Plant Genetic Networks Shaping Phyllosphere Microbial Community.

Phyllosphere microbial communities inhabit the aerial plant parts, such as leaves and flowers, where they form complex molecular interactions with the host plant. Contrary to the relatively well-studied rhizosphere microbiome, scientists are just starting to understand, and potentially utilize, the phyllosphere microbiome. In this article, we summarize the recent studies that have provided novel insights into the mechanism of the host genotype shaping the phyllosphere microbiome and the possibility to select a stable and well-adapted microbiome. We also discuss the most pressing gaps in our knowledge and identify the most promising research directions and tools for understanding the assembly and function of phyllosphere microbiomes - this understanding is necessary if we are to harness phyllosphere microbiomes for improving plant growth and health in managed systems.

Deciphering the role of specialist and generalist plant-microbial interactions as drivers of plant-soil feedback.

Feedback between plants and soil microbial communities can be a powerful driver of vegetation dynamics. Plants elicit changes in the soil microbiome that either promote or suppress conspecifics at the same location, thereby regulating population density-dependence and species co-existence. Such effects are often attributed to the accumulation of host-specific antagonistic or beneficial microbiota in the rhizosphere. However, the identity and host-specificity of the microbial taxa involved are rarely empirically assessed. Here we review the evidence for host-specificity in plant-associated microbes and propose that specific plant-soil feedbacks can also be driven by generalists. We outline the potential mechanisms by which generalist microbial pathogens, mutualists and decomposers can generate differential effects on plant hosts and synthesize existing evidence to predict these effects as a function of plant investments into defence, microbial mutualists and dispersal. Importantly, the capacity of generalist microbiota to drive plant-soil feedbacks depends not only on the traits of individual plants but also on the phylogenetic and functional diversity of plant communities. Identifying factors that promote specialization or generalism in plant-microbial interactions and thereby modulate the impact of microbiota on plant performance will advance our understanding of the mechanisms underlying plant-soil feedback and the ways it contributes to plant co-existence.

Forest fire induces short-term shifts in soil food webs with consequences for carbon cycling.

We tested for fire-induced (5-6 years post-fire) changes in the structure and functioning of the soil food web along a 3000-km north-south transect across European Russia, spanning all major forest types in the northern hemisphere outside the tropics. The total biomass of the detrital food web, including microbes and invertebrates, was not affected by fire. However, fire reduced the biomass of microfauna and mites, but had no impact on mesofauna or macrofauna. Fire also reduced rates of carbon (C) mobilisation by soil biota. Our results demonstrate that fire-induced shifts in soil food webs have significant short-term effects on forest soil C cycling, but that these effects vary across forest types and geographic locations.

Root traits explain rhizosphere fungal community composition among temperate grassland plant species.

While it is known that interactions between plants and soil fungi drive many essential ecosystem functions, considerable uncertainty exists over the drivers of fungal community composition in the rhizosphere. Here, we examined the roles of plant species identity, phylogeny and functional traits in shaping rhizosphere fungal communities and tested the robustness of these relationships to environmental change. We conducted a glasshouse experiment consisting of 21 temperate grassland species grown under three different environmental treatments and characterised the fungal communities within the rhizosphere of these plants. We found that plant species identity, plant phylogenetic relatedness and plant traits all affected rhizosphere fungal community composition. Trait relationships with fungal communities were primarily driven by interactions with arbuscular mycorrhizal fungi, and root traits were stronger predictors of fungal communities than leaf traits. These patterns were independent of the environmental treatments the plants were grown under. Our results showcase the key role of plant root traits, especially root diameter, root nitrogen and specific root length, in driving rhizosphere fungal community composition, demonstrating the potential for root traits to be used within predictive frameworks of plant-fungal relationships. Furthermore, we highlight how key limitations in our understanding of fungal function may obscure previously unmeasured plant-fungal interactions.

Comparing root exudate collection techniques: An improved hybrid method.

1. Plant-microbe interactions are critical for ecosystem functioning and drive rhizosphere processes. Root exudates are an important soil carbon (C) input, as well as a mechanism for communication between plants and rhizosphere microbes, but are notoriously difficult to extract and characterise. Common methods produce either substantial noise from the soil or do not mimic natural systems. Optimising methods for root exudate collection in soil is crucial for advancing our understanding of root-microbe interactions under changing environmental conditions. 2. Hybrid root exudate collection methods, where plants are grown in soil and transferred to hydroponics for exudate collection after root washing, might offer an ecologically relevant alternative to existing approaches. However, this method causes potential root damage as well as osmosis and subsequent leaking of cell contents. Here, we assessed different 'root recovery' periods after root washing and before hybrid root exudate collection, by comparing root exudate quantity and quality with both damaged root extracts and with leachates collected from the intact root-soil system. This was done across three common grassland species representing three functional groups. 3. We found that root exudate profiles of the shortest recovery period (0 days) were similar to damaged root extracts and were very high in C. With an increasing period of root recovery, profiles were more similar to leachates collected from the intact root-soil system, and C concentrations decreased. While both hybrid and leachate collection methods separated species by their root exudate profiles, the hybrid method was less variable in terms of the amount of C measured and provided a more diverse and abundant metabolome with better identification of metabolites. 4. Our results show that a recovery period after root washing of at least 3 days is critical to prevent root damage bias in hybrid collection methods, and that our hybrid method yields exudates that discriminate between species. Our data also suggest that exudates collected with this hybrid method are ecologically valid, which is vital for gaining a mechanistic understanding of their role in ecosystem functioning.

Plant root exudation under drought: implications for ecosystem functioning.

Root exudates are a pathway for plant-microbial communication and play a key role in ecosystem response to environmental change. Here, we collate recent evidence that shows that plants of different growth strategies differ in their root exudation, that root exudates can select for beneficial soil microbial communities, and that drought affects the quantity and quality of root exudation. We use this evidence to argue for a central involvement of root exudates in plant and microbial response to drought and propose a framework for understanding how root exudates influence ecosystem form and function during and after drought. Specifically, we propose that fast-growing plants modify their root exudates to recruit beneficial microbes that facilitate their regrowth after drought, with cascading impacts on their abundance and ecosystem functioning. We identify outstanding questions and methodological challenges that need to be addressed to advance and solidify our comprehension of the importance of root exudates in ecosystem response to drought.

Mapping local and global variability in plant trait distributions.

Our ability to understand and predict the response of ecosystems to a changing environment depends on quantifying vegetation functional diversity. However, representing this diversity at the global scale is challenging. Typically, in Earth system models, characterization of plant diversity has been limited to grouping related species into plant functional types (PFTs), with all trait variation in a PFT collapsed into a single mean value that is applied globally. Using the largest global plant trait database and state of the art Bayesian modeling, we created fine-grained global maps of plant trait distributions that can be applied to Earth system models. Focusing on a set of plant traits closely coupled to photosynthesis and foliar respiration-specific leaf area (SLA) and dry mass-based concentrations of leaf nitrogen ([Formula: see text]) and phosphorus ([Formula: see text]), we characterize how traits vary within and among over 50,000 [Formula: see text]-km cells across the entire vegetated land surface. We do this in several ways-without defining the PFT of each grid cell and using 4 or 14 PFTs; each model's predictions are evaluated against out-of-sample data. This endeavor advances prior trait mapping by generating global maps that preserve variability across scales by using modern Bayesian spatial statistical modeling in combination with a database over three times larger than that in previous analyses. Our maps reveal that the most diverse grid cells possess trait variability close to the range of global PFT means.

Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling.

Root exudates play an important role in ecosystem response to climate change, but the functional consequences of drought-induced changes in the quality of root exudates are unknown. Here, we addressed this knowledge gap in a unique experimental approach. We subjected two common grassland species that differ widely in their growth strategies and root systems, the grass Holcus lanatus and the forb Rumex acetosa, to 2 wk of drought. We collected root exudates and soils at the end of the drought and after 2 wk of recovery and readded all root exudates to all soils in a fully reciprocal set-up to measure root-exudate-induced respiration. We found that soil treatment was unimportant for determining root-exudate-induced respiration. By contrast, root exudates collected from plants that had experienced drought clearly triggered more soil respiration than exudates from undroughted plants. Importantly, this increased respiration compensated for the lower rates of root exudation in droughted plants. Our findings reveal a novel mechanism through which drought can continue to affect ecosystem carbon cycling, and a potential plant strategy to facilitate regrowth through stimulating microbial activity. These findings have important implications for understanding plant and ecosystem response to drought.

Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity.

Theory suggests that more complex food webs promote stability and can buffer the effects of perturbations, such as drought, on soil organisms and ecosystem functions. Here, we tested experimentally how soil food web trophic complexity modulates the response to drought of soil functions related to carbon cycling and the capture and transfer below-ground of recent photosynthate by plants. We constructed experimental systems comprising soil communities with one, two or three trophic levels (microorganisms, detritivores and predators) and subjected them to drought. We investigated how food web trophic complexity in interaction with drought influenced litter decomposition, soil CO2 efflux, mycorrhizal colonization, fungal production, microbial communities and soil fauna biomass. Plants were pulse-labelled after the drought with 13 C-CO2 to quantify the capture of recent photosynthate and its transfer below-ground. Overall, our results show that drought and soil food web trophic complexity do not interact to affect soil functions and microbial community composition, but act independently, with an overall stronger effect of drought. After drought, the net uptake of 13 C by plants was reduced and its retention in plant biomass was greater, leading to a strong decrease in carbon transfer below-ground. Although food web trophic complexity influenced the biomass of Collembola and fungal hyphal length, 13 C enrichment and the net transfer of carbon from plant shoots to microbes and soil CO2 efflux were not affected significantly by varying the number of trophic groups. Our results indicate that drought has a strong effect on above-ground-below-ground linkages by reducing the flow of recent photosynthate. Our results emphasize the sensitivity of the critical pathway of recent photosynthate transfer from plants to soil organisms to a drought perturbation, and show that these effects may not be mitigated by the trophic complexity of soil communities, at least at the level manipulated in this experiment.

Plant attributes explain the distribution of soil microbial communities in two contrasting regions of the globe.

We lack strong empirical evidence for links between plant attributes (plant community attributes and functional traits) and the distribution of soil microbial communities at large spatial scales. Using datasets from two contrasting regions and ecosystem types in Australia and England, we report that aboveground plant community attributes, such as diversity (species richness) and cover, and functional traits can predict a unique portion of the variation in the diversity (number of phylotypes) and community composition of soil bacteria and fungi that cannot be explained by soil abiotic properties and climate. We further identify the relative importance and evaluate the potential direct and indirect effects of climate, soil properties and plant attributes in regulating the diversity and community composition of soil microbial communities. Finally, we deliver a list of examples of common taxa from Australia and England that are strongly related to specific plant traits, such as specific leaf area index, leaf nitrogen and nitrogen fixation. Together, our work provides new evidence that plant attributes, especially plant functional traits, can predict the distribution of soil microbial communities at the regional scale and across two hemispheres.

Legacy effects of drought on plant-soil feedbacks and plant-plant interactions.

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 community controls on short-term ecosystem nitrogen retention.

Retention of nitrogen (N) is a critical ecosystem function, especially in the face of widespread anthropogenic N enrichment; however, our understanding of the mechanisms involved is limited. Here, we tested under glasshouse conditions how plant community attributes, including variations in the dominance, diversity and range of plant functional traits, influence N uptake and retention in temperate grassland. We added a pulse of (15) N to grassland plant communities assembled to represent a range of community-weighted mean plant traits, trait functional diversity and divergence, and species richness, and measured plant and microbial uptake of (15) N, and leaching losses of (15) N, as a short-term test of N retention in the plant-soil system. Root biomass, herb abundance and dominant plant traits were the main determinants of N retention in the plant-soil system: greater root biomass and herb abundance, and lower root tissue density, increased plant (15) N uptake, while higher specific leaf area and root tissue density increased microbial (15) N uptake. Our results provide novel, mechanistic insight into the short-term fate of N in the plant-soil system, and show that dominant plant traits, rather than trait functional diversity, control the fate of added N in the plant-soil system.

Eating from the same plate? Revisiting the role of labile carbon inputs in the soil food web.

An increasing number of empirical studies are challenging the central fundamentals on which the classical soil food web model is built. This model assumes that bacteria consume labile substrates twice as fast as fungi, and that mycorrhizal fungi do not decompose organic matter. Here, we build on emerging evidence that points to significant consumption of labile C by fungi, and to the ability of ectomycorrhizal fungi to decompose organic matter, to show that labile C constitutes a major and presently underrated source of C for the soil food web. We use a simple model describing the dynamics of a recalcitrant and a labile C pool and their consumption by fungi and bacteria to show that fungal and bacterial populations can coexist in a stable state with large inputs into the labile C pool and a high fungal use of labile C. We propose a new conceptual model for the bottom trophic level of the soil food web, with organic C consisting of a continuous pool rather than two or three distinct pools, and saprotrophic fungi using substantial amounts of labile C. Incorporation of these concepts will increase our understanding of soil food web dynamics and functioning under changing conditions.

Soil food web properties explain ecosystem services across European land use systems.

Intensive land use reduces the diversity and abundance of many soil biota, with consequences for the processes that they govern and the ecosystem services that these processes underpin. Relationships between soil biota and ecosystem processes have mostly been found in laboratory experiments and rarely are found in the field. Here, we quantified, across four countries of contrasting climatic and soil conditions in Europe, how differences in soil food web composition resulting from land use systems (intensive wheat rotation, extensive rotation, and permanent grassland) influence the functioning of soils and the ecosystem services that they deliver. Intensive wheat rotation consistently reduced the biomass of all components of the soil food web across all countries. Soil food web properties strongly and consistently predicted processes of C and N cycling across land use systems and geographic locations, and they were a better predictor of these processes than land use. Processes of carbon loss increased with soil food web properties that correlated with soil C content, such as earthworm biomass and fungal/bacterial energy channel ratio, and were greatest in permanent grassland. In contrast, processes of N cycling were explained by soil food web properties independent of land use, such as arbuscular mycorrhizal fungi and bacterial channel biomass. Our quantification of the contribution of soil organisms to processes of C and N cycling across land use systems and geographic locations shows that soil biota need to be included in C and N cycling models and highlights the need to map and conserve soil biodiversity across the world.

Intensive agriculture reduces soil biodiversity across Europe.

Soil biodiversity plays a key role in regulating the processes that underpin the delivery of ecosystem goods and services in terrestrial ecosystems. Agricultural intensification is known to change the diversity of individual groups of soil biota, but less is known about how intensification affects biodiversity of the soil food web as a whole, and whether or not these effects may be generalized across regions. We examined biodiversity in soil food webs from grasslands, extensive, and intensive rotations in four agricultural regions across Europe: in Sweden, the UK, the Czech Republic and Greece. Effects of land-use intensity were quantified based on structure and diversity among functional groups in the soil food web, as well as on community-weighted mean body mass of soil fauna. We also elucidate land-use intensity effects on diversity of taxonomic units within taxonomic groups of soil fauna. We found that between regions soil food web diversity measures were variable, but that increasing land-use intensity caused highly consistent responses. In particular, land-use intensification reduced the complexity in the soil food webs, as well as the community-weighted mean body mass of soil fauna. In all regions across Europe, species richness of earthworms, Collembolans, and oribatid mites was negatively affected by increased land-use intensity. The taxonomic distinctness, which is a measure of taxonomic relatedness of species in a community that is independent of species richness, was also reduced by land-use intensification. We conclude that intensive agriculture reduces soil biodiversity, making soil food webs less diverse and composed of smaller bodied organisms. Land-use intensification results in fewer functional groups of soil biota with fewer and taxonomically more closely related species. We discuss how these changes in soil biodiversity due to land-use intensification may threaten the functioning of soil in agricultural production systems.

Trade-offs in soil microbial functions and soil health in agroecosystems.

Soil microbial communities play pivotal roles in maintaining soil health in agroecosystems. However, how the delivery of multiple microbial functions in agroecosystems is maintained remains poorly understood. This may put us at risk of incurring unexpected trade-offs between soil functions. We elucidate how interactions between soil microbes can lead to trade-offs in the functioning of agricultural soils. Interactions within soil microbial communities can result in not only positive but also neutral and negative relationships among soil functions. Altering soil conditions through soil health-improving agricultural management can alleviate these functional trade-offs by promoting the diversity and interrelationships of soil microbes, which can help to achieve more productive and sustainable agroecosystems.

Heritable microbiome variation is correlated with source environment in locally adapted maize varieties.

Beneficial interactions with microorganisms are pivotal for crop performance and resilience. However, it remains unclear how heritable the microbiome is with respect to the host plant genotype and to what extent host genetic mechanisms can modulate plant-microbiota interactions in the face of environmental stresses. Here we surveyed 3,168 root and rhizosphere microbiome samples from 129 accessions of locally adapted Zea, sourced from diverse habitats and grown under control and different stress conditions. We quantified stress treatment and host genotype effects on the microbiome. Plant genotype and source environment were predictive of microbiome abundance. Genome-wide association analysis identified host genetic variants linked to both rhizosphere microbiome abundance and source environment. We identified transposon insertions in a candidate gene linked to both the abundance of a keystone bacterium Massilia in our controlled experiments and total soil nitrogen in the source environment. Isolation and controlled inoculation of Massilia alone can contribute to root development, whole-plant biomass production and adaptation to low nitrogen availability. We conclude that locally adapted maize varieties exert patterns of genetic control on their root and rhizosphere microbiomes that follow variation in their home environments, consistent with a role in tolerance to prevailing stress.

A slow-fast trait continuum at the whole community level in relation to land-use intensification.

Organismal functional strategies form a continuum from slow- to fast-growing organisms, in response to common drivers such as resource availability and disturbance. However, whether there is synchronisation of these strategies at the entire community level is unclear. Here, we combine trait data for >2800 above- and belowground taxa from 14 trophic guilds spanning a disturbance and resource availability gradient in German grasslands. The results indicate that most guilds consistently respond to these drivers through both direct and trophically mediated effects, resulting in a 'slow-fast' axis at the level of the entire community. Using 15 indicators of carbon and nutrient fluxes, biomass production and decomposition, we also show that fast trait communities are associated with faster rates of ecosystem functioning. These findings demonstrate that 'slow' and 'fast' strategies can be manifested at the level of whole communities, opening new avenues of ecosystem-level functional classification.

Root litter decomposition is suppressed in species mixtures and in the presence of living roots.

Plant species diversity and identity can significantly modify litter decomposition, but the underlying mechanisms remain elusive, particularly for root litter. Here, we aimed to disentangle the mechanisms by which plant species diversity alters root litter decomposition. We hypothesised that (1) interactions between species in mixed communities result in litter that decomposes faster than litter produced in monocultures; (2) litter decomposition is accelerated in the presence of living plants, especially when the litter and living plant identities are matched (known as home-field advantage).Monocultures and a mixture of four common grassland species were established to obtain individual litter and a 'natural' root litter mixture. An 'artificial' mixed litter was created using litter from monocultures, mixed in the same proportions as the species composition in the natural litter mixtures based on qPCR measurements. These six root litter types were incubated in four monocultures, a four-species mixture and an unplanted soil.Root decomposition was strongly affected by root litter identity and the presence, but not diversity, of living roots. Mixed-species litter decomposed slower than expected based on the decomposition of single-species litters. In addition, the presence of living roots suppressed decomposition independent of the match between litter and living plant identities. Decomposition was not significantly different between the 'natural' and 'artificial' root litter mixtures, indicating that root-root interactions in species mixtures did not affect root chemical quality. Synthesis. Suppressed decomposition in the presence of living roots indicates that interactions between microbial communities associated with living roots and root litter control root litter decomposition. As we found no support for the importance of home-field advantage or interspecific root interactions in modifying decomposition, suppressed decomposition of mixed-species litter seems to be primarily driven by chemical rather than biotic interactions.

Fossil-fuel-dependent scenarios could lead to a significant decline of global plant-beneficial bacteria abundance in soils by 2100.

Exploiting the potential benefits of plant-associated microbes represents a sustainable approach to enhancing crop productivity. Plant-beneficial bacteria (PBB) provide multiple benefits to plants. However, the biogeography and community structure remain largely unknown. Here we constructed a PBB database to couple microbial taxonomy with their plant-beneficial traits and analysed the global atlas of potential PBB from 4,245 soil samples. We show that the diversity of PBB peaks in low-latitude regions, following a strong latitudinal diversity gradient. The distribution of potential PBB was primarily governed by environmental filtering, which was mainly determined by local climate. Our projections showed that fossil-fuel-dependent future scenarios would lead to a significant decline of potential PBB by 2100, especially biocontrol agents (-1.03%) and stress resistance bacteria (-0.61%), which may potentially threaten global food production and (agro)ecosystem services.