Alison E. Bennett

Three‐way interactions between plants, microbes and insects

Plants are important mediators of interactions between their associated microbe and insect communities (Van der Putten et al. 2001; Ohgushi 2005). Changes in plants induced by one species have cascading effects on interactions with other species, shaping their abundances and community structure (Ohgushi 2008). While the consequences of such indirect interactions for community structure have predominantly been examined within the plant-associated insect community (e.g. Van Zandt & Agrawal 2004; Poelman et al. 2008; Utsumi 2011), there is growing evidence that there are similar community-wide impacts of plant-mediated interactions between microbes and insects (e.g. Kluth, Kruess & Tscharntke 2001; Omacini et al. 2001; Katayama, Zhang & Ohgushi 2011; Tack, Gripenberg & Roslin 2012). This highlights the ecological importance of three-way interactions between plants, microbes and insects. The study of such ‘plant–microbe– insect’ (PMI) interactions (Fig. 1) is a research area that has been rapidly expanding in the past two decades. Molecular studies of the mechanisms underlying these three-way interactions, as well as ecological and evolutionary studies of the consequences of PMI interactions in natural communities, have recently given a large impetus to this young field. In this special feature, we have brought together eight papers reviewing different aspects of these recent advances in the field of PMI interactions. Research on PMI interactions has gradually bridged the traditionally separated subdisciplines of plant pathology, insect pathology and entomology. Plant pathologists early on realized that insects were not only important vectors of plant disease, but also one of the factors determining what was then called ‘host predisposition’ (Yarwood 1959; Schoeneweiss 1975). This term was used to describe any environmental alteration of the susceptibility of host plants to their pathogens, prior to their interaction. Similarly, in the 1980s, a series of reviews from entomologists appeared on the effects of plantand insect-associated microbes on plant resource exploitation by insects (e.g. Jones 1984; Hammond & Hardy 1988), culminating in the seminal book on microbial mediation of plant–insect interactions by Barbosa, Krischick & Jones 1991, which provided the first detailed and fascinating overview of the widespread, diverse and strong roles played by plantand insect-associated microbes in shaping plant–insect interactions. PMI interactions represent a broad research field, both in terms of the disciplines involved (from molecular

Research priorities for harnessing plant microbiomes in sustainable agriculture

Feeding a growing world population amidst climate change requires optimizing the reliability, resource use, and environmental impacts of food production. One way to assist in achieving these goals is to integrate beneficial plant microbiomes—i.e., those enhancing plant growth, nutrient use efficiency, abiotic stress tolerance, and disease resistance—into agricultural production. This integration will require a large-scale effort among academic researchers, industry researchers, and farmers to understand and manage plant-microbiome interactions in the context of modern agricultural systems. Here, we identify priorities for research in this area: (1) develop model host–microbiome systems for crop plants and non-crop plants with associated microbial culture collections and reference genomes, (2) define core microbiomes and metagenomes in these model systems, (3) elucidate the rules of synthetic, functionally programmable microbiome assembly, (4) determine functional mechanisms of plant-microbiome interactions, and (5) characterize and refine plant genotype-by-environment-by-microbiome-by-management interactions. Meeting these goals should accelerate our ability to design and implement effective agricultural microbiome manipulations and management strategies, which, in turn, will pay dividends for both the consumers and producers of the world food supply.

Arbuscular Mycorrhizal Fungal Networks Vary throughout the Growing Season and between Successional Stages

To date, few analyses of mutualistic networks have investigated successional or seasonal dynamics. Combining interaction data from multiple time points likely creates an inaccurate picture of the structure of networks (because these networks are aggregated across time), which may negatively influence their application in ecosystem assessments and conservation. Using a replicated bipartite mutualistic network of arbuscular mycorrhizal (AM) fungal-plant associations, detected using large sample numbers of plants and AM fungi identified through molecular techniques, we test whether the properties of the network are temporally dynamic either between different successional stages or within the growing season. These questions have never been directly tested in the AM fungal-plant mutualism or the vast majority of other mutualisms. We demonstrate the following results: First, our examination of two different successional stages (young and old forest) demonstrated that succession increases the proportion of specialists within the community and decreases the number of interactions. Second, AM fungal-plant mutualism structure changed throughout the growing season as the number of links between partners increased. Third, we observed shifts in associations between AM fungal and plant species throughout the growing season, potentially reflecting changes in biotic and abiotic conditions. Thus, this analysis opens up two entirely new areas of research: 1) identifying what influences changes in plant-AM fungal associations in these networks, and 2) what aspects of temporal variation and succession are of general importance in structuring bipartite networks and plant-AM fungal communities.

How can we exploit above-belowground interactions to assist in addressing the challenges of food security?

Can above–belowground interactions help address issues of food security? We address this question in this manuscript, and review the intersection of above–belowground interactions and food security. We propose that above–belowground interactions could address two strategies identified by Godfray etal. (2010): reducing the Yield Gap, and Increasing Production Limits. In particular, to minimize the difference between potential and realized production (The Yield Gap) above–belowground interactions could be manipulated to reduce losses to pests and increase crop growth (and therefore yields). To Increase Production Limits we propose two mechanisms: utilizing intercropping (which uses multiple aspects of above–belowground interactions) and breeding for traits that promote beneficial above–belowground interactions, as well as breeding mutualistic organisms to improve their provided benefit. As a result, if they are managed correctly, there is great potential for above–belowground interactions to contribute to food security.

Stressed out symbiotes: hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi

Abiotic stress is a widespread threat to both plant and soil communities. Arbuscular mycorrhizal (AM) fungi can alleviate effects of abiotic stress by improving host plant stress tolerance, but the direct effects of abiotic stress on AM fungi are less well understood. We propose two hypotheses predicting how AM fungi will respond to abiotic stress. The stress exclusion hypothesis predicts that AM fungal abundance and diversity will decrease with persistent abiotic stress. The mycorrhizal stress adaptation hypothesis predicts that AM fungi will evolve in response to abiotic stress to maintain their fitness. We conclude that abiotic stress can have effects on AM fungi independent of the effects on the host plant. AM fungal communities will change in composition in response to abiotic stress, which may mean the loss of important individual species. This could alter feedbacks to the plant community and beyond. AM fungi will adapt to abiotic stress independent of their host plant. The adaptation of AM fungi to abiotic stress should allow the maintenance of the plant-AM fungal mutualism in the face of changing climates.

Can plant–microbe–insect interactions enhance or inhibit the spread of invasive species?

Summary Invasive species are one of the great challenges facing the world leading to great economic losses. Increasing numbers of species introductions are also increasing the likelihood of new species interactions – particularly between plants, microbes and insects. Frequently discovered interactions between plants, microbes and insects are giving rise to a new field: plant–microbe–insect (PMI) interactions. This paper focuses on novel PMI interactions created from the introduction of new plant, insect and microbe species. In particular, this paper asks: Do novel PMI interactions promote or inhibit invasive plants, microbes and insects? And can we predict whether novel PMI interactions are likely to become invasive? While we might predict that novel PMI interactions are likely to be simple additive interactions due to their relatively short period of interaction, instead this review demonstrates that most novel PMI interactions are actually nonadditive. This manuscript shows that there are a great number of instances where invasive species are promoted by novel PMI interactions. By contrast, the studied cases where PMI interactions limit invasive species are predominantly biocontrol PMI interactions. Future research on novel PMI interactions should focus on predicting future novel PMI interactions that promote invasive species. Given that many novel PMI interactions involve plant pathogens and their insect vectors, this novel PMI interaction deserves more focus. New research should also focus on non-novel PMI interactions that could be manipulated to hinder the spread of invasive plant, microbe and insect species.

Early root herbivory impairs arbuscular mycorrhizal fungal colonization and shifts defence allocation in establishing Plantago lanceolata

Research into plant-mediated indirect interactions between arbuscular mycorrhizal (AM) fungi and insect herbivores has focussed on those between plant shoots and above-ground herbivores, despite the fact that only below-ground herbivores share the same part of the host plant as AM fungi. Using Plantago lanceolata L., we aimed to characterise how early root herbivory by the vine weevil (Otiorhynchus sulcatus F.) affected subsequent colonization by AM fungi (Glomus spp.) and determine how the two affected plant growth and defensive chemistry. We exposed four week old P. lanceolata to root herbivory and AM fungi using a 2×2 factorial design (and quantified subsequent effects on plant biomass and iridoid glycosides (IGs) concentrations. Otiorhynchus sulcatus reduced root growth by c. 64%, whereas plant growth was unaffected by AM fungi. Root herbivory reduced extent of AM fungal colonization (by c. 61%). O. sulcatus did not influence overall IG concentrations, but caused qualitative shifts in root and shoot IGs, specifically increasing the proportion of the more toxic catalpol. These changes may reflect defensive allocation in the plant against further attack. This study demonstrates that very early root herbivory during plant development can shape future patterns of AM fungal colonization and influence defensive allocation in the plant.

Root symbionts: Powerful drivers of plant above- and belowground indirect defenses

Soil microbial mutualists of plants, including mycorrhizal fungi, non‐mycorrhizal fungi and plant growth promoting rhizobacteria, have been typically characterized for increasing nutrient acquisition and plant growth. More recently, soil microbes have also been shown to increase direct plant defense against above‐ and belowground herbivores. Plants, however, do not only rely on direct defenses when attacked, but they can also recruit pest antagonists such as predators and parasitoids, both above and belowground, mainly via the release of volatile organic compounds (i.e., indirect defenses). In this review, we illustrate the main features and effects of soil microbial mutualists of plants on plant indirect defenses and discuss possible applications within the framework of sustainable crop protection against root‐ and shoot‐feeding arthropod pests. We indicate the main knowledge gaps and the future challenges to be addressed in the study and application of these multifaceted interactions.

Liming impacts on soils, crops and biodiversity in the UK: A review.

Fertile soil is fundamental to our ability to achieve food security, but problems with soil degradation (such as acidification) are exacerbated by poor management. Consequently, there is a need to better understand management approaches that deliver multiple ecosystem services from agricultural land. There is global interest in sustainable soil management including the re-evaluation of existing management practices. Liming is a long established practice to ameliorate acidic soils and many liming-induced changes are well understood. For instance, short-term liming impacts are detected on soil biota and in soil biological processes (such as in N cycling where liming can increase N availability for plant uptake). The impacts of liming on soil carbon storage are variable and strongly relate to soil type, land use, climate and multiple management factors. Liming influences all elements in soils and as such there are numerous simultaneous changes to soil processes which in turn affect the plant nutrient uptake; two examples of positive impact for crops are increased P availability and decreased uptake of toxic heavy metals. Soil physical conditions are at least maintained or improved by liming, but the time taken to detect change varies significantly. Arable crops differ in their sensitivity to soil pH and for most crops there is a positive yield response. Liming also introduces implications for the development of different crop diseases and liming management is adjusted according to crop type within a given rotation. Repeated lime applications tend to improve grassland biomass production, although grassland response is variable and indirect as it relates to changes in nutrient availability. Other indicators of liming response in grassland are detected in mineral content and herbage quality which have implications for livestock-based production systems. Ecological studies have shown positive impacts of liming on biodiversity; such as increased earthworm abundance that provides habitat for wading birds in upland grasslands. Finally, understanding of liming impacts on soil and crop processes are explored together with functional aspects (in terms of ecosystems services) in a new qualitative framework that includes consideration of how liming impacts change with time. This holistic approach provides insights into the far-reaching impacts that liming has on ecosystems and the potential for liming to enhance the multiple benefits from agriculturally managed land. Recommendations are given for future research on the impact of liming and the implications for ecosystem services.

Plant and insect microbial symbionts alter the outcome of plant‐herbivore‐parasitoid interactions: implications for invaded, agricultural and natural systems

1.Understanding how soil microbial communities influence plant interactions with other organisms, and how this varies with characteristics of the interacting organisms, is important for multiple systems. Solanum spp. are a suitable model for trophic interactions in studies of agricultural and natural systems and can also provide useful corollaries in invaded systems. This study examined the influence of soil mutualist arbuscular mycorrhizal (AM) fungi on growth of different Solanum types fed on by the potato aphid, Macrosiphum euphorbiae, in relation to presence of the aphid facultative endosymbiont Hamiltonella defensa. 2.Four Solanum types comprising two wild species, S. berthaultii and S. polyadenum, and two accessions of S. tuberosum, were grown with or without AM fungi and infested with one of four clonal lines of a single M. euphorbiae genotype (two with and two without H. defensa). Two experiments were conducted to i) characterise plant responses to AM fungi and aphids and ii) assess whether soil AM fungi could influence the success of the parasitoid wasp Aphidus ervi when attacking aphids reared on each Solanum type. 3.In both experiments, similar patterns of plant biomass were observed in relation to AM fungal and aphid treatments. Solanum biomass depended on plant type and aphid infection with H. defensa. Plants exposed to aphids harbouring H. defensa had smaller root biomass, and therefore total plant biomass, compared to plants infested with H. defensa-free aphids. M. euphorbiae performance varied with aphid clonal line, Solanum type and presence of AM fungi. 4.Parasitoid success, measured as the proportion of aphids from which a wasp emerged, was highest from aphids that had fed on plants colonised by AM fungi, although this result also varied with Solanum type and aphid clonal line. 5.Synthesis: The presence of soil AM fungi, combined with within-species plant and insect variation in key traits, can have subtle - but significant - effects on plant fitness and insect success. This study highlights the importance of exploring genotypic variation in plant and pest responses to soil microbiota to identify suitable biocontrol options. This article is protected by copyright. All rights reserved.