Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota

Plant legacies and soil microbial community dynamics control soil respiration

BackgroundThe root-associated microbiome has been of keen research interest especially in the last decade due to the large potential for increasing overall plant performance in agricultural systems. Studies about spatio-temporal variation of the root-associated microbiome focused so far primarily on community-compositional changes of annual plants, while little is known about their perennial counterparts. The aim of this work was to get deep insight into the spatial patterns and temporal dynamics of the root associated microbiota of apple trees.ResultsThe bacterial community structure in rhizospheric soil and endospheric root material from orchard-grown apple trees was characterized based on 16S rRNA gene amplicon sequencing. At the small scale, the rhizosphere and endosphere bacterial communities shifted gradually with increasing root size diameter (PERMANOVA R2-values up to 0.359). At the larger scale, bulk soil heterogeneity introduced variation between tree individuals, especially in the rhizosphere microbiota, while the presence of a root pathogen was contributing to tree-to-tree variation in the endosphere microbiota. Moreover, the communities of both compartments underwent seasonal changes and displayed year-to-year variation (PERMANOVA R2-values of 0.454 and 0.371, respectively).ConclusionsThe apple tree root-associated microbiota can be spatially heterogeneous at field scale due to soil heterogeneities, which particularly influence the microbiota in the rhizosphere soil, resulting in tree-to-tree variation. The presence of pathogens can contribute to this variation, though primarily in the endosphere microbiota. Smaller-scale spatial heterogeneity is observed in the rhizosphere and endosphere microbiota related to root diameter, likely influenced by root traits and processes such as rhizodeposition. The microbiota is also subject to temporal variation, including seasonal effects and annual variation. As a consequence, responses of the tree root microbiota to further environmental cues should be considered in the context of this spatio-temporal variation.

A better understanding of factors shaping the rhizosphere microbiota is important for sustainable crop production. We hypothesized that the effect of agricultural management on the soil microbiota is reflected in the assemblage of the rhizosphere microbiota with implications for plant performance. We designed a growth chamber experiment growing the model plant lettuce under controlled conditions in soils of a long-term field experiment with contrasting histories of tillage (mouldboard plough vs cultivator tillage), fertilization intensity (intensive standard nitrogen (N) + pesticides/growth regulators vs extensive reduced N without fungicides/growth regulators), and last standing field crop (rapeseed vs winter wheat). High-throughput sequencing of bacterial and archaeal 16S rRNA genes and fungal ITS2 regions amplified from total community DNA showed that these factors shaped the soil and rhizosphere microbiota of lettuce, however, to different extents among the microbial domains. Pseudomonas and Olpidium were identified as major indicators for agricultural management in the rhizosphere of lettuce. Long-term extensive fertilization history of soils resulted in higher lettuce growth and increased expression of genes involved in plant stress responses compared to intensive fertilization. Our work adds to the increasing knowledge on how soil microbiota can be manipulated by agricultural management practices which could be harnessed for sustainable crop production.

Effects of plant-induced changes in soil properties, which impact subsequent plant growth, have received increasing attention in plant ecology (e.g., Smith-Ramesh & Reynolds 2017). These plant-soil feedbacks (PSFs) are considered to be important for plant performance and plant-community composition in many terrestrial ecosystems (e.g., van der Putten et al. 2013). However, so far most conclusions on the importance of PSFs in natural systems have been drawn from experiments performed under highly controlled and artificial conditions. Under natural conditions, the growth and development of plants as well as that of soil organisms is influenced by many more abiotic and biotic interactions than in the greenhouse. Hence, there is an urgent need to investigate PSFs under more natural conditions and to better understand the interactions between PSFs and environmental drivers (De Long et al. 2019). This Research Topic comprises 14 articles - ranging from Original research articles, meta-analytical Reviews and Perspectives - that aim to advance our understanding of the contribution of PSFs to plant growth and plant community composition in different environmental contexts.

Plant-soil feedbacks (PSFs) are plant-mediated changes to soil properties that ultimately influence plant performance, and can, thus, determine plant diversity, succession, and invasion. We hypothesized that PSFs influence invasion processes and that PSF mechanisms are largely driven by changes in soil properties produced by specific plant species. To test these hypotheses, we studied the effects of different soils collected from under common plant species on the growth of the invasive plant Phytolacca americana. We found that PSFs may interfere with invasion resistance because P. americana seedlings showed reduced growth (lower biomass) in soils collected from underneath some native species compared with soils collected from underneath P. americana and two non-native plants. We then selected eight co-occurring native and non-native plant species, and examined PSF dynamics and mechanisms in a pairwise conditioned soil greenhouse experiment. Plant species-specific conditioning effects regarding soil nutrients and enzyme activities were observed. Phytolacca americana had a high ability to use soil N, which may be related to its high invasion ability. Soil P was significantly lower in Quercus acutissima-conditioned soil, indicating that low P availability in Q. acutissima forests may enhance resistance to plant invasion. However, surprisingly, some native plants did not produce PSF effects that decreased the relative performance of invasive plants, nor did the invasive plants produce PSF effects that increased their own performance. We speculate that these PSF findings from greenhouse experiments cannot be extrapolated to field conditions because the litter and allelochemicals of some plants may be important for invasion resistance.

Interactions between aboveground and belowground biota have the potential to modify ecosystem responses to climate change, yet little is known about how drought influences plant-soil feedbacks with respect to microbial mediation of plant community dynamics. We tested the hypothesis that drought modifies plant-soil feedback with consequences for plant competition. We measured net pairwise plant-soil feedbacks for two grassland plant species grown in monoculture and competition in soils that had or had not been subjected to a previous drought; these were then exposed to a subsequent drought. To investigate the mechanisms involved, we assessed treatment responses of soil microbial communities and nutrient availability. We found that previous drought had a legacy effect on bacterial and fungal community composition that decreased plant growth in conspecific soils and had knock-on effects for plant competitive interactions. Moreover, plant and microbial responses to subsequent drought were dependent on a legacy effect of the previous drought on plant-soil interactions. We show that drought has lasting effects on belowground communities with consequences for plant-soil feedbacks and plant-plant interactions. This suggests that drought, which is predicted to increase in frequency with climate change, may change soil functioning and plant community composition via the modification of plant-soil feedbacks.

Plant–soil feedback—feedback from plant‐induced changes in soil properties to plant fitness—is increasingly shown to drive the maintenance of local plant diversity at both interspecific and intraspecific levels. A robust understanding of the relationships between plant–soil feedback and functional plant traits, which would improve our ability to generalize plant–soil feedback results beyond specific study systems, is, however, still lacking. This is especially true at the intraspecific plant level. We assessed the relationship between plant–soil feedback and several functional traits in 13 co‐occurring grassland species, including 20 genotypes of the dominant grass, Festuca rubra. The traits encompassed various aspects of growth, root properties and root exudate variability. Combining these traits into principal gradients of functional trait variation, we also tested the potential for the conservation and collaboration gradients to explain variation in PSF. Between‐species plant–soil feedback variation was explained by differences in biomass production and exudate composition, as well as contrasting strategies along the collaboration gradient. Within‐species plant–soil feedback variation—that is between Festuca rubra genotypes—was associated with exudate variability, especially contrasting amounts of exuded phenols. Several traits had a significant effect on plant–soil feedback only via their interaction with exudate composition. Overall, PSF was associated with different traits at between‐species versus within‐species levels. Root exudate variability was, however, involved at both diversity levels. Our results put forth the role of root exudation patterns as an important driver of variation in plant–soil feedback. Better integration between research on plant–soil feedback and on root exudation would therefore improve our understanding of the processes—both ecological and evolutionary—supporting the maintenance of plant diversity within grassland communities. Read the free Plain Language Summary for this article on the Journal blog.

Plant productivity often increases with species richness, but the mechanisms explaining this diversity-productivity relationship are not fully understood. We tested if plant-soil feedbacks (PSF) can help to explain how biomass production changes with species richness. Using a greenhouse experiment, we measured all 240 possible PSFs for 16 plant species. At the same time, 49 plant communities with diversities ranging from one to 16 species were grown in replicated pots. A suite of plant community growth models, parameterized with (PSF) or without PSF (Null) effects, was used to predict plant growth observed in the communities. Selection effects and complementarity effects in modeled and observed data were separated. Plants created soils that increased or decreased subsequent plant growth by 25%±10%, but because PSFs were negative for C3 and C4 grasses, neutral for forbs, and positive for legumes, the net effect of all PSFs was a 2%±17% decrease in plant growth. Experimental plant communities with 16 species produced 37% more biomass than monocultures due to complementarity. Null models incorrectly predicted that 16-species communities would overyield due to selection effects. Adding PSF effects to Null models decreased selection effects, increased complementarity effects, and improved correlations between observed and predicted community biomass. PSF models predicted 26% of overyielding caused by complementarity observed in experimental communities. Relative to Null models, PSF models improved the predictions of the magnitude and mechanism of the diversity-productivity relationship. Results provide clear support for PSFs as one of several mechanisms that determine diversity-productivity relationships and help close the gap in understanding how biodiversity enhances ecosystem services such as biomass production.

Mounting evidence suggests that reciprocal interactions between plants and the soil microbiota can be a primary force that generates key macroscopic patterns of plant communities (coexistence, dominance, and succession) in forest ecosystems. The aim of this article is to review empirical and theoretical perspectives of plant–soil feedback research in the context of forest community ecology. I first use a simple theoretical model to get insights into an array of the dynamics generated by plant–soil feedback: negative plant–soil feedback maintains plant species diversity and reduces plant growth, while positive plant–soil feedback drives plant growth of certain species and hence their dominance. I then describe how ecologists have unveiled the enormously complex plant‐microbiota interaction (i.e., the soil conditioning experiment) and review the linkage of plant–soil feedback with three key plant community patterns: (i) dominance, (ii) spatial structure and (iii) succession. I highlight one belowground plant trait (mycorrhizal type) that can mediate these linkages: arbuscular mycorrhizal species tend to exhibit negative plant–soil feedback while ectomycorrhizal species tend to exhibit positive plant–soil feedback. Although mycorrhizal plant–soil feedback potentially explains the patterns of tree diversity from local to global scales, many questions remain. Future studies should expand plant–soil feedback theory to incorporate numerous other feedback mechanisms and test how mycorrhizal types mediate the net feedback effects that could propagate to shape large‐scale forest structures and dynamics.

Summary Although biotic legacies of past agricultural practices are widespread and increasing in contemporary ecosystems, our understanding of the mechanisms driving such legacies is still poor. Forest understories on former agricultural land show low frequencies and abundance of typical woodland species when compared with ancient forests. These community shifts have been ascribed to the effects of dispersal limitation. A rarely considered mechanism is that post‐dispersal processes driven by plant‐associated communities determine the poor performance and recruitment of woodland indicators. Given the strong alterations in soil conditions due to former agricultural practices, we hypothesized that (abiotic) plant–soil feedbacks could be a major factor in community shifts. We addressed this hypothesis by comparing plant‐associated communities in the soil and above the ground in ancient and post‐agricultural alluvial forests; then, we experimentally tested whether the changes in biotic and abiotic soil properties could affect above‐ground herbivore abundance and pressure and plant performance. Ancient and post‐agricultural communities clearly differed in composition at different levels of the food web. Besides the plant community, we also observed the differences in the microbial and nematode community with increased abundance of root‐feeding nematodes in post‐agricultural soils. The composition of the above‐ground invertebrate community did not differ in ancient and post‐agricultural forest parcels; however, plants growing in post‐agricultural sites showed higher abundance of invertebrate herbivores and suffered more herbivory. Nutrient analyses of soil and plants showed that increased levels of phosphorus (and to a lesser extent, nitrogen) made plants more nutritious for insect herbivores. Laboratory experiments further pointed to this mechanism as an explanation of the poorer performance of woodland indicators in post‐agricultural woodlands. Our results point to biotic and abiotic plant–soil feedbacks coupled with herbivory as a new mechanism to explain the legacy effects in temperate forests. The modification of the below‐ground community and soil abiotic characteristics by previous agricultural activity affects not only the plant growth but also the plant nutrient content in the compared understorey species, making them more susceptible to above‐ground herbivory. Our results provide one of the first examples of integrating plant–soil feedback and above‐ and below‐ground interactions to explain land‐use legacies.

Plants interact continuously with the surrounding soil microbiota, shaping and being shaped by these communities over time, termed as the plant-soil feedback (PSF). As a result, plants can leave a biological imprint in the soil that affects the performance of subsequent plants, a phenomenon termed the soil-borne legacy. In this study, we investigated how the rhizosphere microbiota of rice plants exhibiting (or not) foliar disease symptoms in a Cambodian field was modified and influenced subsequent generation of plants. Based on a visual assessment of foliar symptoms, we collected and mixed the rhizospheres of plants classified as “diseased” or “healthy,” respectively. These mixed rhizospheres were then used to sow new rice plants in controlled conditions, which were subsequently challenged with Xanthomonas oryzae pv. oryzae. Phenotypic analyses revealed that plants grown in the rhizosphere microbiota collected from diseased field plants were smaller, yet displayed smaller symptoms to foliar pathogens compared to those grown in the microbiota of healthy plants. Amplicon sequencing of roots and rhizospheres from field samples confirmed that diseased and healthy plants harbored distinct microbial communities. A dysbiotic rhizosphere was found to be present in leaf-diseased plants, in contrast to healthy ones. These differences were also detectable in the composite rhizosphere mixes, and persisted in the rhizospheres of a new generation of rice plants grown in these soils. This suggests a microbiota-driven legacy, wherein the health status of the previous generation shapes the microbial environment and influences plant phenotype in terms of growth and defense. Our results support the idea that leaf-diseased plants condition their rhizosphere microbiota thus influencing plant phenotype in the next generation. Understanding the impact of disease-induced microbial legacy on next generation plant phenotype is crucial for developing microbiome-based crop protection strategies.

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.

Plant-soil feedbacks (PSFs) play a relevant role as drivers of species abundance, coexistence, and succession in plant communities. However, the potential contribution of PSFs to community dynamics in changing forest ecosystems affected by global change drivers is still largely unexplored. We measured the direction, strength and nature (biological vs. chemical) of PSFs experienced by coexisting tree species in two types of declining Quercus suber forests of southwestern Spain (open woodland vs. closed forest) invaded by the exotic soil pathogen Phytophthora cinnamomi. To test PSFs in a realistic community context, we focused not only on individual PSFs (i.e., comparing the growth of a tree species on conspecific vs. heterospecific soil) but also calculated net-pairwise PSFs by comparing performance of coexisting tree species on their own and each other's soils. We hypothesized that the decline and death of Q.suber would alter the direction and strength of individual and net-pairwise PSFs due to the associated changes in soil nutrients and microbial communities, with implications for recruitment dynamics and species coexistence. In support of our hypothesis, we found that the decline of Q.suber translated into substantial alterations of individual and net-pairwise PSFs, which shifted from mostly neutral to significantly positive or negative, depending on the forest type. In both cases however the identified PSFs benefited other species more than Q.suber (i.e., heterospecific positive PSF in the open woodland, conspecific negative PSF in the closed forest). Our results supported PSFs driven by changes in chemical soil properties (mainly phosphorus) and arbuscular mycorrhizal fungi, but not in pathogen abundance. Overall, our study suggests that PSFs might reinforce the loss of dominance of Q.suber in declining forests invaded by P.cinnamomi by promoting the relative performance of non-declining coexisting species. More generally, our results indicate an increase in the strength of net PSFs as natural forests become disturbed by global change drivers (e.g., invasive species), suggesting an increasingly important role of PSFs in forest community dynamics in the near future.

BackgroundSoils are a key component of agricultural productivity, and soil microbiota determine the availability of many essential plant nutrients. Agricultural domestication of soils, that is, the conversion of previously uncultivated soils to a cultivated state, is frequently accompanied by intensive monoculture, especially in the developing world. However, there is limited understanding of how continuous cultivation alters the structure of prokaryotic soil microbiota after soil domestication, including to what extent crop plants impact soil microbiota composition, and how changes in microbiota composition arising from cultivation affect crop performance.ResultsWe show here that continuous monoculture (> 8 growing seasons) of the major food crop rice under flooded conditions is associated with a pronounced shift in soil bacterial and archaeal microbiota structure towards a more consistent composition, thereby domesticating microbiota of previously uncultivated sites. Aside from the potential effects of agricultural cultivation practices, we provide evidence that rice plants themselves are important drivers of the domestication process, acting through selective enrichment of specific taxa, including methanogenic archaea, in their rhizosphere that differ from those of native plants growing in the same environment. Furthermore, we find that microbiota from soils domesticated by rice cultivation contribute to plant-soil feedback, by imparting a negative effect on rice seedling vigor.ConclusionsSoil domestication through continuous monoculture cultivation of rice results in compositional changes in the soil microbiota, which are in part driven by the rice plants. The consequences include a negative impact on plant performance and increases in greenhouse gas emitting microbes.

Fertilization management can affect plant performance and soil microbiota, involving still poorly understood rhizosphere interactions. We hypothesized that fertilization practice exerts specific effects on rhizodeposition with consequences for recruitment of rhizosphere microbiota and plant performance. To address this hypothesis, we conducted a minirhizotron experiment using lettuce as model plant and field soils with contrasting properties from two long-term field experiments (HUB-LTE: loamy sand, DOK-LTE: silty loam) with organic and mineral fertilization history. Increased relative abundance of plant-beneficial arbuscular mycorrhizal fungi and fungal pathotrophs were characteristic of the rhizospheres in the organically managed soils (HU-org; BIODYN2). Accordingly, defense-related genes were systemically expressed in shoot tissues of the respective plants. As a site-specific effect, high relative occurrence of the fungal lettuce pathogen Olpidium sp. (76–90%) was recorded in the rhizosphere, both under long-term organic and mineral fertilization at the DOK-LTE site, likely supporting Olpidium infection due to a lower water drainage potential compared to the sandy HUB-LTE soils. However, plant growth depressions and Olpidium infection were exclusively recorded in the BIODYN2 soil with organic fertilization history. This was associated with a drastic (87–97%) reduction in rhizosphere abundance of potentially plant-beneficial microbiota (Pseudomonadaceae, Mortierella elongata) and reduced concentrations of the antifungal root exudate benzoate, known to be increased in presence of Pseudomonas spp. In contrast, high relative abundance of Pseudomonadaceae (Gammaproteobacteria) in the rhizosphere of plants grown in soils with long-term mineral fertilization (61–74%) coincided with high rhizosphere concentrations of chemotactic dicarboxylates (succinate, malate) and a high C (sugar)/N (amino acid) ratio, known to support the growth of Gammaproteobacteria. This was related with generally lower systemic expression of plant defense genes as compared with organic fertilization history. Our results suggest a complex network of belowground interactions among root exudates, site-specific factors and rhizosphere microbiota, modulating the impact of fertilization management with consequences for plant health and performance.