Global patterns and drivers of plant-soil microbe interactions.

Plant-soil feedback (PSF) is an important mechanism determining plant community dynamics and structure. Understanding the geographic patterns and drivers of PSF is essential for understanding the mechanisms underlying geographic plant diversity patterns. We compiled a large dataset containing 5969 observations of PSF from 202 studies to demonstrate the global patterns and drivers of PSF for woody and non-woody species. Overall, PSF was negative on average and was influenced by plant attributes and environmental settings. Woody species PSFs did not vary with latitude, but non-woody PSFs were more negative at higher latitudes. PSF was consistently more positive with increasing aridity for both woody and non-woody species, likely due to increased mutualistic microbes relative to soil-borne pathogens. These findings were consistent between field and greenhouse experiments, suggesting that PSF variation can be driven by soil legacies from climates. Our findings call for caution to use PSF as an explanation of the latitudinal diversity gradient and highlight that aridity can influence plant community dynamics and structure across broad scales through mediating plant-soil microbe interactions.

Coexistence of Competing Plants Under Plant-Soil Feedback.

Plant-soil feedback (PSF), the reciprocal interaction between plants and their soil environment, is a fundamental ecological process that can influence coexistence and functional structure in plant communities. Current theory establishes that PSF may enhance diversity or lead to exclusion depending on whether soil conditioning disproportionately benefits heterospecific or conspecific individuals. However, a more complete picture of the impact of PSF requires understanding how PSF interacts with competition. To that end, here we propose an integrated mathematical model combining trait-based competition and soil-explicit PSF. Contrary to the current paradigm, we find that soil conditioning that disproportionately favours conspecific individuals can promote coexistence. Additionally, we show that priority effects are common when soil-conditioning species differ in their edaphic preferences. These effects can allow species with large differences in competitive ability to coexist under certain soil conditions. Our results provide testable predictions tying community-level functional patterns in plant communities to PSF and competition.

Time-dependent interaction modification generated from plant-soil feedback.

Pairwise interactions between species can be modified by other community members, leading to emergent dynamics contingent on community composition. Despite the prevalence of such higher-order interactions, little is known about how they are linked to the timing and order of species' arrival. We generate population dynamics from a mechanistic plant-soil feedback model, then apply a general theoretical framework to show that the modification of a pairwise interaction by a third plant depends on its germination phenology. These time-dependent interaction modifications emerge from concurrent changes in plant and microbe populations and are strengthened by higher overlap between plants' associated microbiomes. The interaction between this overlap and the specificity of microbiomes further determines plant coexistence. Our framework is widely applicable to mechanisms in other systems from which similar time-dependent interaction modifications can emerge, highlighting the need to integrate temporal shifts of species interactions to predict the emergent dynamics of natural communities.

Intransitivity in plant-soil feedbacks is rare but is associated with multispecies coexistence.

Although plant-soil feedback (PSF) is being recognized as an important driver of plant recruitment, our understanding of its role in species coexistence in natural communities remains limited by the scarcity of experimental studies on multispecies assemblages. Here, we experimentally estimated PSFs affecting seedling recruitment in 10 co-occurring Mediterranean woody species. We estimated weak but significant species-specific feedback. Pairwise PSFs impose similarly strong fitness differences and stabilizing-destabilizing forces, most often impeding species coexistence. Moreover, a model of community dynamics driven exclusively by PSFs suggests that few species would coexist stably, the largest assemblage with no more than six species. Thus, PSFs alone do not suffice to explain coexistence in the studied community. A topological analysis of all subcommunities in the interaction network shows that full intransitivity (with all species involved in an intransitive loop) would be rare but it would lead to species coexistence through either stable or cyclic dynamics.

Nitrification Control by Plants and Preference for Ammonium versus Nitrate: Positive Feedbacks Increase Productivity but Undermine Resilience.

AbstractSome plants, via their action on microorganisms, control soil nitrification (i.e., the transformation of ammonium into nitrate). We model how the covariation between plant control of nitrification and preference for ammonium versus nitrate impacts ecosystem properties such as productivity, nitrogen (N) losses, and overall resilience. We show that the control of nitrification can maximize productivity by minimizing total inorganic N losses. We initially predicted that plants with an ammonium preference should achieve the highest biomass when inhibiting nitrification, and conversely that plants preferring nitrate should achieve the highest biomass by stimulating nitrification. With a parametrization derived from the Lamto savanna (Ivory Coast), we find that productivity is maximal for plants that slightly prefer ammonium and inhibit nitrification. Such situations, however, lead to strong positive feedbacks that can cause abrupt shifts from a highly to a lowly productive ecosystem. The comparison with other parameter sets (Pawnee short-grass prairie [United States], intensively cultivated field, and a hypothetical parameter set in which ammonium is highly volatilized and nitrate inputs are high) shows that strategies yielding the highest biomass may be counterintuitive (i.e., preferring nitrate but inhibiting nitrification). We argue that the level of control yielding the highest productivity depends on ecosystem properties (quantity of N deposition, leaching rates, and baseline nitrification rates), not only preference. Finally, while contrasting N preferences offer, as expected, the possibility of coexistence through niche partitioning, we stress how control of nitrification can be framed as a niche construction process that adds an additional dimension to coexistence conditions.

Root-exuded benzoxazinoids can alleviate negative plant-soil feedbacks.

Plants can suppress the growth of other plants by modifying soil properties. These negative plant-soil feedbacks are often species-specific, suggesting that some plants possess resistance strategies. However, the underlying mechanisms remain largely unknown. Here, we investigated whether benzoxazinoids, a class of dominant secondary metabolites that are exuded into the soil by maize and other cereals, allow maize plants to cope with plant-soil feedbacks. We find that three out of five tested crop species reduce maize (Zea mays L.) performance via negative plant-soil feedbacks relative to the mean across species. This effect is partially alleviated by the capacity of maize plants to produce benzoxazinoids. Soil complementation with purified benzoxazinoids restores the protective effect for benzoxazinoid-deficient mutants. Sterilization and reinoculation experiments suggest that benzoxazinoid-mediated protection acts via changes in soil biota. Substantial variation of the protective effect between experiments and soil types illustrates context dependency. In conclusion, exuded plant secondary metabolites allow plants to cope with plant-soil feedbacks. These findings expand the functional repertoire of plant secondary metabolites and reveal a mechanism by which plants can resist negative effects of soil feedbacks. The uncovered phenomenon may represent a promising avenue to stabilize plant performance in crop rotations.

A trait-based framework linking the soil metabolome to plant-soil feedbacks.

By modifying the biotic and abiotic properties of the soil, plants create soil legacies that can affect vegetation dynamics through plant-soil feedbacks (PSF). PSF are generally attributed to reciprocal effects of plants and soil biota, but these interactions can also drive changes in the identity, diversity and abundance of soil metabolites, leading to more or less persistent soil chemical legacies whose role in mediating PSF has rarely been considered. These chemical legacies may interact with microbial or nutrient legacies to affect species coexistence. Given the ecological importance of chemical interactions between plants and other organisms, a better understanding of soil chemical legacies is needed in community ecology. In this Viewpoint, we aim to: highlight the importance of belowground chemical interactions for PSF; define and integrate soil chemical legacies into PSF research by clarifying how the soil metabolome can contribute to PSF; discuss how functional traits can help predict these plant-soil interactions; propose an experimental approach to quantify plant responses to the soil solution metabolome; and describe a testable framework relying on root economics and seed dispersal traits to predict how plant species affect the soil metabolome and how they could respond to soil chemical legacies.

Joint evolution of mutualistic interactions, pollination, seed dispersal mutualism, and mycorrhizal symbiosis in trees.

Mycorrhizal symbiosis, seed dispersal, and pollination are recognized as the most prominent mutualistic interactions in terrestrial ecosystems. However, it remains unclear how these symbiotic relationships have interacted to contribute to current plant diversity. We analyzed evolutionary relationships among mycorrhizal type, seed dispersal mode, and pollination mode in two global databases of 699 (database I) and 10 475 (database II) tree species. Although database II had been estimated from phylogenetic patterns and therefore had lower certainty of the mycorrhizal type than database I, whose mycorrhizal type was determined by direct observation, database II allowed analysis of many more taxa from more regions than database I. We found evidence of joint evolution of all three features in both databases. This result is robust to the effects of both sampling bias and missing taxa. Most arbuscular mycorrhizal-associated trees had endozoochorous (biotic) seed dispersal and biotic pollination, with long dispersal distances, whereas most ectomycorrhizal-associated trees had anemochorous (abiotic) seed dispersal and wind (abiotic) pollination mode, with shorter dispersal distances. These results provide a novel scenario in mutualistic interactions, seed dispersal, pollination, and mycorrhizal symbiosis types, which have jointly evolved and shaped current tree diversity and forest ecosystem world-wide.

Can plants build their niche through modulation of soil microbial activities linked with nitrogen cycling? A test with Arabidopsis thaliana.

In natural systems, different plant species have been shown to modulate specific nitrogen (N) cycling processes so as to meet their N demand, thereby potentially influencing their own niche. This phenomenon might go beyond plant interactions with symbiotic microorganisms and affect the much less explored plant interactions with free-living microorganisms involved in soil N cycling, such as nitrifiers and denitrifiers. Here, we investigated variability in the modulation of soil nitrifying and denitrifying enzyme activities (NEA and DEA, respectively), and their ratio (NEA : DEA), across 193 Arabidopsis thaliana accessions. We studied the genetic and environmental determinants of such plant-soil interactions, and effects on plant biomass production in the next generation. We found that NEA, DEA, and NEA : DEA varied c. 30-, 15- and 60-fold, respectively, among A. thaliana genotypes and were related to genes linked with stress response, flowering, and nitrate nutrition, as well as to soil parameters at the geographic origin of the analysed genotypes. Moreover, plant-mediated N cycling activities correlated with the aboveground biomass of next-generation plants in home vs away nonautoclaved soil, suggesting a transgenerational impact of soil biotic conditioning on plant performance. Altogether, these findings suggest that nutrient-based plant niche construction may be much more widespread than previously thought.

Pseudomonas fluorescens Inoculation Enhances Salix matsudana Growth by Modifying Phyllosphere Microbiomes, Surpassing Nitrogen Fertilization.

The enhancement of plant growth by soil fertilization and microbial inoculation involves different mechanisms, particularly by altering the phyllosphere microbiome. This study investigated how nitrogen (N) fertilization, Pseudomonas fluorescens strain R124 inoculation and their combined effects influence the growth of different-aged Salix matsudana cuttings by modulating N dynamics within the phyllosphere microbiome. Results showed that P. fluorescens inoculation was significantly more effective than N fertilization alone, enhancing biomass, plant nutrient uptake, soil nutrient content and root development by 90.51%, 18.18%, 72.74% and 126.20%, respectively. Crucially, the inoculation notably shifted the beta-diversity of the phyllosphere microbial community, with K-strategy fungi enhancing plant N fixation and subsequent plant growth. Cuttings from middle-aged forests displayed more robust growth than those from young-aged, associated with a varied impact on phyllosphere fungi, notably increasing the relative abundance of Myriangiales in young (76.37%) and Capnodiales in middle-aged cuttings (42.37%), which improve phyllosphere stability and plant health. These findings highlight the effectiveness of microbial inoculation over N fertilization in promoting plant growth and provide valuable insights for the sustainable management of willow plantations at different stages of development.

Plant-soil interactions during the native and exotic range expansion of an annual plant.

Range expansions, whether they are biological invasions or climate change-mediated range shifts, may have profound ecological and evolutionary consequences for plant-soil interactions. Range-expanding plants encounter soil biota with which they have a limited coevolutionary history, especially when introduced to a new continent. Past studies have found mixed results on whether plants experience positive or negative soil feedback interactions in their novel range, and these effects often change over time. One important theoretical explanation is that plants locally adapt to the soil pathogens and mutualists in their novel range. We tested this hypothesis in Dittrichia graveolens, an annual plant that is both expanding its European native range, initially coinciding with climate warming, and rapidly invading California after human introduction. In parallel greenhouse experiments on both continents, we used plant genotypes and soils from 5 locations at the core and edge of each range to compare plant growth in soil inhabited by D. graveolens and nearby control microsites as a measure of plant-soil feedback. Plant-soil interactions were highly idiosyncratic across each range. On average, plant-soil feedbacks were more positive in the native range than in the exotic range. In line with the strongly heterogeneous pattern of soil responses along our biogeographic gradients, we found no evidence for evolutionary differentiation between plant genotypes from the core to the edge of either range. Our results suggest that the evolution of plant-soil interactions during range expansion may be more strongly driven by local evolutionary dynamics varying across the range than by large-scale biogeographic shifts.

No evidence that modification of soil microbiota by woody invader facilitates subsequent invasion by herbaceous species.

Many terrestrial ecosystems are co-invaded by multiple exotic species. The "invasional meltdown" hypothesis predicts that an initial invasive species will facilitate secondary invasions. In the plant kingdom, the potential underlying mechanisms of this hypothesis may be that modification of the soil properties by the initial invaders benefits for the subsequent exotic species invasion. In this study, we analyzed the composition of soil microbial communities and soil chemical properties from sites invaded by woody Rhus typhina, as well as uninvaded sites, to assess the impact of R. typhina invasion. Furthermore, we conducted a greenhouse experiment with multiple native-invasive pairs of herbaceous species to test whether R. typhina invasion facilitates subsequent exotic herb invasion. Our results showed that R. typhina invasion significantly altered the composition of soil fungal communities, especially pathogenic, endophytic, and arbuscular mycorrhizal fungi. However, this change in microbial composition led to neither direction nor magnitude changes in negative plant-soil feedback effects on both native and invasive species. This indicates that initial R. typhina invasion does not facilitate subsequent herb invasion, which does not support the "invasional meltdown" hypothesis. Additionally, R. typhina invasion significantly decreased soil total nitrogen and organic carbon contents, which may explain the significantly lower biomass of herbaceous roots grown in invaded soils compared with uninvaded soils. Alternately, although invasive herb growth was significantly more inhibited by soil microbiota compared with native herb growth, such inhibition cannot completely eliminate the risk of exotic herb invasion because of their innate growth advantages. Therefore, microbial biocontrol agents for plant invasion management should be combined with another approach to suppress the innate growth advantages of exotic species.

Quantifying soil microbial effects on plant species coexistence: A conceptual synthesis.

Soil microorganisms play a critical role in shaping the biodiversity dynamics of plant communities. These microbial effects can arise through direct mediation of plant fitness by pathogens and mutualists, and over the past two decades, numerous studies have shined a spotlight on the role of dynamic feedbacks between plants and soil microorganisms as key determinants of plant species coexistence. Such feedbacks occur when plants modify the composition of the soil community, which in turn affects plant performance. Stimulated by a theoretical model developed in the 1990s, a bulk of the empirical evidence for microbial controls over plant coexistence comes from experiments that quantify plant growth in soil communities that were previously conditioned by conspecific or heterospecific plants. These studies have revealed that soil microbes can generate strong negative to positive frequency-dependent dynamics among plants. Even as soil microbes have become recognized as a key player in determining plant coexistence outcomes, the past few years have seen a renewed interest in expanding the conceptual foundations of this field. New results include re-interpretations of key metrics from classic two-species models, extensions of plant-soil feedback theory to multispecies communities, and frameworks to integrate plant-soil feedbacks with processes like intra- and interspecific competition. Here, I review the implications of theoretical developments for interpreting existing empirical results and highlight proposed analyses and designs for future experiments that can enable a more complete understanding of microbial regulation of plant community dynamics.

Plant-soil microbe feedbacks depend on distance and ploidy in a mixed cytotype population of Larrea tridentata.

PREMISE: Theory predicts that mixed ploidy populations should be short-lived due to strong fitness disadvantages for the rare ploidy. However, mixed ploidy populations are common, suggesting that the fitness costs for rare ploidies are counterbalanced by ecological benefits that emerge when rare. We investigated whether differences in ecological interactions with soil microbes help to maintain a tetraploid-hexaploid population of Larrea tridentata (creosote bush) in the Sonoran Desert, California, United States, where prior work documented ploidy-specific root-associated microbes. METHODS: We used a plant-soil feedback (PSF) experiment to test whether host-specific soil microbes can alter the outcomes of intraploidy vs. interploidy competition. Host-specific soil microbes can build up over time; thus, distance from a host plant can affect the fitness of nearby plants. RESULTS: Seedlings grown in soils from near plants of a different ploidy produced greater biomass relative to seedlings grown in soils from near plants of the same ploidy. Moreover, seedlings grown in soils from near plants of a different ploidy produced more biomass than those grown in soils that were farther from plants of a different ploidy. These results suggest that the ecological consequences of PSF may facilitate the persistence of mixed ploidy populations. CONCLUSIONS: This is the first evidence, to our knowledge, that is consistent with plant-soil microbe feedback as a viable mechanism to maintain the coexistence of multiple ploidy levels in a single population.

Soil legacy effects of plants and drought on aboveground insects in native and range-expanding plant communities.

Soils contain biotic and abiotic legacies of previous conditions that may influence plant community biomass and associated aboveground biodiversity. However, little is known about the relative strengths and interactions of the various belowground legacies on aboveground plant-insect interactions. We used an outdoor mesocosm experiment to investigate the belowground legacy effects of range-expanding versus native plants, extreme drought and their interactions on plants, aphids and pollinators. We show that plant biomass was influenced more strongly by the previous plant community than by the previous summer drought. Plant communities consisted of four congeneric pairs of natives and range expanders, and their responses were not unanimous. Legacy effects affected the abundance of aphids more strongly than pollinators. We conclude that legacies can be contained as soil 'memories' that influence aboveground plant community interactions in the next growing season. These soil-borne 'memories' can be altered by climate warming-induced plant range shifts and extreme drought.

Allelochemicals and soil microorganisms jointly mediate sex-specific belowground interactions in dioecious Populus cathayana.

Little is known about how sex differences in root zone characteristics, such as contents of allelochemicals and soil microbial composition, mediate intra- and intersexual interactions in dioecious plants. We examined the processes and mechanisms of sex-specific belowground interactions mediated by allelochemicals and soil microorganisms in Populus cathayana females and males in replicated 30-yr-old experimental stands in situ and in a series of controlled experiments. Female roots released a greater amount and more diverse phenolic allelochemicals into the soil environment, resulting in growth inhibition of the same sex neighbors and deterioration of the community of soil microorganisms. When grown with males, the growth of females was consistently enhanced, especially the root growth. Compared with female monocultures, the presence of males reduced the total phenolic accumulation in the soil, resulting in a shift from allelopathic inhibition to chemical facilitation. This association was enhanced by a favorable soil bacterial community and increased bacterial diversity, and it induced changes in the orientation of female roots. Our study highlighted a novel mechanism that enhances female performance by males through alterations in the allelochemical content and soil microbial composition. The possibility to improve productivity by chemical mediation provides novel opportunities for managing plantations of dioecious plants.

Aboveground herbivory can promote exotic plant invasion through intra- and interspecific aboveground-belowground interactions.

Aboveground herbivores and soil biota profoundly affect plant invasions. However, how they interactively affect plant invasions through plant-soil feedbacks (PSFs) remains unclear. To explore how herbivory by the introduced beetle Agasicles hygrophila affects Alternanthera philoxeroides invasions in China, we integrated multiyear field surveys and a 2-yr PSF experiment, in which we examined how herbivory affects PSFs on the performance of native and invasive plants and the introduced beetles. Despite increased herbivory from A. hygrophila, A. philoxeroides dominance over co-occurring congeneric native Alternanthera sessilis remained constant from 2014 to 2019. While occurring at lower abundances, A. sessilis experienced similar herbivore damage, suggesting apparent competitive effects. Our experiments revealed that herbivory on A. philoxeroides altered soil microbial communities, prolonged its negative PSF on A. sessilis, and decreased A. hygrophila larvae performance on the next-generation invasive plants. Consequently, A. hygrophila larvae performed better on leaves of natives than those of invasives when grown in soils conditioned by invasive plants defoliated by the introduced beetles. Our findings suggest that aboveground herbivory might promote rather than suppress A. philoxeroides invasion by enhancing its soil-mediated self-reinforcement, providing a novel mechanistic understanding of plant invasions. These findings highlight the need to incorporate an aboveground-belowground perspective during the assessment of potential biocontrol agents.

Soil fertility determines whether ectomycorrhizal fungi accelerate or decelerate decomposition in a temperate forest.

Ectomycorrhizal (ECM) fungi can both accelerate and decelerate decomposition of organic matter in forest soils, but a mechanistic understanding of this differential influence is limited. Here, we tested how ECM fungi affect decomposition along a natural fertility gradient in a temperate forest of European beech. Trees were girdled to reduce belowground carbon supply to the soil. Girdling shifted soil fungal community composition and decreased hyphal biomass production and soil CO2 efflux, indicating a reduced ECM fungal activity. Girdling also affected decomposition processes, but the effects depended on fertility. Our results indicate that ECM fungi decelerate decomposition under conditions of low fertility while under conditions of high fertility ECM fungi and their host roots have an accelerating effect. We conclude that both acceleration and deceleration of decomposition of organic matter by ECM fungi can occur within a forest, with soil fertility determining the direction and magnitude of these effects. We suggest a positive feedback between fertility, stand productivity and soil carbon and nitrogen dynamics that is mediated to a large extent by ECM fungi.

The rhizosphere microbiome and host plant glucosinolates exhibit feedback cycles in Brassica rapa.

The rhizosphere microbiome influences many aspects of plant fitness, including production of secondary compounds and defence against insect herbivores. Plants also modulate the composition of the microbial community in the rhizosphere via secretion of root exudates. We tested both the effect of the rhizosphere microbiome on plant traits, and host plant effects on rhizosphere microbes using recombinant inbred lines (RILs) of Brassica rapa that differ in production of glucosinolates (GLS), secondary metabolites that contribute to defence against insect herbivores. First, we investigated the effect of genetic variation in GLS production on the composition of the rhizosphere microbiome. Using a Bayesian Dirichlet-multinomial regression model (DMBVS), we identified both negative and positive associations between bacteria from six genera and the concentration of five GLS compounds produced in plant roots. Additionally, we tested the effects of microbial inoculation (an intact vs. disrupted soil microbiome) on GLS production and insect damage in these RILs. We found a significant microbial treatment × genotype interaction, in which total GLS was higher in the intact relative to the disrupted microbiome treatment in some RILs. However, despite differences in GLS production between microbial treatments, we observed no difference in insect damage between treatments. Together, these results provide evidence for a full feedback cycle of plant-microbe interactions mediated by GLS; that is, GLS compounds produced by the host plant "feed-down" to influence rhizosphere microbial community and rhizosphere microbes "feed-up" to influence GLS production.

Core arbuscular mycorrhizal fungi are predicted by their high abundance-occupancy relationship while host-specific taxa are rare and geographically structured.

Habitat restoration may depend on the recovery of plant microbial symbionts such as arbuscular mycorrhizal (AM) fungi, but this requires a better understanding of the rules that govern their community assembly. We examined the interactions of soil and host-associated AM fungal communities between remnant and restored patches of subtropical montane forests. While AM fungal richness did not differ between habitat types, community membership did and was influenced by geography, habitat and host. These differences were largely driven by rare host-specific AM fungi that displayed near-complete turnover between forest types, while core AM fungal taxa were highly abundant and ubiquitous. The bipartite networks in the remnant forest were more specialized and hosts more specific than in the restored forest. Host-associated AM fungal communities nested within soil communities in both habitats, but only significantly so in the restored forest. Our results provide evidence that restored and remnant forests harbour the same core fungal symbionts, while rare host-specific taxa differ, and that geography, host identity and taxonomic resolution strongly affect the observed distribution patterns of these fungi. We suggest that host-specific interactions with AM fungi, as well as spatial processes, should be explicitly considered to effectively re-establish target host and symbiont communities.