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.

Corrigendum: Microbiome variation across populations of desert halophyte Zygophyllum qatarensis.

[This corrects the article DOI: 10.3389/fpls.2022.841217.].

Causes and consequences of differences in soil and seed microbiomes for two alpine plants.

Seed and soil microbiomes strongly affect plant performance, and these effects can scale-up to influence plant community structure. However, seed and soil microbial community composition are variable across landscapes, and different microbial communities can differentially influence multiple plant metrics (biomass, germination rate), and community stabilizing mechanisms. We determined how microbiomes inside seeds and in soils varied among alpine plant species and communities that differed in plant species richness and density. Across 10 common alpine plant species, we found a total of 318 bacterial and 128 fungal operational taxonomic units (OTUs) associated with seeds, with fungal richness affected by plant species identity more than sampling location. However, seed microbes had only marginally significant effects on plant germination success and timing. In contrast, soil microbes associated with two different plant species had significant effects on plant biomass, and their effect depended both on the plant species and the location the soils were sampled from. This led to significant changes in plant-soil feedback at different locations that varied in plant density and richness, such that plant-soil feedback favored plant species coexistence in some locations and opposed coexistence at other locations. Importantly, we found that coexistence-facilitating feedback was associated with low plant species richness, suggesting that soil microbes may promote the diversity of colonizing plants during the course of climate change and glacial recession.

Microbiome Variation Across Populations of Desert Halophyte Zygophyllum qatarensis.

Microbial symbionts play a significant role in plant health and stress tolerance. However, few studies exist that address rare species of core-microbiome function during abiotic stress. In the current study, we compared the microbiome composition of succulent dwarf shrub halophyte Zygophyllum qatarensis Hadidi across desert populations. The results showed that rhizospheric and endosphere microbiome greatly varied due to soil texture (sandy and gravel). No specific bacterial amplicon sequence variants were observed in the core-microbiome of bulk soil and rhizosphere, however, bacterial genus Alcaligenes and fungal genus Acidea were abundantly distributed across root and shoot endospheres. We also analyzed major nutrients such as silicon (Si), magnesium, and calcium across different soil textures and Z. qatarensis populations. The results showed that the rhizosphere and root parts had significantly higher Si content than the bulk soil and shoot parts. The microbiome variation can be attributed to markedly higher Si - suggesting that selective microbes are contributing to the translocation of soluble Si to root. In conclusion, low core-microbiome species abundance might be due to the harsh growing conditions in the desert - making Z. qatarensis highly selective to associate with microbial communities. Utilizing rare microbial players from plant microbiomes may be vital for increasing crop stress tolerance and productivity during stresses.

Changes in precipitation patterns can destabilize plant species coexistence via changes in plant-soil feedback.

Climate change can alter species coexistence through changes in biotic interactions. By describing reciprocal interactions between plants and soil microbes, plant-soil feedback (PSF) has emerged as a powerful framework for predicting plant species coexistence and community dynamics, but little is known about how PSF will respond to changing climate conditions. Hence, the context dependency of PSF has recently gained attention. Water availability is a major driver of all biotic interactions, and it is expected that precipitation patterns will change with ongoing climate change. We tested how soil water content affects PSF by conducting a full factorial pairwise PSF experiment using eight plant species common to southeastern United States coastal prairies under three watering treatments. We found coexistence-stabilizing negative PSF at drier-than-average conditions shifted to coexistence-destabilizing positive PSF under wetter-than-average conditions. A simulation model parameterized with the experimental results supports the prediction that more positive PSF accelerates the erosion of diversity within communities while decreasing the predictability in plant community composition. Our results underline the importance of considering environmental context dependency of PSF in light of a rapidly changing climate.

Native soil amendments combined with commercial arbuscular mycorrhizal fungi increase biomass of Panicum amarum.

Coastal dune restorations often fail because of poorly performing plants. The addition of beneficial microbes can improve plant performance, though it is unclear if the source of microbes matters. Here, we tested how native soil amendments and commercially available arbuscular mycorrhizal (AM) fungi influenced performance of Panicum amarum, a dominant grass on Texas coastal dunes. In a greenhouse experiment, we manipulated the identity of native soil amendments (from P. amarum, Uniola paniculata, or unvegetated areas), the presence of soil microbes in the native soil amendments (live or sterile), and the presence of the commercial AM fungi (present or absent). Native soils from vegetated areas contained 149% more AM fungal spores than unvegetated areas. The commercial AM fungi, when combined with previously vegetated native soils, increased aboveground biomass of P. amarum by 26%. Effects on belowground biomass were weaker, although the addition of any microbes decreased the root:shoot ratio. The origin of native soil amendments can influence restoration outcomes. In this case soil from areas with vegetation outperformed soil from areas without vegetation. Combining native soils with commercial AM fungi may provide a strategy for increasing plant performance while also maintaining other ecosystem functions provided by native microbes.

Plant genotypic diversity effects on soil nematodes vary with trophic level.

At local spatial scales, loss of genetic diversity within species can lead to species loss. Few studies, however, have examined plant genotypic diversity effects across trophic levels. We investigated genotypic diversity effects of Phragmites australis on belowground biomass and soil nematode communities. Our results revealed that belowground plant biomass and nematode abundance responses to plant genotypic diversity were uncoupled. Decreasing plant genotypic diversity decreased the abundance of lower, but not higher trophic level nematodes. Low plant genotypic diversity also decreased the structural footprint and functional indices of nematodes, indicating lowered metabolic functioning of higher trophic level nematodes and decreased soil food web stability. Our study suggests that plant genotypic diversity effects differ across trophic levels, taxonomic groups and ecosystem functions and that decreasing plant genotypic diversity could destabilise belowground food webs. This highlights the importance of conserving intraspecific plant diversity.

Soil precipitation legacies influence intraspecific plant-soil feedback.

Feedbacks between plants and soil microbial communities can play an important role in structuring plant communities. However, little is known about how soil legacies caused by environmental disturbances such as drought and extreme precipitation events may affect plant-soil feedback or whether plant-soil feedback operates within species as it does between species. If soil legacies alter plant-soil feedback among genotypes within a plant species, then soil legacies may alter the diversity within plant populations. We conducted a fully factorial pairwise plant-soil feedback experiment to test how precipitation legacies influenced intraspecific plant-soil feedbacks among three genotypes of a dominant grass species, Panicum virgatum. Panicum virgatum experienced negative intraspecific plant-soil feedback, i.e., genotypes generally performed worse on soil from the same genotype than different genotypes. Soil precipitation legacies reversed the rank order of the strength of negative feedback among the genotypes. Feedback is often positively correlated with plant relative abundance. Therefore, our results suggest that soil precipitation legacies may alter the genotypic composition of P. virgatum populations, favoring genotypes that develop less negative feedback. Changes in intraspecific diversity will likely further affect community structure and ecosystem functioning, and may constrain the ability of populations to respond to future changes in climate.

When and where plant-soil feedback may promote plant coexistence: a meta-analysis.

Plant-soil feedback (PSF) theory provides a powerful framework for understanding plant dynamics by integrating growth assays into predictions of whether soil communities stabilise plant-plant interactions. However, we lack a comprehensive view of the likelihood of feedback-driven coexistence, partly because of a failure to analyse pairwise PSF, the metric directly linked to plant species coexistence. Here, we determine the relative importance of plant evolutionary history, traits, and environmental factors for coexistence through PSF using a meta-analysis of 1038 pairwise PSF measures. Consistent with eco-evolutionary predictions, feedback is more likely to mediate coexistence for pairs of plant species (1) associating with similar guilds of mycorrhizal fungi, (2) of increasing phylogenetic distance, and (3) interacting with native microbes. We also found evidence for a primary role of pathogens in feedback-mediated coexistence. By combining results over several independent studies, our results confirm that PSF may play a key role in plant species coexistence, species invasion, and the phylogenetic diversification of plant communities.

Genetic mixture of multiple source populations accelerates invasive range expansion.

A wealth of population genetic studies have documented that many successful biological invasions stem from multiple introductions from genetically distinct source populations. Yet, mechanistic understanding of whether and how genetic mixture promotes invasiveness has lagged behind documentation that such mixture commonly occurs. We conducted a laboratory experiment to test the influence of genetic mixture on the velocity of invasive range expansion. The mechanistic basis for effects of genetic mixture could include evolutionary responses (mixed invasions may harbour greater genetic diversity and thus elevated evolutionary potential) and/or fitness advantages of between-population mating (heterosis). If driven by evolution, positive effects of source population mixture should increase through time, as selection sculpts genetic variation. If driven by heterosis, effects of mixture should peak following first reproductive contact and then dissipate. Using a laboratory model system (beetles spreading through artificial landscapes), we quantified the velocity of range expansion for invasions initiated with one, two, four or six genetic sources over six generations. Our experiment was designed to test predictions corresponding to the evolutionary and heterosis mechanisms, asking whether any effects of genetic mixture occurred in early or later generations of range expansion. We also quantified demography and dispersal for each experimental treatment, since any effects of mixture should be manifest in one or both of these traits. Over six generations, invasions with any amount of genetic mixture (two, four and six sources) spread farther than single-source invasions. Our data suggest that heterosis provided a 'catapult effect', leaving a lasting signature on range expansion even though the benefits of outcrossing were transient. Individual-level trait data indicated that genetic mixture had positive effects on local demography (reduced extinction risk and enhanced population growth) during the initial stages of invasion but no consistent effects on dispersal ability. Our work is the first to demonstrate that genetic mixture can alter the course of spatial expansion, the stage of invasion typically associated with the greatest ecological and economic impacts. We suggest that similar effects of genetic mixture may be a common feature of biological invasions in nature, but that these effects can easily go undetected.

Genetic variation in resistance to leaf fungus indirectly affects spider density.

Many host-plants exhibit genetic variation in resistance to pathogens; however, little is known about the extent to which genetic variation in pathogen resistance influences other members of the host-plant community, especially arthropods at higher trophic levels. We addressed this knowledge gap by using a common garden experiment to examine whether genotypes of Populus trichocarpa varied in resistance to a leaf-blistering pathogen, Taphrina sp., and in the density of web-building spiders, the dominant group of predatory arthropods. In addition, we examined whether variation in spider density was explained by variation in the density and size of leaf blisters caused by Taphrina. We found that P. trichocarpa genotypes exhibited strong differences in their resistance to Taphrina and that P. trichocarpa genotypes that were more susceptible to Taphrina supported more web-building spiders, the dominant group of predatory arthropods. We suspect that this result is caused by blisters increasing the availability of suitable habitat for predators, and not due to variation in herbivores because including herbivore density as a covariate did not affect our models. Our study highlights a novel pathway by which genetic variation in pathogen resistance may affect higher trophic levels in arthropod communities.

Competition overwhelms the positive plant-soil feedback generated by an invasive plant.

Invasive plant species can modify soils in a way that benefits their fitness more than the fitness of native species. However, it is unclear how competition among plant species alters the strength and direction of plant-soil feedbacks. We tested how community context altered plant-soil feedback between the non-native invasive forb Lespedeza cuneata and nine co-occurring native prairie species. In a series of greenhouse experiments, we grew plants individually and in communities with soils that differed in soil origin (invaded or uninvaded by L. cuneata) and in soils that were live vs. sterilized. In the absence of competition, L. cuneata produced over 60% more biomass in invaded than uninvaded soils, while native species performance was unaffected. The absence of a soil origin effect in sterile soil suggests that the positive plant-soil feedback was caused by differences in the soil biota. However, in the presence of competition, the positive effect of soil origin on L. cuneata growth disappeared. These results suggest that L. cuneata may benefit from positive plant-soil feedback when establishing populations in disturbed landscapes with few interspecific competitors, but does not support the hypothesis that plant-soil feedbacks influence competitive outcomes between L. cuneata and native plant species. These results highlight the importance of considering whether competition influences the outcome of interactions between plants and soils.

Local and latitudinal variation in abundance: the mechanisms shaping the distribution of an ecosystem engineer.

Ecological processes that determine the abundance of species within ecological communities vary across space and time. These scale-dependent processes are especially important when they affect key members of a community, such as ecosystem engineers that create shelter and food resources for other species. Yet, few studies have examined the suite of processes that shape the abundance of ecosystem engineers. Here, we evaluated the relative influence of temporal variation, local processes, and latitude on the abundance of an engineering insect-a rosette-galling midge, Rhopalomyia solidaginis (Diptera: Cecidomyiidae). Over a period of 3-5 years, we studied the density and size of galls across a suite of local experiments that manipulated genetic variation, soil nutrient availability, and the removal of other insects from the host plant, Solidago altissima (tall goldenrod). We also surveyed gall density within a single growing season across a 2,300 km latitudinal transect of goldenrod populations in the eastern United States. At the local scale, we found that host-plant genotypic variation was the best predictor of rosette gall density and size within a single year. We found that the removal of other insect herbivores resulted in an increase in gall density and size. The amendment of soil nutrients for four years had no effect on gall density, but galls were smaller in carbon-added plots compared to control and nitrogen additions. Finally, we observed that gall density varied several fold across years. At the biogeographic scale, we observed that the density of rosette gallers peaked at mid-latitudes. Using meta-analytic approaches, we found that the effect size of time, followed by host-plant genetic variation and latitude were the best predictors of gall density. Taken together, our study provides a unique comparison of multiple factors across different spatial and temporal scales that govern engineering insect herbivore density.

Genetic diversity within a dominant plant outweighs plant species diversity in structuring an arthropod community.

Plant biodiversity is being lost at a rapid rate. This has spurred much interest in elucidating the consequences of this loss for higher trophic levels. Experimental tests have shown that both plant species diversity and genetic diversity within a plant species can influence arthropod community structure. However, the majority of these studies have been conducted in separate systems, so their relative importance is currently unresolved. Furthermore, potential interactions between the two levels of diversity, which likely occur in natural systems, have not been investigated. To clarify these issues, we conducted three experiments in a freshwater sand dune ecosystem. We (1) independently manipulated plant species diversity, (2) independently manipulated genetic diversity within the dominant plant species, Ammophila breviligulata, and (3) jointly manipulated genetic diversity within the dominant plant and species diversity. We found that genetic diversity within the dominant plant species, Ammophila breviligulata, more strongly influenced arthropod communities than plant species diversity, but this effect was dependent on the presence of other species. In species mixtures, A. breviligulata genetic diversity altered overall arthropod community composition, and arthropod richness and abundance peaked at the highest level of genetic diversity. Positive nonadditive effects of diversity were detected, suggesting that arthropods respond to emergent properties of diverse plant communities. However, in the independent manipulations where A. breviligulata was alone, effects of genetic diversity were weaker, with only arthropod richness responding. In contrast, plant species diversity only influenced arthropods when A. breviligulata was absent, and then only influenced herbivore abundance. In addition to showing that genetic diversity within a dominant plant species can have large effects on arthropod community composition, these results suggest that understanding how species diversity and genetic diversity interact to influence community structure may be critically important for predicting the consequences of biodiversity loss.

Fungal endophytes of native grasses decrease insect herbivore preference and performance.

Endophytic fungal symbionts of grasses are well known for their protective benefit of herbivory reduction. However, the majority of studies on endophyte-grass symbioses have been conducted on economically important, agricultural species-particularly tall fescue (Lolium arundinaceum) and perennial ryegrass (Lolium perenne)-raising the hypothesis that strong benefits are the product of artificial selection. We examined whether fungal endophytes found in natural populations of native grass species deterred insect herbivores. By testing several native grass-endophyte symbiota, we examined phylogenetic signals in the effects of endophytes on insects and compared the relative importance of herbivore and symbiotum identity in the outcome of the interactions. Preference was assessed using three herbivore species [Spodoptera frugiperda (Lepidoptera), Schistocerca americana (Orthoptera), Rhopalosiphum padi (Hemiptera)] and ten native symbiota, which spanned seven grass genera. We also assessed herbivore performance in a no choice experiment for five native symbiota against S. frugiperda. We compared greenhouse and laboratory trials with natural levels of herbivory measured in experimental field populations. In all cases, we included the agronomic grass species, L. arundinaceum, to compare with results from the native grasses. Both in the field and in experimental trials, herbivores showed a significant preference for endophyte-free plant material for the majority of native grasses, with up to three times lower herbivory for endophyte-symbiotic plants; however, the degree of response depended on the identity of the herbivore species. Endophyte presence also significantly reduced performance of S. frugiperda for the majority of grass species. In contrast, the endophyte in L. arundinaceum had few significant anti-herbivore effects, except for a reduction in herbivory at one of two field sites. Our results demonstrate that the mechanisms by which native symbionts deter herbivores are at least as potent as those in model agricultural systems, despite the absence of artificial selection.

Host-plant genotypic diversity mediates the distribution of an ecosystem engineer.

Ecosystem engineers affect ecological communities by physically modifying the environment. Understanding the factors determining the distribution of engineers offers a powerful predictive tool for community ecology. In this study, we examine whether the goldenrod bunch gall midge (Rhopalomyia solidaginis) functions as an ecosystem engineer in an old-field ecosystem by altering the composition of arthropod species associated with a dominant host plant, Solidago altissima. We also examine the suite of factors that could affect the distribution and abundance of this ecosystem engineer. The presence of bunch galls increased species richness and altered the structure of associated arthropod communities. The best predictors of gall abundance were host-plant genotype and plot-level genotypic diversity. We found positive, nonadditive effects of genotypic diversity on gall abundance. Our results indicate that incorporating a genetic component in studies of ecosystem engineers can help predict their distribution and abundance, and ultimately their effects on biodiversity.