Intraspecific plant–soil feedback and intraspecific overyielding in Arabidopsis thaliana

Understanding the mechanisms of community coexistence and ecosystem functioning may help to counteract the current biodiversity loss and its potentially harmful consequences. In recent years, plant–soil feedback that can, for example, be caused by below‐ground microorganisms has been suggested to play a role in maintaining plant coexistence and to be a potential driver of the positive relationship between plant diversity and ecosystem functioning. Most of the studies addressing these topics have focused on the species level. However, in addition to interspecific interactions, intraspecific interactions might be important for the structure of natural communities. Here, we examine intraspecific coexistence and intraspecific diversity effects using 10 natural accessions of the model species Arabidopsis thaliana (L.) Heynh. We assessed morphological intraspecific diversity by measuring several above‐ and below‐ground traits. We performed a plant–soil feedback experiment that was based on these trait differences between the accessions in order to determine whether A. thaliana experiences feedback at intraspecific level as a result of trait differences. We also experimentally tested the diversity–productivity relationship at intraspecific level. We found strong differences in above‐ and below‐ground traits between the A. thaliana accessions. Overall, plant–soil feedback occurred at intraspecific level. However, accessions differed in the direction and strength of this feedback: Some accessions grew better on their own soils, some on soils from other accessions. Furthermore, we found positive diversity effects within A. thaliana: Accession mixtures produced a higher total above‐ground biomass than accession monocultures. Differences between accessions in their feedback response could not be explained by morphological traits. Therefore, we suggest that they might have been caused by accession‐specific accumulated soil communities, by root exudates, or by accession‐specific resource use based on genetic differences that are not expressed in morphological traits. Synthesis. Our results provide some of the first evidence for intraspecific plant–soil feedback and intraspecific overyielding. These findings may have wider implications for the maintenance of variation within species and the importance of this variation for ecosystem functioning. Our results highlight the need for an increased focus on intraspecific processes in plant diversity research to fully understand the mechanisms of coexistence and ecosystem functioning.     

Current plant diversity but not its soil legacy influences exotic plant invasion

植物多样性而非其土壤遗留效应影响外来植物入侵 植物多样性可以影响外来植物入侵,然而植物多样性的土壤遗留效应是否能够影响外来植物入侵目前仍不清楚。植物多样性能够改变土壤微生物群落和土壤理化性质,这种遗留效应可能会对该土壤中外来植物的生长产生影响。因此,我们假设植物多样性的土壤遗留效应会影响外来植物的入侵。为了检验该假说,我们开展了一个两阶段的植物-土壤反馈实验。在土壤驯化阶段,我们将12个植物物种(4种禾草植物、3种豆科植物和5种杂类草植物)分别单独种植,或者随机选择8个物种(包含3个功能型)混合种植在土壤中。在反馈阶段,我们将入侵植物三叶鬼针草(Bidens pilosa)分别与本地禾草荩草(Arthraxon hispidus)、本地杂类草翅果菊(Pterocypsela indica)或者同时与荩草和翅果菊种植在被驯化过的土壤中。研 究结果显示,三叶鬼针草相对于其本地竞争植物的生长取决于驯化植物和竞争植物物种的功能型。驯化植物的多样性对三叶鬼针草与其本地竞争植物之间的生长差异没有显著影响。然而,随着本地竞争植物物种多样性的增加,三叶鬼针草相对于其本地竞争植物的生长显著降低。这些结果表明,当前的植物多样性可以通过增加入侵植物和本地植物之间的生长不平衡性来减少外来植物的入侵。但是,植物多样性的土壤遗留效应对外来植物入侵的影响可能很小。     

Predators in the plant–soil feedback loop: aboveground plant‐associated predators may alter the outcome of plant–soil interactions

Plant–soil feedback (PSF) can structure plant communities, promoting coexistence (negative PSF) or monodominance (positive PSF). At higher trophic levels, predators can alter plant community structure by re‐allocating resources within habitats. When predator and plant species are spatially associated, predators may alter the outcome of PSF. Here, I explore the influence of plant‐associated predators on PSF using a generalised cellular automaton model that tracks nutrients, plants, herbivores and predators. I explore key contingencies in plant–predator associations such as whether predators associate with live vs. senesced vegetation. Results indicate that plant‐associated predators shift PSF to favour the host plant when predators colonise live vegetation, but the outcome of PSF will depend upon plant dispersal distance when predators colonise dead vegetation. I apply the model to two spider‐associated invasive plants, finding that spider predators should shift PSF dynamics in a way that inhibits invasion by one forest invader, but exacerbates invasion by another.     

Relative importance of competition and plant–soil feedback,their synergy,context dependency and implications for coexistence

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant–soil feedback (PSF) on plant performance is poorly understood. Using a meta‐analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter‐ vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide‐treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter‐ to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low‐resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.     

Geographic mosaics of plant–soil microbe interactions in a global plant invasion

Aim Our aim in this study was to document the global biogeographic variation in the effects of soil microbes on the growth of Centaurea solstitialis (yellow starthistle; Asteraceae), a species that has been introduced throughout the world, but has become highly invasive only in some introduced regions. Location  To assess biogeographic variation in plant–soil microbe interactions, we collected seeds and soils from native Eurasian C. solstitialis populations and introduced populations in California, Argentina and Chile. Methods To test whether escape from soil‐borne natural enemies may contribute to the success of C. solstitialis, we compared the performance of plants using seeds and soils collected from each of the biogeographic regions in greenhouse inoculation/sterilization experiments. Results  We found that soil microbes had pervasive negative effects on plants from all regions, but these negative effects were significantly weaker in soils from non‐native ranges in Chile and California than in those from the non‐native range in Argentina and the native range in Eurasia. Main conclusions The biogeographic differences in negative effects of microbes in this study conformed to the enemy‐release hypothesis (ERH) overall, but the strong negative effect of soil biota in Argentina, where C. solstitialis is invasive, and weaker effects in Chile where it is not, indicated that different factors influencing invasion are likely to occur in large scale biogeographic mosaics of interaction strengths.     

Microbial phylotype composition and diversity predicts plant productivity and plant–soil feedbacks

The relationship between ecological variation and microbial genetic composition is critical to understanding microbial influence on community and ecosystem function. In glasshouse trials using nine native legume species and 40 rhizobial strains, we find that bacterial rRNA phylotype accounts for 68% of amoung isolate variability in symbiotic effectiveness and 79% of host specificity in growth response. We also find that rhizobial phylotype diversity and composition of soils collected from a geographical breadth of sites explains the growth responses of two acacia species. Positive soil microbial feedback between the two acacia hosts was largely driven by changes in diversity of rhizobia. Greater rhizobial diversity accumulated in association with the less responsive host species, Acacia salicina, and negatively affected the growth of the more responsive Acacia stenophylla. Together, this work demonstrates correspondence of phylotype with microbial function, and demonstrates that the dynamics of rhizobia on host species can feed back on plant population performance.     

Plant‐driven changes in soil microbial communities influence seed germination through negative feedbacks

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The interplay between soil structure,roots, and microbiota as a determinant of plant–soil feedback

Plant–soil feedback (PSF) can influence plant community structure via changes in the soil microbiome. However, how these feedbacks depend on the soil environment remains poorly understood. We hypothesized that disintegrating a naturally aggregated soil may influence the outcome of PSF by affecting microbial communities. Furthermore, we expected plants to differentially interact with soil structure and the microbial communities due to varying root morphology. We carried out a feedback experiment with nine plant species (five forbs and four grasses) where the “training phase” consisted of aggregated versus disintegrated soil. In the feedback phase, a uniform soil was inoculated in a fully factorial design with soil washings from conspecific‐ versus heterospecific‐trained soil that had been either disintegrated or aggregated. This way, the effects of prior soil structure on plant performance in terms of biomass production and allocation were examined. In the training phase, soil structure did not affect plant biomass. But on disintegrated soil, plants with lower specific root length (SRL) allocated more biomass aboveground. PSF in the feedback phase was negative overall. With training on disintegrated soil, conspecific feedback was positively correlated with SRL and significantly differed between grasses and forbs. Plants with higher SRL were likely able to easily explore the disintegrated soil with smaller pores, while plants with lower SRL invested in belowground biomass for soil exploration and seemed to be more susceptible to fungal pathogens. This suggests that plants with low SRL could be more limited by PSF on disintegrated soils of early successional stages. This study is the first to examine the influence of soil structure on PSF. Our results suggest that soil structure determines the outcome of PSF mediated by SRL. We recommend to further explore the effects of soil structure and propose to include root performance when working with PSF.     

The role of vegetation–microclimate feedback in promoting shrub encroachment in the northern Chihuahuan desert

Many arid and semi‐arid landscapes around the world are affected by a shift from grassland to shrubland vegetation, presumably induced by climate warming, increasing atmospheric CO₂ concentrations, and/or changing land use. This major change in vegetation cover is likely sustained by positive feedbacks with the physical environment. Recent research has focused on a feedback with microclimate, whereby cold intolerant shrubs increase the minimum nocturnal temperatures in their surroundings. Despite the rich literature on the impact of land cover change on local climate conditions, changes in microclimate resulting from shrub expansion into desert grasslands have remained poorly investigated. It is unclear to what extent such a feedback can affect the maximum extent of shrub expansion and the configuration of a stable encroachment front. Here, we focus on the case of the northern Chihuahuan desert, where creosotebush (Larrea tridentata) has been replacing grasslands over the past 100–150 years. We use a process‐based coupled atmosphere‐vegetation model to investigate the role of this feedback in sustaining shrub encroachment in the region. Simulations indicate that the feedback allows juvenile shrubs to establish in the grassland during average years and, once established, reduce their vulnerability to freeze‐induced mortality by creating a warmer microclimate. Such a feedback is crucial in extreme cold winters as it may reduce shrub mortality. We identify the existence of a critical zone in the surroundings of the encroachment front, in which vegetation dynamics are bistable: in this zone, vegetation can be stable both as grassland and as shrubland. The existence of these alternative stable states explains why in most cases the shift from grass to shrub cover is found to be abrupt and often difficult to revert.     

Ericaceous plant–fungus network in a harsh alpine–subalpine environment

In terrestrial ecosystems, plant species and diverse root‐associated fungi form complex networks of host–symbiont associations. Recent studies have revealed that structures of those below‐ground plant–fungus networks differ between arbuscular mycorrhizal and ectomycorrhizal symbioses. Nonetheless, we still remain ignorant of how ericaceous plant species, which dominate arctic and alpine tundra, constitute networks with their root‐associated fungi. Based on a high‐throughput DNA sequencing data set, we characterized the statistical properties of a network involving 16 ericaceous plant species and more than 500 fungal taxa in the alpine–subalpine region of Mt. Tateyama, central Japan. While all the 16 ericaceous species were associated mainly with fungi in the order Helotiales, they varied remarkably in association with fungi in other orders such as Sebacinales, Atheliales, Agaricales, Russulales and Thelephorales. The ericaceous plant–fungus network was characterized by high symbiont/host preferences. Moreover, the network had a characteristic structure called ‘anti‐nestedness’, which has been previously reported in ectomycorrhizal plant–fungus networks. The results lead to the hypothesis that ericaceous plants in harsh environments can host unexpectedly diverse root‐associated fungal taxa, constituting networks whose structures are similar to those of previously reported ectomycorrhizal networks but not to those of arbuscular mycorrhizal ones.     

Convergent ecosystem responses to 23‐year ambient and manipulated warming link advancing snowmelt and shrub encroachment to transient and long‐term climate–soil carbon feedback

Ecosystem responses to climate change can exert positive or negative feedbacks on climate, mediated in part by slow‐moving factors such as shifts in vegetation community composition. Long‐term experimental manipulations can be used to examine such ecosystem responses, but they also present another opportunity: inferring the extent to which contemporary climate change is responsible for slow changes in ecosystems under ambient conditions. Here, using 23 years of data, we document a shift from nonwoody to woody vegetation and a loss of soil carbon in ambient plots and show that these changes track previously shown similar but faster changes under experimental warming. This allows us to infer that climate change is the cause of the observed shifts in ambient vegetation and soil carbon and that the vegetation responses mediate the observed changes in soil carbon. Our findings demonstrate the realism of an experimental manipulation, allow attribution of a climate cause to observed ambient ecosystem changes, and demonstrate how a combination of long‐term study of ambient and experimental responses to warming can identify mechanistic drivers needed for realistic predictions of the conditions under which ecosystems are likely to become carbon sources or sinks over varying timescales.     

Transgenerational soil‐mediated differences between plants experienced or naïve to a grass invasion

Invasive species may undergo rapid change as they invade. Native species persisting in invaded areas may also experience rapid change over this short timescale relative to native populations in uninvaded areas. We investigated the response of the native Achillea millefolium to soil from Holcus lanatus‐invaded and uninvaded areas, and we sought to determine whether differential responses between A. millefolium from invaded (invader experienced) and uninvaded (invader naïve) areas were mediated by soil community changes. Plants grown from seed from experienced and naïve areas responded differently to invaded and uninvaded soil with respect to germination time, biomass, and height. Overall, experienced plants grew faster and taller than their naïve counterparts. Naïve native plants showed negative feedbacks with their home soil and positive feedbacks with invaded soil; experienced plants were less responsive to soil differences. Our results suggest that native plants naïve to invasion may be more sensitive to soil communities than experienced plants, consistent with recent studies. While differences between naïve and experienced plants are transgenerational, our design cannot differentiate between differences that are genetically based, plastic, or both. Regardless, our results highlight the importance of seed source and population history in restoration, emphasizing the restoration potential of experienced seed sources.     

Phenotypic plasticity of four Chenopodiaceae species with contrasting saline–sodic tolerance in response to increased salinity–sodicity

It is unknown whether phenotypic plasticity in fitness‐related traits is associated with salinity–sodicity tolerance. This study compared growth and allocation phenotypic plasticity in two species with low salinity–sodicity tolerance (Chenopodium acuminatum and C. stenophyllum) and two species with high salinity–sodicity tolerance (Suaeda glauca and S. salsa) in a pot experiment in the Songnen grassland, China. While the species with low tolerance had higher growth and allocation plasticity than the highly tolerant species, the highly tolerant species only adjusted their growth traits and maintained higher fitness (e.g., plant height and total biomass) in response to increased soil salinity–sodicity, with low biomass allocation plasticity. Most plasticity is “apparent” plasticity (ontogenetic change), and only a few traits, for example, plant height:stem diameter ratio and root:shoot biomass ratio, represent “real” plasticity (real change in response to the environment). Our results show that phenotypic plasticity was negatively correlated with saline–sodic tolerance and could be used as an index of species sensitivity to soil salinity–sodicity.     

A substantial role of soil erosion in the land carbon sink and its future changes

Realistic representation of land carbon sink in climate models is vital for predicting carbon climate feedbacks in a changing world. Although soil erosion that removes land organic carbon has increased substantially since the onset of agriculture, it is rarely included in the current generation of climate models. Using an Earth system model (ESM) with soil erosion represented, we estimated that on average soil erosion displaces 5% of newly fixed land organic carbon downslope annually in the continental United States. In the lower Mississippi river basin and the Cascades, the fraction can be as large as 40%. About 12% of the eroded organic carbon is eventually exported to inland waters, which is equal to 14% of the simulated net carbon gain by terrestrial ecosystems. By comparing the eroded organic carbon export to rivers with the particulate organic carbon export to oceans, we demonstrated that a large fraction of the carbon export to rivers could have been mineralized in inland waters. Importantly, with a direct comparison of eroded and exported soil organic carbon and land net carbon uptake, we found that ESMs that ignore soil erosion likely offset the erosional carbon loss by increasing heterotrophic respiration implicitly. But as soil erosion and heterotrophic respiration respond differently to a warming climate, this unrealistic compensation would lead to biased predictions of future land carbon sink.     

Nitrogen deposition weakens plant–microbe interactions in grassland ecosystems

Soil carbon (C) and nitrogen (N) stoichiometry is a main driver of ecosystem functioning. Global N enrichment has greatly changed soil C : N ratios, but how altered resource stoichiometry influences the complexity of direct and indirect interactions among plants, soils, and microbial communities has rarely been explored. Here, we investigated the responses of the plant‐soil‐microbe system to multi‐level N additions and the role of dissolved organic carbon (DOC) and inorganic N stoichiometry in regulating microbial biomass in semiarid grassland in northern China. We documented a significant positive correlation between DOC and inorganic N across the N addition gradient, which contradicts the negative nonlinear correlation between nitrate accrual and DOC availability commonly observed in natural ecosystems. Using hierarchical structural equation modeling, we found that soil acidification resulting from N addition, rather than changes in the plant community, was most closely related to shifts in soil microbial community composition and decline of microbial respiration. These findings indicate a down‐regulating effect of high N availability on plant–microbe interactions. That is, with the limiting factor for microbial biomass shifting from resource stoichiometry to soil acidity, N enrichment weakens the bottom‐up control of soil microorganisms by plant‐derived C sources. These results highlight the importance of integratively studying the plant‐soil‐microbe system in improving our understanding of ecosystem functioning under conditions of global N enrichment.     

Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles – upscaling an aggregate biophysical model

Microbial communities inhabiting soil aggregates dynamically adjust their activity and composition in response to variations in hydration and other external conditions. These rapid dynamics shape signatures of biogeochemical activity and gas fluxes emitted from soil profiles. Recent mechanistic models of microbial processes in unsaturated aggregate‐like pore networks revealed a highly dynamic interplay between oxic and anoxic microsites jointly shaped by hydration conditions and by aerobic and anaerobic microbial community abundance and self‐organization. The spatial extent of anoxic niches (hotspots) flicker in time (hot moments) and support substantial anaerobic microbial activity even in aerated soil profiles. We employed an individual‐based model for microbial community life in soil aggregate assemblies represented by 3D angular pore networks. Model aggregates of different sizes were subjected to variable water, carbon and oxygen contents that varied with soil depth as boundary conditions. The study integrates microbial activity within aggregates of different sizes and soil depth to obtain estimates of biogeochemical fluxes from the soil profile. The results quantify impacts of dynamic shifts in microbial community composition on CO₂ and N₂O production rates in soil profiles in good agreement with experimental data. Aggregate size distribution and the shape of resource profiles in a soil determine how hydration dynamics shape denitrification and carbon utilization rates. Results from the mechanistic model for microbial activity in aggregates of different sizes were used to derive parameters for analytical representation of soil biogeochemical processes across large scales of practical interest for hydrological and climate models.     

The strength of negative plant–soil feedback increases from the intraspecific to the interspecific and the functional group level

One of the processes that may play a key role in plant species coexistence and ecosystem functioning is plant–soil feedback, the effect of plants on associated soil communities and the resulting feedback on plant performance. Plant–soil feedback at the interspecific level (comparing growth on own soil with growth on soil from different species) has been studied extensively, while plant–soil feedback at the intraspecific level (comparing growth on own soil with growth on soil from different accessions within a species) has only recently gained attention. Very few studies have investigated the direction and strength of feedback among different taxonomic levels, and initial results have been inconclusive, discussing phylogeny, and morphology as possible determinants. To test our hypotheses that the strength of negative feedback on plant performance increases with increasing taxonomic level and that this relationship is explained by morphological similarities, we conducted a greenhouse experiment using species assigned to three taxonomic levels (intraspecific, interspecific, and functional group level). We measured certain fitness‐related aboveground traits and used them along literature‐derived traits to determine the influence of morphological similarities on the strength and direction of the feedback. We found that the average strength of negative feedback increased from the intraspecific over the interspecific to the functional group level. However, individual accessions and species differed in the direction and strength of the feedback. None of our results could be explained by morphological dissimilarities or individual traits. Synthesis. Our results indicate that negative plant–soil feedback is stronger if the involved plants belong to more distantly related species. We conclude that the taxonomic level is an important factor in the maintenance of plant coexistence with plant–soil feedback as a potential stabilizing mechanism and should be addressed explicitly in coexistence research, while the traits considered here seem to play a minor role.     

Positive climate feedbacks of soil microbial communities in a semi‐arid grassland

Soil microbial communities may be able to rapidly respond to changing environments in ways that change community structure and functioning, which could affect climate–carbon feedbacks. However, detecting microbial feedbacks to elevated CO₂ (eCO₂) or warming is hampered by concurrent changes in substrate availability and plant responses. Whether microbial communities can persistently feed back to climate change is still unknown. We overcame this problem by collecting microbial inocula at subfreezing conditions under eCO₂ and warming treatments in a semi‐arid grassland field experiment. The inoculant was incubated in a sterilised soil medium at constant conditions for 30 days. Microbes from eCO₂ exhibited an increased ability to decompose soil organic matter (SOM) compared with those from ambient CO₂ plots, and microbes from warmed plots exhibited increased thermal sensitivity for respiration. Microbes from the combined eCO₂ and warming plots had consistently enhanced microbial decomposition activity and thermal sensitivity. These persistent positive feedbacks of soil microbial communities to eCO₂ and warming may therefore stimulate soil C loss.     

Negative plant‐phyllosphere feedbacks in native Asteraceae hosts – a novel extension of the plant‐soil feedback framework

Over the past 25 years, the plant‐soil feedback (PSF) framework has catalyzed our understanding of how belowground microbiota impact plant fitness and species coexistence. Here, we apply a novel extension of this framework to microbiota associated with aboveground tissues, termed ‘plant‐phyllosphere feedback (PPFs)’. In parallel greenhouse experiments, rhizosphere and phyllosphere microbiota of con‐ and heterospecific hosts from four species were independently manipulated. In a third experiment, we tested the combined effects of soil and phyllosphere feedback under field conditions. We found that three of four species experienced weak negative PSF whereas, in contrast, all four species experienced strong negative PPFs. Field‐based feedback estimates were highly negative for all four species, though variable in magnitude. Our results suggest that phyllosphere microbiota, like rhizosphere microbiota, can potentially mediate plant species coexistence via negative feedbacks. Extension of the PSF framework to the phyllosphere is needed to more fully elucidate plant‐microbiota interactions.