the role of chemical communication in maintaining the fungal symbiosis is poorly understood. Previous evidence indicates that I . typographus can distinguish fungal symbionts of the genera Grosmannia , Endoconidiophora , and Ophiostoma by their de novo synthesized volatile compounds. Here, we hypothesize that the fungal symbionts of this bark beetle species metabolize spruce resin monoterpenes of the beetle’s host tree, Norway spruce ( Picea abies ), and that the volatile products are used as cues by beetles for locating breeding sites with beneficial symbionts. We show that Grosmannia penicillata and other fungal symbionts alter the profile of spruce bark volatiles by converting the major monoterpenes into an attractive blend of oxygenated derivatives. Bornyl acetate was metabolized to camphor, and α- and β-pinene to trans -4-thujanol and other oxygenated products. Electrophysiological measurements showed that I . typographus possesses dedicated olfactory sensory neurons for oxygenated metabolites. Both camphor and trans -4-thujanol attracted beetles at specific doses in walking olfactometer experiments, and the presence of symbiotic fungi enhanced attraction of females to pheromones. Another co-occurring nonbeneficial fungus ( Trichoderma sp.) also produced oxygenated monoterpenes, but these were not attractive to I . typographus . Finally, we show that colonization of fungal symbionts on spruce bark diet stimulated beetles to make tunnels into the diet. Collectively, our study suggests that the blends of oxygenated metabolites of conifer monoterpenes produced by fungal symbionts are used by walking bark beetles as attractive or repellent cues to locate breeding or feeding sites containing beneficial microbial symbionts. The oxygenated metabolites may aid beetles in assessing the presence of the fungus, the defense status of the host tree and the density of conspecifics at potential feeding and breeding sites.

A tree biodiversity and ecosystem function experiment shows that leaf bacterial diversity is positively related to plant community productivity, and explains a portion of the variation in productivity that would otherwise be attributed to plant diversity and functional traits. Leaf bacteria promote plant production Biodiversity-ecosystem function studies have shown that plant species richness, functional diversity and functional identity are among the key factors driving terrestrial ecosystem productivity. Here, Isabelle Laforest-Lapointe and colleagues assess the contribution that leaf bacterial diversity makes to plant community production in a tree biodiversity-ecosystem function experiment carried out in Montreal, Canada. They find that leaf bacterial diversity is positively related to plant community productivity and explains a portion of the variation in productivity that would otherwise be attributed to plant diversity and functional traits. They conclude that biodiversity-ecosystem function relationships in plant communities could in part be driven by positive interactions that involve other trophic levels, including the plant microbiome. Research on biodiversity and ecosystem functioning has demonstrated links between plant diversity and ecosystem functions such as productivity 1 , 2 . At other trophic levels, the plant microbiome has been shown to influence host plant fitness and function 3 , 4 , and host-associated microbes have been proposed to influence ecosystem function through their role in defining the extended phenotype of host organisms 5 , 6 However, the importance of the plant microbiome for ecosystem function has not been quantified in the context of the known importance of plant diversity and traits. Here, using a tree biodiversity–ecosystem functioning experiment, we provide strong support for the hypothesis that leaf bacterial diversity is positively linked to ecosystem productivity, even after accounting for the role of plant diversity. Our results also show that host species identity, functional identity and functional diversity are the main determinants of leaf bacterial community structure and diversity. Our study provides evidence of a positive correlation between plant-associated microbial diversity and terrestrial ecosystem productivity, and a new mechanism by which models of biodiversity–ecosystem functioning relationships can be improved.