Symbiont plasticity as a driver of plant success.

We discuss which plant species are likely to become winners, that is achieve the highest global abundance, in changing landscapes, and whether plant-associated microbes play a determining role. Reduction and fragmentation of natural habitats in historic landscapes have led to the emergence of patchy, hybrid landscapes, and novel landscapes where anthropogenic ecosystems prevail. In patchy landscapes, species with broad niches are favoured. Plasticity in the degree of association with symbiotic microbes may contribute to broader plant niches and optimization of symbiosis costs and benefits, by downregulating symbiosis when it is unnecessary and upregulating it when it is beneficial. Plasticity can also be expressed as the switch from one type of mutualism to another, for example from nutritive to defensive mutualism with increasing soil fertility and the associated increase in parasite load. Upon dispersal, wide mutualistic partner receptivity is another facet of symbiont plasticity that becomes beneficial, because plants are not limited by the availability of specialist partners when arriving at new locations. Thus, under conditions of global change, symbiont plasticity allows plants to optimize the activity of mutualistic relationships, potentially allowing them to become winners by maximizing geographic occupancy and local abundance.

Niche types and community assembly.

Studies of niche differentiation and biodiversity often focus on a few niche dimensions due to the methodological challenge of describing hyperdimensional niche space. However, this may limit our understanding of community assembly processes. We used the full spectrum of realized niche types to study arbuscular mycorrhizal fungal communities: distinguishing abiotic and biotic, and condition and resource, axes. Estimates of differentiation in relation to different niche types were only moderately correlated. However, coexisting taxon niches were consistently less differentiated than expected, based on a regional null model, indicating the importance of habitat filtering at that scale. Nonetheless, resource niches were relatively more differentiated than condition niches, which is consistent with the effect of a resource niche-based coexistence mechanism. Considering niche types, and in particular distinguishing resource and condition niches, provides a more complete understanding of community assembly, compared with studying individual niche axes or the full niche.

A trait-based framework linking the soil metabolome to plant-soil feedbacks.

By modifying the biotic and abiotic properties of the soil, plants create soil legacies that can affect vegetation dynamics through plant-soil feedbacks (PSF). PSF are generally attributed to reciprocal effects of plants and soil biota, but these interactions can also drive changes in the identity, diversity and abundance of soil metabolites, leading to more or less persistent soil chemical legacies whose role in mediating PSF has rarely been considered. These chemical legacies may interact with microbial or nutrient legacies to affect species coexistence. Given the ecological importance of chemical interactions between plants and other organisms, a better understanding of soil chemical legacies is needed in community ecology. In this Viewpoint, we aim to: highlight the importance of belowground chemical interactions for PSF; define and integrate soil chemical legacies into PSF research by clarifying how the soil metabolome can contribute to PSF; discuss how functional traits can help predict these plant-soil interactions; propose an experimental approach to quantify plant responses to the soil solution metabolome; and describe a testable framework relying on root economics and seed dispersal traits to predict how plant species affect the soil metabolome and how they could respond to soil chemical legacies.

Metabarcoding of soil environmental DNA to estimate plant diversity globally.

Introduction: Traditional approaches to collecting large-scale biodiversity data pose huge logistical and technical challenges. We aimed to assess how a comparatively simple method based on sequencing environmental DNA (eDNA) characterises global variation in plant diversity and community composition compared with data derived from traditional plant inventory methods. Methods: We sequenced a short fragment (P6 loop) of the chloroplast trnL intron from from 325 globally distributed soil samples and compared estimates of diversity and composition with those derived from traditional sources based on empirical (GBIF) or extrapolated plant distribution and diversity data. Results: Large-scale plant diversity and community composition patterns revealed by sequencing eDNA were broadly in accordance with those derived from traditional sources. The success of the eDNA taxonomy assignment, and the overlap of taxon lists between eDNA and GBIF, was greatest at moderate to high latitudes of the northern hemisphere. On average, around half (mean: 51.5% SD 17.6) of local GBIF records were represented in eDNA databases at the species level, depending on the geographic region. Discussion: eDNA trnL gene sequencing data accurately represent global patterns in plant diversity and composition and thus can provide a basis for large-scale vegetation studies. Important experimental considerations for plant eDNA studies include using a sampling volume and design to maximise the number of taxa detected and optimising the sequencing depth. However, increasing the coverage of reference sequence databases would yield the most significant improvements in the accuracy of taxonomic assignments made using the P6 loop of the trnL region.

Plant-soil feedback under drought: does history shape the future?

Plant-soil feedback (PSF) is widely recognised as a driver of plant community composition, but understanding of its response to drought remains in its infancy. Here, we provide a conceptual framework for the role of drought in PSF, considering plant traits, drought severity, and historical precipitation over ecological and evolutionary timescales. Comparing experimental studies where plants and microbes do or do not share a drought history (through co-sourcing or conditioning), we hypothesise that plants and microbes with a shared drought history experience more positive PSF under subsequent drought. To reflect real-world responses to drought, future studies need to explicitly include plant-microbial co-occurrence and potential co-adaptation and consider the precipitation history experienced by both plants and microbes.

Global diversity and distribution of nitrogen-fixing bacteria in the soil.

Our knowledge of microbial biogeography has advanced in recent years, yet we lack knowledge of the global diversity of some important functional groups. Here, we used environmental DNA from 327 globally collected soil samples to investigate the biodiversity patterns of nitrogen-fixing bacteria by focusing on the nifH gene but also amplifying the general prokaryotic 16S SSU region. Globally, N-fixing prokaryotic communities are driven mainly by climatic conditions, with most groups being positively correlated with stable hot or seasonally humid climates. Among soil parameters, pH, but also soil N content were most often shown to correlate with the diversity of N-fixer groups. However, specific groups of N-fixing prokaryotes show contrasting responses to the same variables, notably in Cyanobacteria that were negatively correlated with stable hot climates, and showed a U-shaped correlation with soil pH, contrary to other N-fixers. Also, the non-N-fixing prokaryotic community composition was differentially correlated with the diversity and abundance of N-fixer groups, showing the often-neglected impact of biotic interactions among bacteria.

Light availability and plant shade tolerance modify plant-microbial interactions and feedbacks in subtropical trees.

Plant-soil feedbacks (PSFs) are an important mechanism of species coexistence in forest communities. However, evidence remains limited for how light availability regulates PSFs in species with different shade tolerance via changes in plant-microbial interactions. Here we tested in a glasshouse experiment how PSFs changed as a function of light availability and tree shade tolerance. Soil bacterial and fungal communities were profiled using the 16S rRNA and ITS2 gene sequencing, respectively. Under low light, individual PSFs were positively related to shade tolerance, while the least shade-tolerant species produced the most positive PSFs under high light. Pairwise PSFs between species with contrasting shade tolerance were strongly positive under high light but negative under low light, thereby promoting the dominance of less shade-tolerant species in forest gaps and species coexistence under closed canopy, respectively. Under high light, PSFs were related to soil microbial composition and diversity, with the relative abundance of arbuscular mycorrhizal fungi being the primary driver of PSFs. Under low light, none of soil microbial properties were significantly related to PSFs. These findings indicate PSFs and plant shade tolerance interact to promote species coexistence and improve our understanding of how soil microbes contribute to variation in PSFs.

The multiscale feedback theory of biodiversity.

Plants and their environments engage in feedback loops that not only affect individuals, but also scale up to the ecosystem level. Community-level negative feedback facilitates local diversity, while the ability of plants to engineer ecosystem-wide conditions for their own benefit enhances local dominance. Here, we suggest that local and regional processes influencing diversity are inherently correlated: community-level negative feedback predominates among large species pools formed under historically common conditions; ecosystem-level positive feedback is most apparent in historically restricted habitats. Given enough time and space, evolutionary processes should lead to transitions between systems dominated by positive and negative feedbacks: species-poor systems should become richer due to diversification of dominants and adaptation of subordinates; however, new monodominants may emerge due to migration or new adaptations.

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.

Dominance, diversity, and niche breadth in arbuscular mycorrhizal fungal communities.

Classical theory identifies resource competition as the major structuring force of biotic communities and predicts that (i) levels of dominance and richness in communities are inversely related, (ii) narrow niches allow dense "packing" in niche space and thus promote diversity, and (iii) dominants are generalists with wide niches, such that locally abundant taxa also exhibit wide distributions. Current empirical support, however, is mixed. We tested these expectations using published data on arbuscular mycorrhizal (AM) fungal community composition worldwide. We recorded the expected negative relationship between dominance and richness and, to a degree, the positive association between local and global dominance. However, contrary to expectations, dominance was pronounced in communities where more specialists were present and, conversely, richness was higher in communities with more generalists. Thus, resource competition and niche packing appear to be of limited importance in AM fungal community assembly; rather, patterns of dominance and diversity seem more consistent with habitat filtering and stochastic processes.

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.

Functional diversity and identity of plant genotypes regulate rhizodeposition and soil microbial activity.

Our understanding of the linkages between plant diversity and soil carbon and nutrient cycling is primarily derived from studies at the species level, while the importance and mechanisms of diversity effects at the genotype level are poorly understood. Here we examine how genotypic diversity and identity, and associated variation in functional traits, within a common grass species, Anthoxanthum odoratum, modified rhizodeposition, soil microbial activity and litter decomposition. Root litter quality was not significantly affected by plant genotypic diversity, but decomposition was enhanced in soils with the legacy of higher genotypic diversity. Plant genotypic diversity and identity modified rhizodeposition and associated microbial activity via two independent pathways. Plant genotypic diversity enhanced soil functioning via positive effects on variation in specific leaf area and total rhizodeposition. Genotype identity affected both rhizodeposit quantity and quality, and these effects were mediated by differences in mean specific leaf area, shoot mass and plant height. Rhizodeposition was more strongly predicted by aboveground than belowground traits, suggesting strong linkages between photosynthesis and root exudation. Our study demonstrates that functional diversity and identity of plant genotypes modulates belowground carbon supply and quality, representing an important but overlooked pathway by which biodiversity affects ecosystem functioning.

An integrated framework of plant form and function: the belowground perspective.

Plant trait variation drives plant function, community composition and ecosystem processes. However, our current understanding of trait variation disproportionately relies on aboveground observations. Here we integrate root traits into the global framework of plant form and function. We developed and tested an overarching conceptual framework that integrates two recently identified root trait gradients with a well-established aboveground plant trait framework. We confronted our novel framework with published relationships between above- and belowground trait analogues and with multivariate analyses of above- and belowground traits of 2510 species. Our traits represent the leaf and root conservation gradients (specific leaf area, leaf and root nitrogen concentration, and root tissue density), the root collaboration gradient (root diameter and specific root length) and the plant size gradient (plant height and rooting depth). We found that an integrated, whole-plant trait space required as much as four axes. The two main axes represented the fast-slow 'conservation' gradient on which leaf and fine-root traits were well aligned, and the 'collaboration' gradient in roots. The two additional axes were separate, orthogonal plant size axes for height and rooting depth. This perspective on the multidimensional nature of plant trait variation better encompasses plant function and influence on the surrounding environment.

Root traits explain plant species distributions along climatic gradients yet challenge the nature of ecological trade-offs.

Ecological theory is built on trade-offs, where trait differences among species evolved as adaptations to different environments. Trade-offs are often assumed to be bidirectional, where opposite ends of a gradient in trait values confer advantages in different environments. However, unidirectional benefits could be widespread if extreme trait values confer advantages at one end of an environmental gradient, whereas a wide range of trait values are equally beneficial at the other end. Here, we show that root traits explain species occurrences along broad gradients of temperature and water availability, but model predictions only resembled trade-offs in two out of 24 models. Forest species with low specific root length and high root tissue density (RTD) were more likely to occur in warm climates but species with high specific root length and low RTD were more likely to occur in cold climates. Unidirectional benefits were more prevalent than trade-offs: for example, species with large-diameter roots and high RTD were more commonly associated with dry climates, but species with the opposite trait values were not associated with wet climates. Directional selection for traits consistently occurred in cold or dry climates, whereas a diversity of root trait values were equally viable in warm or wet climates. Explicit integration of unidirectional benefits into ecological theory is needed to advance our understanding of the consequences of trait variation on species responses to environmental change.

Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi.

The arbuscular mycorrhizal (AM) fungi are a globally distributed group of soil organisms that play critical roles in ecosystem function. However, the ecological niches of individual AM fungal taxa are poorly understood. We collected > 300 soil samples from natural ecosystems worldwide and modelled the realised niches of AM fungal virtual taxa (VT; approximately species-level phylogroups). We found that environmental and spatial variables jointly explained VT distribution worldwide, with temperature and pH being the most important abiotic drivers, and spatial effects generally occurring at local to regional scales. While dispersal limitation could explain some variation in VT distribution, VT relative abundance was almost exclusively driven by environmental variables. Several environmental and spatial effects on VT distribution and relative abundance were correlated with phylogeny, indicating that closely related VT exhibit similar niche optima and widths. Major clades within the Glomeraceae exhibited distinct niche optima, Acaulosporaceae generally had niche optima in low pH and low temperature conditions, and Gigasporaceae generally had niche optima in high precipitation conditions. Identification of the realised niche space occupied by individual and phylogenetic groups of soil microbial taxa provides a basis for building detailed hypotheses about how soil communities respond to gradients and manipulation in ecosystems worldwide.

The fungal collaboration gradient dominates the root economics space in plants.

Plant economics run on carbon and nutrients instead of money. Leaf strategies aboveground span an economic spectrum from "live fast and die young" to "slow and steady," but the economy defined by root strategies belowground remains unclear. Here, we take a holistic view of the belowground economy and show that root-mycorrhizal collaboration can short circuit a one-dimensional economic spectrum, providing an entire space of economic possibilities. Root trait data from 1810 species across the globe confirm a classical fast-slow "conservation" gradient but show that most variation is explained by an orthogonal "collaboration" gradient, ranging from "do-it-yourself" resource uptake to "outsourcing" of resource uptake to mycorrhizal fungi. This broadened "root economics space" provides a solid foundation for predictive understanding of belowground responses to changing environmental conditions.

Drought soil legacy overrides maternal effects on plant growth.

Maternal effects (i.e. trans-generational plasticity) and soil legacies generated by drought and plant diversity can affect plant performance and alter nutrient cycling and plant community dynamics. However, the relative importance and combined effects of these factors on plant growth dynamics remain poorly understood.We used soil and seeds from an existing plant diversity and drought manipulation field experiment in temperate grassland to test maternal, soil drought and diversity legacy effects, and their interactions, on offspring plant performance of two grassland species (Alopecurus pratensis and Holcus lanatus) under contrasting glasshouse conditions.Our results showed that drought soil legacy effects eclipsed maternal effects on plant biomass. Drought soil legacy effects were attributed to changes in both abiotic (i.e. nutrient availability) and biotic soil properties (i.e. microbial carbon and enzyme activity), as well as plant root and shoot atom 15N excess. Further, plant tissue nutrient concentrations and soil microbial C:N responses to drought legacies varied between the two plant species and soils from high and low plant diversity treatments. However, these diversity effects did not affect plant root or shoot biomass.These findings demonstrate that while maternal effects resulting from drought occur in grasslands, their impacts on plant performance are likely minor relative to drought legacy effects on soil abiotic and biotic properties. This suggests that soil drought legacy effects could become increasingly important drivers of plant community dynamics and ecosystem functioning as extreme weather events become more frequent and intense with climate change. A plain language summary is available for this article.

Fungal diversity regulates plant-soil feedbacks in temperate grassland.

Feedbacks between plants and soil microbial communities play an important role in vegetation dynamics, but the underlying mechanisms remain unresolved. Here, we show that the diversity of putative pathogenic, mycorrhizal, and saprotrophic fungi is a primary regulator of plant-soil feedbacks across a broad range of temperate grassland plant species. We show that plant species with resource-acquisitive traits, such as high shoot nitrogen concentrations and thin roots, attract diverse communities of putative fungal pathogens and specialist saprotrophs, and a lower diversity of mycorrhizal fungi, resulting in strong plant growth suppression on soil occupied by the same species. Moreover, soil properties modulate feedbacks with fertile soils, promoting antagonistic relationships between soil fungi and plants. This study advances our capacity to predict plant-soil feedbacks and vegetation dynamics by revealing fundamental links between soil properties, plant resource acquisition strategies, and the diversity of fungal guilds in soil.