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Abstract Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination.We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs.We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host‐specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host‐specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs.Synthesis. Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host‐specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe‐mediated interactions between plants at different life stages that next‐generation sequencing can begin to unravel.
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Global patterns and drivers of plant–soil microbe interactions
Abstract 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.
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- Award ID(s):
- 1754287
- PAR ID:
- 10525873
- Publisher / Repository:
- Ecology Letters
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 27
- Issue:
- 1
- ISSN:
- 1461-023X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Although plant–soil feedbacks (interactions between plants and soils, often mediated by soil microbes, abbreviated as PSFs) are widely known to influence patterns of plant diversity at local and landscape scales, these interactions are rarely examined in the context of important environmental factors. Resolving the roles of environmental factors is important because the environmental context may alter PSF patterns by modifying the strength or even direction of PSFs for certain species. One important environmental factor that is increasing in scale and frequency with climate change is fire, though the influence of fire on PSFs remains essentially unexamined. By changing microbial community composition, fire may alter the microbes available to colonize the roots of plants and thus seedling growth post‐fire. This has potential to change the strength and/or direction of PSFs, depending on how such changes in microbial community composition occur and the plant species with which the microbes interact. We examined how a recent fire altered PSFs of two leguminous, nitrogen‐fixing tree species in Hawaiʻi. For both species, growing in conspecific soil resulted in higher plant performance (as measured by biomass production) than growing in heterospecific soil. This pattern was mediated by nodule formation, an important process for growth for legume species. Fire weakened PSFs for these species and therefore pairwise PSFs, which were significant in unburned soils, but were nonsignificant in burned soils. Theory suggests that positive PSFs such as those found in unburned sites would reinforce the dominance of species where they are locally dominant. The change in pairwise PSFs with burn status shows PSF‐mediated dominance might diminish after fire. Our results demonstrate that fire can modify PSFs by weakening the legume‐rhizobia symbiosis, which may alter local competitive dynamics between two canopy dominant tree species. These findings illustrate the importance of considering environmental context when evaluating the role of PSFs for plants.more » « less
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Abstract Mounting evidence suggests that plant–soil feedbacks (PSF) may determine plant community structure. However, we still have a poor understanding of how predictions from short‐term PSF experiments compare with outcomes of long‐term field experiments involving competing plants. We conducted a reciprocal greenhouse experiment to examine how the growth of prairie grass species depended on the soil communities cultured by conspecific or heterospecific plant species in the field. The source soil came from monocultures in a long‐term competition experiment (LTCE; Cedar Creek Ecosystem Science Reserve, MN, USA). Within the LTCE, six species of perennial prairie grasses were grown in monocultures or in eight pairwise competition plots for 12 years under conditions of low or high soil nitrogen availability. In six cases, one species clearly excluded the other; in two cases, the pair appeared to coexist. In year 15, we gathered soil from all 12 soil types (monocultures of six species by two nitrogen levels) and grew seedlings of all six species in each soil type for 7 weeks. Using biomass estimates from this greenhouse experiment, we predicted coexistence or competitive exclusion using pairwise PSFs, as derived by Bever and colleagues, and compared model predictions to observed outcomes within the LTCE. Pairwise PSFs among the species pairs ranged from negative, which is predicted to promote coexistence, to positive, which is predicted to promote competitive exclusion. However, these short‐term PSF predictions bore no systematic resemblance to the actual outcomes of competition observed in the LTCE. Other forces may have more strongly influenced the competitive interactions or critical assumptions that underlie the PSF predictions may not have been met. Importantly, the pairwise PSF score derived by Bever et al. is only valid when the two species exhibit an internal equilibrium, corresponding to the Lotka–Volterra competition outcomes of stable coexistence and founder control. Predicting the other two scenarios, competitive exclusion by either species irrespective of initial conditions, requires measuring biomass in uncultured soil, which is methodologically challenging. Subject to several caveats that we discuss, our results call into question whether long‐term competitive outcomes in the field can be predicted from the results of short‐term PSF experiments.more » « less
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Abstract Although diversity‐dependent plant–soil feedbacks (PSFs) may contribute significantly to plant diversity effects on ecosystem functioning, the influences of underlying abiotic and biotic mechanistic pathways have been little explored to date. Here, we assessed such pathways with a PSF experiment using soil conditioned for ≥12 yr from two grassland biodiversity experiments. Model plant communities differing in plant species and functional group richness (current plant diversity treatment) were grown in soils conditioned by plant communities with either low‐ or high‐diversity (soil history treatment). Our results indicate that plant diversity can modify plant productivity through both diversity‐mediated plant–plant and plant–soil interactions, with the main driver (current plant diversity or soil history) differing with experimental context. Structural equation modeling suggests that the underlying mechanisms of PSFs were explained to a significant extent by both abiotic and biotic pathways (specifically, soil nitrogen availability and soil nematode richness). Thus, effects of plant diversity loss on plant productivity may persist or even increase over time because of biotic and abiotic soil legacy effects.more » « less
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Abstract AimNitrogen (N)‐fixing plants are an important component of global plant communities, but the drivers of N‐fixing plant diversity, especially in temperate regions, remain underexplored. Here, we examined broad‐scale patterns of N‐fixing and non‐fixing plant phylogenetic diversity (PD) and species richness (SR) across a wide portion of temperate North America, focusing on relationships with soil N and aridity. We also tested whether exotic species, with and without N‐fixing symbiosis, have fewer abiotic limitations compared with native species. LocationUSA and Puerto Rico. Time periodCurrent. Major taxa studiedVascular plants, focusing on N‐fixing groups (orders Fabales, Fagales, Rosales and Cucurbitales). MethodsWe subset National Ecological Observatory Network (NEON) plant plot data from all sites along two axes (N fixing–non‐N fixing and native–exotic), calculating plot‐level SR, PD and mean pairwise phylogenetic distance (MPD). We then used linear mixed models to investigate relationships between diversity values and key soil measurements, along with aridity, temperature and fire frequency. ResultsAridity was the sole predictor of proportional phylogenetic diversity of N fixers. The SR of N fixers still decreased marginally in arid regions, whereas native N‐fixer MPD increased with aridity, indicative of unique lineages of N fixers in the driest conditions, in contrast to native non‐N fixers. The SR of both native N fixers and non‐N fixers increased in low‐N soils. Aridity did not affect SR of exotic non‐N fixers, unlike other groups, whereas exotic N fixers showed lower MPD in increasingly high‐N soils, suggesting filtering, contrary what was found for native N fixers. Main conclusionsOur results suggest that it is not nitrogen, or any soil nutrient, that has the strongest effect on the relative success of N fixers in plant communities. Rather, aridity is the key driver, at least for native species, in line with empirical results from other biomes and increased understanding of N fixation as a key mechanism to avoid water loss.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/ele.14364
