From the establishment of the first biodiversity experiments in the 1990s, studies have consistently reported positive relationships between plant diversity and productivity in grasslands. However, the predominant hypotheses that may explain this pattern have changed. Initially, there was a strong focus on plant–plant interactions such as facilitation and resource partitioning, but the results from the first experiments that manipulated soil communities have led to a paradigm shift. In the current view on mechanisms that drive plant diversity–productivity relationships, fungal pathogen‐induced reductions of plant productivity at low diversity play an important role. This role rests on two assumptions: the effects of pathogens (a) are plant‐species specific (i.e. not all plant species are affected equally by a fungal pathogen) and (b) display negative density dependence (i.e. decrease with decreasing host plant density and hence, with increasing plant species richness). Here, we review the empirical evidence for these two assumptions. In the biodiversity literature, this is mainly based on indirect approaches, such as soil sterilization, plant–soil feedback studies and plant biomass patterns. The identification and functional characterization of the fungal pathogens that actually drive the plant diversity–productivity relationship have only recently started. Synthesis. Nevertheless, these studies, together with studies on plant–pathogen interactions in agricultural crops and forests, clearly suggest host‐specific, negative density‐dependent effects of fungal pathogens are common. Moreover, recent studies suggest that the reduced impact of pathogens at high plant diversity depends not just on host density but also on effects of neighbouring (non‐host) plant species on the pathogen. Understanding how neighbouring plants affect the interactions between a pathogen and its host plants and disentangling the role of plant–pathogen interactions from other mechanisms potentially driving diversity–productivity relationships are important future challenges.

Soil-borne fungal diseases are a major problem in agriculture. A century ago, the Dutch plant pathologist Johanna Westerdijk recognized the importance of linking fungal biology with ecology to understand plant disease dynamics. To explore new ways to manage soil-borne fungal disease in agriculture by 'learning from nature', we follow in her footsteps: we link below ground plant-fungal pathogen interactions to ecological settings, i.e. natural grasslands. Ecological research hypothesised that the build-up of 'enemies' is reduced in species-rich vegetation compared to monocultures. To understand how plant diversity can suppress soilborne fungal pathogens, we first need to identify fungal actors in species-rich grasslands. Next-generation sequencing revealed a first glimpse of the potential fungal actors, but their ecological functions often remain elusive. Databases are becoming available to predict the ecological fungal guild, but classic phytopathology studies that isolate and characterize -taxonomically and functionally -, remain essential. Secondly, we need to set-up experiments that reveal ecological mechanisms underlying the complex below ground interactions between plant diversity and fungal pathogens. Several studies suggested that disease incidence of (hostspecific) pathogens is related to abundance of the host plant species. However, recent studies suggest that next to host species density, presence of heterospecific species additionally affects disease dynamics. We explore the direct and indirect ways of these neighboring plants diluting pathogen pressure. We argue that combining the expertise of plant pathologists and ecologists will improve our understanding of belowground plant-fungal pathogen interactions in natural grasslands and contribute to the design of sustainable and productive intercropping strategies in agriculture.

The navel orangeworm, Amyelois transitella (Walker), is a polyphagous pest of California nut crops and is responsible for extensive losses in the United States. It directly damages crops by feeding and contaminating nuts with frass and webbing and vectors saprophytic fungi that infect crops. The navel orangeworm is commonly associated with Aspergillus species, including the toxigenic Aspergillus flavus, which causes crop loss by producing carcinogens, including aflatoxin B1. This lepidopteran-fungus association is the most economically serious pest complex in Central Valley orchards, and evidence indicates that this relationship is mutualistic. We assessed preference and performance of navel orangeworm larvae associated with A. flavus in behavioral bioassays in which neonates were allowed to orient within arenas to media with or without fungal tissue, and performance bioassays in which larvae were reared with and without A. flavus on potato dextrose agar (PDA) and a semidefined almond PDA diet to evaluate effects on development and pupal weight. Navel orangeworm larvae were attracted to A. flavus and developed faster in its presence, indicating a nutritional benefit to the caterpillars. Larvae reached pupation ∼33% faster on diet containing A. flavus, and pupal weights were ∼18% higher for males and ∼13% higher for females on this diet. Our findings indicate that A. flavus plays an important role in larval orientation and development on infected hosts. The preference-performance relationship between navel orangeworms and Aspergillus flavus is consistent with a facultative mutualism that has broad implications for pest management efforts and basic understanding of Lepidoptera-plant interactions.

Biodiversity can reduce or increase disease transmission. These divergent effects suggest that community composition rather than diversity per se determines disease transmission. In natural plant communities, little is known about the functional roles of neighbouring plant species in belowground disease transmission.Here, we experimentally investigated disease transmission of a fungal root pathogen (Rhizoctonia solani) in two focal plant species in combinations with four neighbour species of two ages. We developed stochastic models to test the relative importance of two transmissionmodifying mechanisms: (1) infected hosts serve as nutrient supply to increase hyphal growth, so that successful disease transmission is self-reinforcing; and (2) plant resistance increases during plant development.Neighbouring plants either reduced or increased disease transmission in the focal plants. These effects depended on neighbour age, but could not be explained by a simple dichotomy between hosts and nonhost neighbours. Model selection revealed that both transmissionmodifying mechanisms are relevant and that focal host-neighbour interactions changed which mechanisms steered disease transmission rate.Our work shows that neighbour-induced shifts in the importance of these mechanisms across root networks either make or break disease transmission chains. Understanding how diversity affects disease transmission thus requires integrating interactions between focal and neighbour species and their pathogens.

1. Plant diversity can reduce the risk of plant disease, but positive, and neutral effects have also been reported. These contrasting relationships suggest that plant community composition, rather than diversity per se, affects disease risk.Here, we investigated how the diversity and composition of plant communities drive root-associated pathogen accumulation belowground.2. In a temperate grassland biodiversity experiment, containing 16 plant species (forbs and grasses), we determined the abundance of root-associated fungal pathogens in individual plant species growing in monocultures and in fourspecies mixtures through Illumina MiSeq amplicon sequencing.3. In the plant monocultures, we identified three major fungal pathogens that differed in host range: Paraphoma chrysanthemicola, associated with roots of forb species of the Asteraceae family, Slopeiomyces cylindrosporus, associated with grass species, and Rhizoctonia solani, associated with multiple forb and grass species. In mixtures, there was no significant reduction in relative abundance of these pathogens in their host species as compared to monocultures. However, in mixtures, there was a significant increase in relative abundance of each pathogen in several non-host and host plant species. Across mixtures, plant community composition affected pathogen relative abundance in individual plant species. This effect was driven by the presence of a particular neighbouring plant species (depending on the pathogen), rather than functional group composition (i.e. grass/forb ratio) or averaged pathogen pressure (based on monocultures) of all neighbours. Specifically, the presence of neighbour host species Achillea millefolium significantly increased P. chrysanthemicola, but decreased R. solani relative abundance in several host and non-host plant species in mixtures. Synthesis.Our results indicate that interactions between different plant speciesboth host and non-hosts-and fungal pathogens underlie the effects of plant

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