Fungal Pathogen Communities Research Articles

Negative plant–soil feedback influences a dominant seeded species, Western yarrow (Achillea millefolium), in grassland restoration

Plant community ecology guides restoration of degraded lands, yet seed‐based restorations sometimes fail or result in unpredictable outcomes, necessitating a better understanding of community trajectory and stability. Western yarrow (Achillea millefolium) declined suddenly in two separate restoration projects after initial high relative abundance. To assess the potential role of soil pathogens, we surveyed plant and soil fungal communities in these restorations, and used an 8‐year‐old field experiment that crossed yarrow planted in varying densities with a fungicide treatment. Two greenhouse experiments then evaluated whether the suppressive effect in yarrow soil spread to native species used in restoration. Lower yarrow cover in a restoration project 5 years compared to 3 years after seeding coincided with higher relative abundance of fungal taxa that can cause disease, particularly Crown‐rot fungi (Paraphoma spp.). Paraphoma increased over time in experimental plots and coincided with yarrow decline. Decline onset was density‐dependent, occurring faster in plant communities where yarrow density was higher. Fungicide applications altered fungal pathogen communities and promoted yarrow cover relative to control plots. In the greenhouse, yarrow grew larger with fungicide, consistent with suppression of fungal pathogens. However, biomass of natives grown in yarrow‐conditioned soil was not affected by fungicides, suggesting pathogens did not spread. The rapid establishment and competitive nature of yarrow, followed by pathogen‐induced decline, make it an attractive early transitional “bridge species,” so long as its pathogens are species‐specific. Our results suggest negative plant‐soil feedback can drive rapid decline of individual species, and considering plant–soil feedback could improve restoration predictability.

National-scale investigation reveals the dominant role of phyllosphere fungal pathogens in sorghum yield loss

Fungal plant pathogens threaten crop production and sustainable agricultural development. However, the environmental factors driving their diversity and nationwide biogeographic model remain elusive, impacting our capacity to predict their changes under future climate scenarios. Here, we analyzed potential fungal plant pathogens from 563 samples collected from 57 agricultural fields across China. Over 28.0% of fungal taxa in the phyllosphere were identified as potential plant pathogens, compared to 22.3% in the rhizosphere. Dominant fungal plant pathogen groups were Cladosporium (in the phyllosphere) and Fusarium (in the rhizosphere), with higher diversity observed in the phyllosphere than in rhizosphere soil. Deterministic processes played an important role in shaping the potential fungal plant pathogen community assembly in both habitats. Mean annual precipitation and temperature were the most important factor influencing phyllosphere fungal plant pathogen richness. Significantly negative relationships were found between fungal pathogen diversity and sorghum yield. Notably, compared to the rhizosphere, the phyllosphere fungal plant pathogen diversity played a more crucial role in sorghum yield. Together, our work provides novel insights into the factors governing the spatial patterns of fungal plant pathogens in the crop microbiome, and highlights the potential significance of aboveground phyllosphere fungal plant pathogens in crop productivity.

Ant handling changes myrmecochore seed coat microbiomes and alters diversity of seed‐borne plant pathogenic fungi

Abstract The putative benefits to seeds in myrmecochory (ant‐mediated seed dispersal) are often cast in a reward context. However, microbes have been mostly overlooked as seed mortality agents in myrmecochory, as have potential treatments provided by ant‐handling. We investigated the effects of ant handling on the diversity of seed coat fungal communities of three myrmecochorous plant species. Ant‐handling altered measures of both alpha and beta diversity of fungal communities. Ant‐handled seeds harboured different overall fungal communities and plant pathogen communities than non‐ant‐handled seeds. The myrmecochore pathogenic fungal community showed high dissimilarity (high pairwise community turnover) between ant‐handled and control seeds, while beta diversity measures for ant‐handled seeds and seeds with manually removed elaiosomes were less dissimilar. Ant handling may offer an additional benefit to myrmecochorous seeds via the reduction in the seed coat pathogenic community, which may be driven by elaiosome removal or as a by‐product of ant cleaning behaviours and chemical secretions. Read the free Plain Language Summary for this article on the Journal blog.

The interaction of climate, plant, and soil factors drives putative soil fungal pathogen diversity and community structure in dry grasslands.

Soil pathogens play important roles in shaping soil microbial diversity and controlling ecosystem functions. Though climate and local environmental factors and their influences on fungal pathogen communities have been examined separately, few studies explore the relative contributions of these factors. This is particularly crucial in eco-fragile regions, which are more sensitive to environmental changes. Herein we investigated the diversity and community structure of putative soil fungal pathogens in cold and dry grasslands on the Tibetan Plateau, using high-throughput sequencing. The results showed that steppe soils had the highest diversity of all pathogens and plant pathogens; contrastingly, meadow soils had the highest animal pathogen diversity. Structural equation modelling revealed that climate, plant, and soil had similar levels of influence on putative soil fungal pathogen diversity, with total effects ranging from 52% to 59% (all p < 0.001), with precipitation exhibiting a stronger direct effect than plant and soil factors. Putative soil fungal pathogen community structure gradually changed with desert, steppe, and meadow, and was primarily controlled by the interactions of climate, plant, and soil factors rather than by distinct factors individually. This finding contrasts with most studies of soil bacterial and fungal community structure, which generally report dominant roles of individual environmental factors.

Plant species identity and mycorrhizal type explain the root-associated fungal pathogen community assembly of seedlings based on functional traits in a subtropical forest.

As a crucial factor in determining ecosystem functioning, interaction between plants and soil-borne fungal pathogens deserves considerable attention. However, little attention has been paid into the determinants of root-associated fungal pathogens in subtropical seedlings, especially the influence of different mycorrhizal plants. Using high-throughput sequencing techniques, we analyzed the root-associated fungal pathogen community for 19 subtropical forest species, including 10 ectomycorrhizal plants and 9 arbuscular mycorrhizal plants. We identified the roles of different factors in determining the root-associated fungal pathogen community. Further, we identified the community assembly process at species and mycorrhizal level and managed to reveal the drivers underlying the community assembly. We found that plant species identity, plant habitat, and plant mycorrhizal type accounted for the variations in fungal pathogen community composition, with species identity and mycorrhizal type showing dominant effects. The relative importance of different community assembly processes, mainly, homogeneous selection and drift, varied with plant species identity. Interestingly, functional traits associated with acquisitive resource-use strategy tended to promote the relative importance of homogeneous selection, while traits associated with conservative resource-use strategy showed converse effect. Drift showed the opposite relationships with functional traits compared with homogeneous selection. Notably, the relative importance of different community assembly processes was not structured by plant phylogeny. Drift was stronger in the pathogen community for ectomycorrhizal plants with more conservative traits, suggesting the predominant role of stochastic gain and loss in the community assembly. Our work demonstrates the determinants of root-associated fungal pathogens, addressing the important roles of plant species identity and plant mycorrhizal type. Furthermore, we explored the community assembly mechanisms of root-associated pathogens and stressed the determinant roles of functional traits, especially leaf phosphorus content (LP), root nitrogen content (RN) and root tissue density (RTD), at species and mycorrhizal type levels, offering new perspectives on the microbial dynamics underlying ecosystem functioning.

Rapid differentiation of soil and root microbiomes in response to plant composition and biodiversity in the field

Research suggests that microbiomes play a major role in structuring plant communities and influencing ecosystem processes, however, the relative roles and strength of change of microbial components have not been identified. We measured the response of fungal, arbuscular mycorrhizal fungal (AMF), bacteria, and oomycete composition 4 months after planting of field plots that varied in plant composition and diversity. Plots were planted using 18 prairie plant species from three plant families (Poaceae, Fabaceae, and Asteraceae) in monoculture, 2, 3, or 6 species richness mixtures and either species within multiple families or one family. Soil cores were collected and homogenized per plot and DNA were extracted from soil and roots of each plot. We found that all microbial groups responded to the planting design, indicating rapid microbiome response to plant composition. Fungal pathogen communities were strongly affected by plant diversity. We identified OTUs from genera of putatively pathogenic fungi that increased with plant family, indicating likely pathogen specificity. Bacteria were strongly differentiated by plant family in roots but not soil. Fungal pathogen diversity increased with planted species richness, while oomycete diversity, as well as bacterial diversity in roots, decreased. AMF differentiation in roots was detected with individual plant species, but not plant family or richness. Fungal saprotroph composition differentiated between plant family composition in plots, providing evidence for decomposer home-field advantage. The observed patterns are consistent with rapid microbiome differentiation with plant composition, which could generate rapid feedbacks on plant growth in the field, thereby potentially influencing plant community structure, and influence ecosystem processes. These findings highlight the importance of native microbial inoculation in restoration.

Plant physiology, microbial community, and risks of multiple fungal diseases along a soil nitrogen gradient

Nitrogen (N) is an essential element for plant growth and development. N levels in soil may also impact plant disease occurrence. However, the physiological and microbial mechanisms between N levels in soil and plant disease occurrence are not quite clear at present. In this study, we examined the impact of seven urea levels (0 to 800 mg kg−1 soil) on the physiology of tomato (Lycopersicon esculentum) and fungal disease occurrence. Our results showed that the disease incidence and index caused by a tomato early blight pathogen (Alternaria alternata) increased with increasing N levels. The disease index and percentage of disease incidence were positively correlated with N content, indole-3-acetic acid (IAA) and salicylic acid (SA) in plants, but negatively correlated with fungal community diversity. In addition to pathogens (A. alternata) that cause known early blight, 39 other fungal taxa were also identified as plant pathogens in tomato roots, leaves, and soil, the dominant putative pathogens included Ceratobasidiaceae sp., Fusarium oxysporum, Macrophomina phaseolina, Nectriaceae sp., Podosphaera fusca and Trichoderma viride. N levels affected the distribution and dynamics of the fungal pathogen community, such as the abundance of Fusarium oxysporum increased by 33% on roots from days 25 to 35. Our results demonstrated that plants undergo complex disease risk from different pathogens under different N levels, highlighting a need for proper N management, and integration of nutrient management as a disease control approach for sustainable agricultural production.

Fungal Pathogens in Grasslands.

Grasslands are major primary producers and function as major components of important watersheds. Although a concise definition of grasslands cannot be given using a physiognomic or structural approach, grasslands can be described as vegetation communities experiencing periodical droughts and with canopies dominated by grasses and grass-like plants. Grasslands have a cosmopolitan distribution except for the Antarctic region. Fungal interactions with grasses can be pathogenic or symbiotic. Herbivorous mammals, insects, other grassland animals, and fungal pathogens are known to play important roles in maintaining the biomass and biodiversity of grasslands. Although most pathogenicity studies on the members of Poaceae have been focused on economically important crops, the plant-fungal pathogenic interactions involved can extend to the full range of ecological circumstances that exist in nature. Hence, it is important to delineate the fungal pathogen communities and their interactions in man-made monoculture systems and highly diverse natural ecosystems. A better understanding of the key fungal players can be achieved by combining modern techniques such as next-generation sequencing (NGS) together with studies involving classic phytopathology, taxonomy, and phylogeny. It is of utmost importance to develop experimental designs that account for the ecological complexity of the relationships between grasses and fungi, both above and below ground. In grasslands, loss in species diversity increases interactions such as herbivory, mutualism, predation or infectious disease transmission. Host species density and the presence of heterospecific host species, also affect the disease dynamics in grasslands. Many studies have shown that lower species diversity increases the severity as well as the transmission rate of fungal diseases. Moreover, communities that were once highly diverse but have experienced decreased species richness and dominancy have also shown higher pathogenicity load due to the relaxed competition, although this effect is lower in natural communities. This review addresses the taxonomy, phylogeny, and ecology of grassland fungal pathogens and their interactions in grassland ecosystems.

More diverse tree communities promote foliar fungal pathogen diversity, but decrease infestation rates per tree species, in a subtropical biodiversity experiment

Abstract Fungal pathogens have the potential to affect plant biogeography and ecosystem processes through their influence on the fitness and functioning of their plant hosts. Simultaneously, changes in plant communities can influence fungal pathogen communities. Exactly which host plant attributes determine the composition of fungal pathogen communities on the leaves remains poorly understood. Here, we characterized foliar fungal pathogen communities in subtropical tree communities along an experimental diversity gradient in Jiangxi, South‐East China. On 32 tree species, we identified all visible fungal structures and symptoms microscopically and studied fungi‐specific traits such as conidia or spores in detail. We asked how different facets of biodiversity, including taxonomic, phylogenetic and functional tree diversity, shape fungal diversity and fungal infestation at different scales. We found a positive relationship between tree richness and fungal richness at the plot level. At the level of individual trees of the same species, the relationship between tree species richness and fungal species richness was marginally significantly negative. Importantly, the fungal infestation rates decreased as tree species richness increased, suggesting that colonization of hosts by specialist fungi was impeded by dilution of the pool of available hosts. Moreover, we found evidence for similar topologies between phylogenetic topologies of trees and fungal genera which is a precondition for coevolution and we identified leaf traits, including leaf habit (deciduous/evergreen), leaf magnesium content and stomata size that predicted fungal richness and infestation. Synthesis. Our study indicates that host tree species harbour different foliar fungal pathogens, which sums up to the highest fungal pathogen richness in more diverse forest stands. At the same time, the foliar fungal pathogen infestation rate for each tree species decreased with increasing tree richness in forests. We identified leaf traits that can help to better predict fungal pathogen richness and infestation, and we show that phylogenetically closely related tree species harbour phylogenetically closely related foliar fungal pathogens. These new insights might be helpful to improve the pest resilience of future forests and plantations.

Nest substrate, more than ant activity, drives fungal pathogen community dissimilarity in seed-dispersing ant nests.

Myrmecochory is a widespread mutualism in which plants benefit from seed dispersal services by ants. Ants might also be providing seeds with an additional byproduct benefit via reduced plant pathogen loads in the ant nest environment through their antimicrobial glandular secretions. We investigate this byproduct benefit by identifying fungal communities in ant nests and surrounding environments and quantifying fungal community change (1) through time, (2) between different nest substrates, and (3) as a function of average ant activity levels within nests (based on observed ant activity at nest entrances throughout the summer). We split fungal communities by functional guild to determine seed-dispersing ant-induced changes in the overall fungal community, the animal pathogen fungal community, the plant pathogen fungal community, and the myrmecochore pathogen fungal community. Nest substrate (soil or log) explained much of the variation in fungal community dissimilarity, while substrate occupation (ant nest or control sample) and time had no influence on fungal community composition. Average ant activity had no effect on the community turnover in fungal communities except for the myrmecochore pathogenic fungal community. In this community, higher ant activity throughout the summer resulted in more fluctuation in the pathogenic community in the ant nest. Our results are not consistent with a byproduct benefit framework in myrmecochory, but suggest that nest substrate drives dissimilarity in fungal communities. The influence of nest substrate on fungal communities has important implications for seeds taken into ant nests, as well as ant nest location choice by queens and during nest relocation.

An invasive plant rapidly increased the similarity of soil fungal pathogen communities.

Plant invasions can change soil microbial communities and affect subsequent invasions directly or indirectly via foliar herbivory. It has been proposed that invaders promote uniform biotic communities that displace diverse, spatially variable communities (the biotic homogenization hypothesis), but this has not been experimentally tested for soil microbial communities, so the underlying mechanisms and dynamics are unclear. Here, we compared density-dependent impacts of the invasive plant Alternanthera philoxeroides and its native congener A. sessilis on soil fungal communities, and their feedback effects on plants and a foliar beetle. We conducted a plant-soil feedback (PSF) experiment and a laboratory bioassay to examine PSFs associated with the native and invasive plants and a beetle feeding on them. We also characterized the soil fungal community using high-throughput sequencing. We found locally differentiated soil fungal pathogen assemblages associated with high densities of the native plant A. sessilis but little variation in those associated with the invasive congener A. philoxeroides, regardless of plant density. In contrast, arbuscular mycorrhizal fungal assemblages associated with high densities of the invasive plant were more variable. Soil biota decreased plant shoot mass but their effect was weak for the invasive plant growing in native plant-conditioned soils. PSFs increased the larval biomass of a beetle reared on leaves of the native plant only. Moreover, PSFs on plant shoot and root mass and beetle mass were predicted by different pathogen taxa in a plant species-specific manner. Our results suggest that plant invasions can rapidly increase the similarity of soil pathogen assemblages even at low plant densities, leading to taxonomically and functionally homogeneous soil communities that may limit negative soil effects on invasive plants.

Habitat type and interannual variation shape unique fungal pathogen communities on a California native bunchgrass.

The role of infectious disease in regulating host populations is increasingly recognized, but how environmental conditions affect pathogen communities and infection levels remains poorly understood. Over 3 y, we compared foliar disease burden, fungal pathogen community composition, and foliar chemistry in the perennial bunchgrass Stipa pulchra occurring in adjacent serpentine and nonserpentine grassland habitats with distinct soil types and plant communities. We found that serpentine and nonserpentine S. pulchra experienced consistent, low disease pressure associated with distinct fungal pathogen communities with high interannual species turnover. Additionally, plant chemistry differed with habitat type. The results indicate that this species experiences minimal foliar disease associated with diverse fungal communities that are structured across landscapes by spatially and temporally variable conditions. Distinct fungal communities associated with different growing conditions may shield S. pulchra from large disease outbreaks, contributing to the low disease burden observed on this and other Mediterranean grassland species.

Meta-Analysis and Evaluation by Insect-Mediated Baiting Reveal Different Patterns of Hypocrealean Entomopathogenic Fungi in the Soils From Two Regions of China.

A survey was carried out on forest soils and grassland soils from Hebei and Sichuan provinces using Tenebrio molitor larvae as a bait, and high-throughput DNA sequencing (HTS) of the fungal internal transcribed spacer-2 ribosomal DNA was used to monitor the natural distribution of three leading hypocrealean families of insect fungal pathogens (Clavicipitaceae, Cordycipitaceae, and Ophiocordycipitaceae). The occurrence of insect fungal pathogens in soil samples from 98 different sites was compared. The use of insect bait indicated that entomopathogenic fungi of the genus Metarhizium were predominant, followed by Beauveria and Isaria. Molecular characterization using the Mz_FG543 intergenic region revealed that the Metarhizium species pool was phylogenetically composed of three closely related species as follows; Metarhizium pingshaense (n = 74), Metarhizium robertsii (n = 51), and Metarhizium brunneum (n = 26), as well as one isolate which clustered with Metarhizium flavoviride. Nine potentially new phylogenetic species were delimited within the M. flavoviride species complex by sequencing of the 5′ elongation factor-1 alpha region locus. The Beauveria (n = 64) and Isaria (n = 5) isolates were characterized via sequence analyses of the Bloc region. An intergenic spacer phylogeny of the Beauveria isolate assemblage revealed the phylogenetic species within the Beauveria bassiana clade. Interestingly, the individuals of M. pingshaense (n = 18) and M. brunneum (n = 12) exhibited the presence of both mating types in Sichuan Province. Similarly, for the Beauveria isolates, reproductive mode assays demonstrated that all four B. bassiana subclades possessed bipolar outcrossing mating systems. Of these, 19 isolates contained two mating types, and the rest were fixed for single mating types, revealing opportunities for intra-lineage heterothallic mating. The HTS results showed a significantly higher occurrence of the Clavicipitaceae family and the Metarhizium genus in the soil samples. The Venn diagram showed Metarhizium anisopliae (senso lato), Isaria farinose, and B. bassiana as frequently abundant fungal pathogen operational taxonomic units (core) across sampling sites, while the baiting method showed that the genus of Isaria was isolated locally. The Mantel test verified that community dissimilarity increased significantly with geographical distance, suggesting that geographical coordinates are possible factors that influence the insect fungal pathogen community composition in the studied sites. This study is the first to highlight the usefulness of utilizing soil baiting and deep sequencing to investigate the population dynamics of entomopathogens in soil.

Geographical Distribution of Fungal Plant Pathogens in Dust Across the United States

As the world’s population grows, global food production will need to increase. While food production efficiency has increased in recent decades through pathogen control, climate change poses new challenges in crop protection against pathogens. Understanding the natural geographical distribution and dispersal likelihood of fungal plant pathogens is essential for forecasting disease plant spread. Here we used cultivation-independent techniques to identify fungal plant pathogens in 1,289 near-surface dust samples collected across the United States. We found that overall fungal pathogen community composition is more related to environmental conditions (in particular soil pH, precipitation and frost) than to agricultural hosts and practices. We also delimited five susceptibility geographical areas in the United States where different sets of pathogens tend to occur.

Fungal pathogens pose a potential threat to animal and plant health in desertified and pika-burrowed alpine meadows on the Tibetan Plateau.

Intact Tibetan meadows provide significant defense against soil-borne pathogen dispersal. However, dramatic meadow degradation has been observed due to climate change and pika damage, but their impacts on soil-borne pathogens are still unclear. With approximately 40% of the world's population living in Tibetan Plateau and its downstream watersheds, this lack of knowledge should be of great concern. Here, we used Illumina amplicon sequencing to characterize the changes in potential human, domestic animal, plant, and zoonotic bacterial and fungal pathogens in nondegraded, desertified, and pika-burrowed meadows. The relative abundance of bacterial domestic animal pathogens and zoonotic pathogens were significantly increased by desertification. Pika burrowing significantly increased the relative abundance of bacterial human pathogens and zoonotic pathogens. The species richness and relative abundance of fungal pathogens was significantly increased by desertification and pika burrowing. Accordingly, fungal plant and animal pathogens categorized by FUNGuid significantly increased in desertified and pika-burrowed meadows. Soil chemical and plant properties explained 38% and 64% of the bacterial and fungal pathogen community variance, respectively. Therefore, our study indicates for the first time that both alpine meadow desertification and pika burrowing could potentially increase infectious disease risks in the alpine ecosystem, especially for fungal diseases.

The seeds of success: release from fungal attack on seeds may influence the invasiveness of alien Impatiens

Although closely related, Impatiens glandulifera and Impatiens balfourii differ in their invasiveness in Europe; only the former is highly invasive there. Following the assumptions of the enemy release hypothesis (ERH), we tested whether these differences may be explained by the levels of seed infestation by pathogenic fungi. Using seeds collected along the Swiss-Italian border, we recorded four true pathogens of seeds: Fusarium culmorum, F. oxysporum, F. sporotrichoides, and Giberella avenacea. In Italy the seeds of I. balfourii were infected by fungal pathogens more often than those of I. glandulifera, while in Switzerland both species were under the same level of pressure. However, the overall differences in pathogen abundance were consistent with the ERH: seeds of the more invasive species were attacked less. This could be a result of differences between the communities of fungal pathogens attacking the seeds of both species in each country. The number of colonies of secondary pathogens (Cladosporium cladosporioides, Alternaria alternata) correlated negatively with the number of colonies of true pathogens; we suggest that the secondary pathogens may have prevented the occurrence of the true pathogens. The reason for the between-country differences in the fungal pathogen communities is unclear. A possible explanation is that Italy and Switzerland differ in their road and green-area maintenance work schemes, which may have influenced pathogen pressure on seeds. This study is one of the few that offers results indicating that release from enemies may be crucial to the invasion success of plants as early as the seed stage.

Land-use intensification causes multitrophic homogenization of grassland communities.

Land-use intensification is a major driver of biodiversity loss. Alongside reductions in local species diversity, biotic homogenization at larger spatial scales is of great concern for conservation. Biotic homogenization means a decrease in β-diversity (the compositional dissimilarity between sites). Most studies have investigated losses in local (α)-diversity and neglected biodiversity loss at larger spatial scales. Studies addressing β-diversity have focused on single or a few organism groups (for example, ref. 4), and it is thus unknown whether land-use intensification homogenizes communities at different trophic levels, above- and belowground. Here we show that even moderate increases in local land-use intensity (LUI) cause biotic homogenization across microbial, plant and animal groups, both above- and belowground, and that this is largely independent of changes in α-diversity. We analysed a unique grassland biodiversity dataset, with abundances of more than 4,000 species belonging to 12 trophic groups. LUI, and, in particular, high mowing intensity, had consistent effects on β-diversity across groups, causing a homogenization of soil microbial, fungal pathogen, plant and arthropod communities. These effects were nonlinear and the strongest declines in β-diversity occurred in the transition from extensively managed to intermediate intensity grassland. LUI tended to reduce local α-diversity in aboveground groups, whereas the α-diversity increased in belowground groups. Correlations between the β-diversity of different groups, particularly between plants and their consumers, became weaker at high LUI. This suggests a loss of specialist species and is further evidence for biotic homogenization. The consistently negative effects of LUI on landscape-scale biodiversity underscore the high value of extensively managed grasslands for conserving multitrophic biodiversity and ecosystem service provision. Indeed, biotic homogenization rather than local diversity loss could prove to be the most substantial consequence of land-use intensification.

Differentiating genetic and environmental drivers of plant–pathogen community interactions

Summary Plant genotypic variation can shape associated arthropod and microbial communities locally, as has been demonstrated in controlled common garden experiments. However, the relative roles of plant genetics and the environment in defining communities at larger spatial scales are not well known. The environmental heterogeneity hypothesis maintains that plant genetic effects on associated communities diminish across the landscape as environmental variation predominates. Alternatively, the local adaptation hypothesis argues that plant genetic effects change across landscapes as a result of species interactions being locally adapted. Thus, very different mechanisms could produce similar patterns. Using replicated common gardens located along an elevation and distance gradient, observational studies in the wild, and a greenhouse inoculation experiment, we examined these two non‐mutually exclusive hypotheses for Populus angustifolia and its fungal leaf pathogen community. Supporting the environmental heterogeneity hypothesis, plant genotypic effects on fungal leaf pathogen communities were two to three times stronger within than among gardens. Consistent with the local adaptation hypothesis, plant genotypic effects on pathogens also varied significantly among gardens (i.e. G × E interaction effect). Observational data from the wild and our greenhouse inoculation experiment unveiled clinal adaptation in plant genetic resistance that is correlated with disease risk along the elevation gradient, but did not support local pathogen adaptation to plants or vice versa. Synthesis. While our study found that plant genotype plays a significant role in shaping associated pathogen communities at local and geographic scales, the environment most strongly influenced P. angustifolia leaf pathogens at the geographic scale. Plant genetic effects on pathogens were also influenced by the environment, highlighting the potential for environmental (e.g. climate) change to trigger local evolutionary responses in plant–pathogen community interactions.

Genetic basis of pathogen community structure for foundation tree species in a common garden and in the wild

Summary Genetic variation within and among foundation plant species is known to affect arthropod, plant and soil microbial communities. We hypothesized that the same would be expected for pathogen communities, which have typically been studied only as individual pathogen species. In a common garden in Utah, USA, we first tested how genetic differences within and among Populus angustifolia, P. fremontii and their interspecific hybrid P. × hinckleyana affect a fungal leaf pathogen community. Next, we tested how Populus genetic differences at the level of species and hybrids affect fungal leaf pathogen communities in the wild, specifically in a natural Populus hybridization zone (13 river km) and throughout the larger Weber River watershed (150 river km). In the common garden, genetic variation both within and among Populus species and hybrids significantly affected the structure (i.e. species abundances and composition) of pathogen communities. In the wild, genetic variation among Populus species and hybrids also significantly affected pathogen communities, though not as strongly as was found in the common garden environment. Stand‐level density of the susceptible Populus species most strongly affected the structure of pathogen communities in the hybrid zone. Synthesis. Plant species and genotypic variation can affect the local and geographic distribution of pathogen communities in a similar fashion as other diverse organisms (e.g. arthropods, plants, soil microbes), both within a relatively controlled common garden environment and in the wild.