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Whilst many interactions with fungi are detrimental for plants, others are beneficial and result in improved growth and stress tolerance. Thus, plants have evolved sophisticated mechanisms to restrict pathogenic interactions while promoting mutualistic relationships. Numerous studies have demonstrated the importance of nitric oxide (NO) in the regulation of plant defence against fungal pathogens. NO triggers a reprograming of defence-related gene expression, the production of secondary metabolites with antimicrobial properties, and the hypersensitive response. More recent studies have shown a regulatory role of NO during the establishment of plant–fungal mutualistic associations from the early stages of the interaction. Indeed, NO has been recently shown to be produced by the plant after the recognition of root fungal symbionts, and to be required for the optimal control of mycorrhizal symbiosis. Although studies dealing with the function of NO in plant–fungal mutualistic associations are still scarce, experimental data indicate that different regulation patterns and functions for NO exist between plant interactions with pathogenic and mutualistic fungi. Here, we review recent progress in determining the functions of NO in plant–fungal interactions, and try to identify common and differential patterns related to pathogenic and mutualistic associations, and their impacts on plant health.

Invasions of alien plants are typically studied as invasions of individual species, yet interactions between plants and symbiotic fungi (mutualists and potential pathogens) affect plant survival, physiological traits, and reproduction and hence invasion success. Studies show that plant–fungal associations are frequently key drivers of plant invasion success and impact, but clear conceptual frameworks and integration across studies are needed to move beyond a series of case studies towards a more predictive understanding. Here, we consider linked plant–fungal invasions from the perspective of plant and fungal origin, simplified to the least complex representations or ‘motifs’. By characterizing these interaction motifs, parallels in invasion processes between pathogen and mutualist fungi become clear, although the outcomes are often opposite in effect. These interaction motifs provide hypotheses for fungal-driven dynamics behind observed plant invasion trajectories. In some situations, the effects of plant–fungal interactions are inconsistent or negligible. Variability in when and where different interaction motifs matter may be driven by specificity in the plant–fungal interaction, the size of the effect of the symbiosis (negative to positive) on plants and the dependence (obligate to facultative) of the plant−fungal interaction. Linked plant–fungal invasions can transform communities and ecosystem function, with potential for persistent legacies preventing ecosystem restoration.

Abstract Ambrosia beetles are fungal-growing insects excavating galleries deep inside the wood. Their success as invaders increased scientific interest towards them. However, most studies on their microbiota targeted their fungal associates whereas the role of bacterial associates is understudied. To explore the role of abundant microbial associates, we isolated bacteria from active galleries of two widespread ambrosia beetles, Xylosandrus crassiusculus and X. germanus. These isolates were classified within the Erwiniaceae family and through a phylogenetic analysis including isolates from other insects we showed that they clustered with isolates obtained from ambrosia and bark beetles, including Erwinia typographi. The whole genome analysis of the isolate from active galleries of X. crassiusculus suggested that this bacterium plays both a nutritional role, by providing essential amino acids and enzymes for the hydrolysis of plant biomass, and a defensive role, by producing antibiotics. This defensive role was also tested in vitro against fungi, including mutualists, common associates, and parasites. The bacteria inhibited the growth of some of the common associates and parasites but did not affect mutualists. Our study supported the hypothesis of a mutualist role of Erwiniaceae bacteria in ambrosia beetles and highlighed the importance of bacteria in maintaining the symbiosis of their host with nutritional fungi. What is the functional role of an Erwiniaceae bacterium that is part of the core microbiota of ambrosia beetles?

Sixty year ago, Charles Elton posed that species-rich communities should be more resistant to biological invasion. Still, little is known about which processes could drive the diversity–invasibility relationship. Here we examined whether soil-microbe-mediated apparent competition on alien invaders is more negative when the soil originates from multiple native species. We trained soils with five individually grown native species and used amplicon sequencing to analyze the resulting bacterial and fungal soil communities. We mixed the soils to create trained soils from one, two or four native species. We then grew four alien species separately on these differently trained soils. In the soil-conditioning phase, the five native species built species-specific bacterial and fungal communities in their rhizospheres. In the test phase, it did not matter for biomass of alien plants whether the soil had been trained by one or two native species. However, the alien species achieved 11.7% (95% CI: 3.7–20.1%) less aboveground biomass when grown on soils trained by four native species than on soils trained by two native species. Our results revealed soil-microbes-mediated apparent competition as a mechanism underlying the negative relationship between diversity and invasibility.

In nature, plant species simultaneously interact with many different mutualistic partners. These mutualists may influence one another through direct interference or indirectly by competing for shared reward resources or through alteration of plant traits. Together, these mutualists also may combine to affect plant hosts in ways that may not be predictable based on pairwise interactions. Given that the outcome of mutualistic interactions often depends on environmental conditions, multi-mutualist effects on one another, and their plant hosts may be affected by global changes. Here, we grew focal plants under simulated global warming conditions and manipulated the presence of partner mutualists to test how warming affects the outcome of interactions between focal plants and their partners (nitrogen-fixing rhizobia, ant defenders, and pollinators) and interactions among these partner mutualists. We find that warming alters the fitness benefits plants receive from rhizobium resource mutualists but not ant mutualists and that warming altered plant investment in all mutualists. We also find that mutualist partners interact, often by altering the availability of plant-produced rewards that facilitate interactions with other partners. Our work illustrates that global changes may affect some but not all mutualisms, often asymmetrically (e.g., affecting investment in the mutualist partner but not plant host benefits) and also highlights the ubiquity of interactions between the multiple mutualists associating with a shared host.

Trying to unravel Darwin's entangled bank further, we describe the architecture of a network involving multiple forms of mutualism (pollination by animals, seed dispersal by birds and plant protection by ants) and evaluate whether this multi-network shows evidence of a structure that promotes robustness. We found that species differed strongly in their contributions to the organization of the multi-interaction network, and that only a few species contributed to the structuring of these patterns. Moreover, we observed that the multi-interaction networks did not enhance community robustness compared with each of the three independent mutualistic networks when analysed across a range of simulated scenarios of species extinction. By simulating the removal of highly interacting species, we observed that, overall, these species enhance network nestedness and robustness, but decrease modularity. We discuss how the organization of interlinked mutualistic networks may be essential for the maintenance of ecological communities, and therefore the long-term ecological and evolutionary dynamics of interactive, species-rich communities. We suggest that conserving these keystone mutualists and their interactions is crucial to the persistence of species-rich mutualistic assemblages, mainly because they support other species and shape the network organization.

Background and aims: Soil inoculation is a powerful tool for the restoration of terrestrial ecosystems. However, the origin of the donor material may differentially influence early- and late-successional plant species. Donor soil from late-succession stages may benefit target plant species due to a higher abundance of soil-borne mutualists. Arable soils, on the other hand, may suppress ruderals as they support more root herbivores that preferentially attack ruderal plant species, while mid-succession soils may be intermediate in their effects on ruderals and target species performance. We hypothesized that a mixture of arable and late-succession inocula may outperform pure late-successional inocula for restoration, by promoting late-successional target plants, while simultaneously reducing ruderal species’ performance. Methods: We conducted a glasshouse experiment and tested the growth of ruderal and target plant species on pure and mixed inocula. The inocula were derived from arable fields, mid-succession grasslands and late-succession heathlands and we created a replacement series testing different pairwise mixitures for each of these inocula types (ratios: 100:0, 75:25, 50:50, 25:75, 0:100 of inoculum A and B respectively). Results: In general, we found that a higher proportion of heathland material led to a higher aboveground biomass of target plant species, while responses of ruderal species were variable. We found synergistic effects when specific inocula were mixed. In particular, a 50:50 mixture of heathland and arable soil in the inoculum led to a significant reduction in ruderal species biomass relative to the two respective pure inocula. The overall response was driven by Myosotis arvensis, since the other two ruderal species were not significantly affected. Conclusions: Mixing inocula from different successional stages can lead to synergistic effects on restoration, but this highly depends on the specific combination of inocula, the mixing ratio and plant species. This suggest that specific inocula may need to be developed in order to rapidly restore different plant communities.

Why some species become invasive while others do not remains an elusive question. It has been proposed that invasive species should depend less on mutualisms, because their spread would then be less constrained by the availability of mutualistic partners. We tested this idea with the genus Pinus, whose degree of invasiveness is known at the species level (being highly and negatively correlated with seed size), and which forms obligate mutualistic associations with ectomycorrhizal fungi (EMF). Mycorrhizal dependence is defined as the degree to which a plant needs the mycorrhizal fungi to show the maximum growth. In this regard, we use plant growth response to mycorrhizal fungi as a proxy for mycorrhizal dependence. We assessed the responsiveness of Pinus species to EMF using 1,206 contrasts published on 34 species, and matched these data with data on Pinus species invasiveness. Surprisingly, we found that species that are more invasive depend more on mutualisms (EMF). Seedling growth of species with smaller seeds benefited more from mutualisms, indicating a higher dependence. A higher reliance on EMF could be part of a strategy in which small-seeded species produce more seeds that can disperse further, and these species are likely to establish only if facilitated by mycorrhizal fungi. On the contrary, big-seeded species showed a lower dependence on EMF, which may be explained by their tolerance to stressful conditions during establishment. However, the limited dispersal of larger seeds may limit the spread of these species. We present strong evidence against a venerable belief in ecology that species that rely more on mutualisms are less prone to invade, and suggest that in certain circumstances greater reliance on mutualists can increase spread capacity.

1. Plant species can influence soil biota, which in turn can influence the relative performance of plant species. These plant-soil feedbacks (PSFs) have been hypothesized to affect many community-level dynamics including species coexistence, dominance and invasion. 2. The importance of PSFs in exotic species invasion, although widely hypothesized, has been difficult to determine because invader establishment necessarily precedes invader-mediated PSFs. Here, we combine a spatial simulation model of invasion that incorporates PSFs with a meta-analysis that synthesizes published case studies describing feedbacks between pairs of native and exotic species. 3. While our spatial model confirmed the link between positive soil feedbacks ('home' advantage) for exotic species and exotic species spread, results were dependent on the initial abundance of the exotic species and the equivalence of dispersal and life history characteristics between exotic and native species. 4. The meta-analysis of 52 native-exotic pairwise feedback comparisons in 22 studies synthesized measures of native and exotic performance in soils conditioned by native and exotic species. The analysis indicated that the growth responses of native species were often greater in soil conditioned by native species than in soil conditioned exotic species (a 'home' advantage). The growth responses of exotic species were variable and not consistently related to species soil-conditioning effects. 5. Synthesis. Overlaying empirical estimates of pairwise PSFs with spatial simulations, we conclude that the empirically measured PSFs between native and exotic plant species are often not consistent with predictions of the spread of exotic species and mono-dominance. This is particularly the case when exotic species are initially rare and share similar dispersal and average fitness characteristics with native species. However, disturbance and other processes that increase the abundance of exotic species as well as the inclusion of species dispersal and life history differences can interact with PSF effects to explain the spread of invasive species.

The ideal-weed hypothesis predicts that invasive plants should be less dependent on mutualisms. However, evidence in favor of or against this hypothesis comes mainly from observational studies. Here, we experimentally tested this hypothesis using a two-factor greenhouse experiment, comparing the seedling growth response of different Pinus species (varying in invasiveness) to ectomycorrhizal fungal inoculation. Most species showed no response until they were 6 mo old, at which point inoculation increased growth between 10 and 260% among the different species. This growth response was higher for species with lower seed mass, higher dispersal ability, higher Z score (a proxy for invasiveness) and higher number of naturalized regions, all of which correspond to higher invasiveness. Our results show that timing is a crucial factor when comparing mycorrhizal dependency of different species. Dependence on mutualistic microorganisms could be part of a strategy in which invasive species produce smaller seeds, in greater number, which can disperse further, but where seedlings are more reliant on mycorrhizas to improve access to water, nutrients, and protection from pathogens. Our results suggest that reliance on mutualisms may enhance, rather than limit, nonnative species in their ability to spread, establish, and colonize.