Humans are driving biodiversity change, which also alters community functional traits. However, how changes in the functional traits of the community alter ecosystem functions-especially belowground-remains an important gap in our understanding of the consequences of biodiversity change. We test hypotheses for how the root traits of the root economics space (composed of the collaboration and conservation gradients) are associated with proxies for ecosystem functioning across grassland and forest ecosystems in both observational and experimental datasets from 810 plant communities. First, we assessed whether community-weighted means of the root economics space traits adhered to the same trade-offs as species-level root traits. Then, we examined the relationships between community-weighted mean root traits and aboveground biomass production, root standing biomass, soil fauna biomass, soil microbial biomass, decomposition of standard and plot-specific material, ammonification, nitrification, phosphatase activity, and drought resistance. We found evidence for a community collaboration gradient but not for a community conservation gradient. Yet, links between community root traits and ecosystem functions were more common than we expected, especially for aboveground biomass, microbial biomass, and decomposition. These findings suggest that changes in species composition, which alter root trait means, will in turn affect critical ecosystem functions.
Trait-based approaches have been increasingly used to relate plants to soil microbial communities. Using the recently described root economics space as an approach to explain the structure of soil-borne fungal communities, our study in a grassland diversity experiment reveals distinct root trait strategies at the plant community level. In addition to significant effects of plant species richness, we show that the collaboration and conservation gradient are strong drivers of the composition of the different guilds of soil fungi. Saprotrophic fungi are most diverse in species-rich plant communities with 'slow' root traits, whereas plant pathogenic fungi are most diverse and abundant in communities with 'fast' and 'DIY' root traits. Fungal biomass is strongly driven by plant species richness. Our results illustrate that the root economics space and plant species richness jointly determine the effects of plants on soil fungal communities and their potential role in plant fitness and ecosystem functioning.
Plant-parasitic nematodes are harmful pathogens for many agricultural crops. Within this category, root-knot nematodes (RKN, Meloidogyne spp.) are worldwide regarded as the most impactful because of their wide geographical distribution and their polyphagous nature. Host plant resistances against RKN have been successfully introduced in a few crops only. As the use of nematicides is becoming increasingly restricted because of environmental and human health concerns, there is a need for alternative strategies to control RKN. One such approach is the stimulation of local nematode antagonists. We investigated this in an experimental field setting with two main variables: density of the Columbia root-knot nematode Meloidogyne chitwoodi, and the type of cover crop. For each of the three M. chitwoodi densities, the effects of ten cover crop treatments were tested on both the resident (DNA) and the active (RNA) fractions of the bacterial and fungal communities. In our analyses, we focused on changes in the abundance of plant-parasitic nematode antagonists. From the eight bacterial and 26 fungal genera known from global literature to harbour potential antagonists of plant-parasitic nematodes, we detected respectively five and 14 genera in our agricultural field. Among the bacterial genera, four genera were shown to comprise bacterial species for which nematode antagonism has been documented. The fungal genera included facultative nematode parasites (e.g., Arthrobotrys spp.), endophytes strengthening host defences (e.g., Acremonium spp.), as well as multiple obligatory nematophagous species. This study revealed that conventionally managed arable fields may harbour an unexpectedly high diversity of nematode antagonists. Multiple antagonists were stimulated by cover crops in a cover crop-specific manner, and, to a lesser extent, by increased RKN densities. The richness in putative nematode antagonists did not translate into M. chitwoodi suppression, and currently we are investigating whether this relates to the facultative nematophagous lifestyle of most of these antagonists.
Despite recent advances in plant trait ecology, we identified a knowledge gap in understanding how plants strategize to cope with severe and recurrent disturbances. Here, we propose a new classification system based on three hierarchical binary attributes: woodiness, reflecting longevity of plant structures; clonality, indicating the ability to regenerate from both above- and belowground organs; and resprouting ability, referring to the ability to replace aboveground organs. This framework results in six Belowground Persistence Types (BPTs): 1, herbaceous seeder; 2, herbaceous non-clonal resprouter; 3, herbaceous clonal resprouter; 4, woody seeder; 5, woody non-clonal resprouter; and 6, woody clonal resprouter. This proposed classification system opens new avenues for research, especially concerning plant distributions in a world experiencing increasingly frequent and severe disturbance events.
Plants release a substantial fraction of their photosynthesized carbon into the rhizosphere as root exudates that drive microbiome assembly. Deciphering how plants modulate the composition and activities of rhizosphere microbiota through root exudates is challenging, as no dedicated computational methods exist to systematically identify microbial root exudate catabolic pathways. Here, we integrate published information on catabolic genes in bacteria that contribute to their rhizosphere competence and develop the rhizoSMASH algorithm for genome-synteny-based annotation of rhizosphere-competence-related catabolic gene clusters (rCGCs) in bacteria with 58 curated detection rules. Our analysis reveals heterogeneity in rCGC prevalence both across and within plant-associated bacterial taxa, indicating extensive niche specialization. Furthermore, we demonstrate the predictive value of the presence or absence of rCGCs for rhizosphere competence in machine learning with two case studies. rhizoSMASH provides an extensible framework for studying rhizosphere bacterial catabolism, facilitating microbiome-assisted breeding approaches for sustainable agriculture.
Our symposium explored the relationships between biodiversity and disease ecology across plant and animal systems. During our current period of global biodiversity loss, researchers are uncovering how these losses affect disease dynamics in ecosystems, influencing not only wild plants and animals but also agricultural systems and human health. While biodiversity is often assumed to reduce disease risk through the so-called “dilution effect,” research findings have been inconsistent, revealing important gaps in understanding. A major obstacle to developing a unified perspective has been the historical separation between plant and animal disease ecology research. Emerging from the PADDLE (Plant and Animal Diversity and Disease across Levels in Ecology) consortium, the symposium aimed to foster dialogue and promote cross-system comparisons to uncover broader ecological patterns and mechanisms. A central goal for the original consortium was to improve understanding of “host quality” and to develop shared terminology, leading to the creation of a conceptual model defining host quality components from a pathogen's perspective. The symposium contributions spanned a wide range of research topics, which coalesced into three key themes: the fundamental nature of hosts and host quality, the role of the environment, and the commonalities between plant and animal systems. Overall, the symposium highlighted the value of integrating diverse perspectives and methodologies to better address the challenges at the intersection of global change, biodiversity loss, and infectious disease risk.
The global food system accelerates biodiversity loss, which in turn undermines the resilience and sustainability of food production. Strategic, coordinated action across the food system’s diverse actors and networks is essential to drive structural change and reverse biodiversity loss.
Fine roots and their traits determine resource uptake from the soil, thus being fundamental for plant and ecosystem functioning. It has been five years since the concept of the root economics space (RES) has been developed to describe multidimensional fine-root trait coordination. The RES proposed a novel fungal collaboration gradient in addition to the established fast-slow gradient of resource conservation. This review addresses both researchers already using the RES and those newly introduced to the concept. Our objective is to evaluate the empirical support for the concept, explore trait extensions and implications for ecosystem functioning, and examine future prospects of the RES. We conducted a literature review of 134 papers working with the RES to quantitatively assess support for the concept and its two trait gradients. The RES, particularly the collaboration gradient, is widely supported across organizational levels, habitats and study designs. Multidimensionality in the trait space appears to be a universal pattern. We further map traits that have been added to the RES concept and discuss the special role of legumes and ecto- versus arbuscular mycorrhizal fungi. We conclude that the RES is a powerful concept to understand fine-root functional variation. Moving forward, we emphasize the need to integrate additional traits to develop a more comprehensive framework for understanding plant and ecosystem functioning.
Cover crops are used in cropping systems to enhance ecosystem services, such as soil resilience to erosion or microbial activity. Different cover crops are selected to steer specific processes, but whether cover crop mixtures have an added value over monocultures remains debated. Here, we investigated if cover crop mixtures accumulate soil microbiotas distinct from those of monocultures, potentially leading to more varied microbially-driven soil functions. We performed a field experiment at three locations in the Netherlands, each including nine cover crop monocultures, five- and eight-species mixtures, and a fallow control. After three months, we measured cover crop biomass and profiled soil bacterial, fungal, and arbuscular mycorrhizal fungal communities via amplicon sequencing. The different crop monocultures produced similar biomass across all three locations, and mixtures had average productivity compared to monocultures. The diversity and community structure of soil microbial communities was primarily determined by the geographical location, and then by cover crop treatment at each location. Although the cover crop species affected the soil microbiome differently, cover crop mixtures did neither increase microbial diversity nor the overall community differentiation compared to monocultures. Our results suggest that mixing cover crop species does not significantly influence microbially-driven soil functions, at least in short-term crop rotations.
Plant roots respond to soil nutrient availability, but also to the identity of neighbor plants, and root exudates play a role therein. However, how root exudates influence root behavior is not well understood. A sequence of eight experiments was designed to investigate whether and how root growth and distribution of maize (Zea mays L.) was affected when growing with neighboring wheat (Triticum aestivum L.). We focused on the role of 6-methoxy-benzoxazolin-2-one (MBOA), an important allelochemical in root exudates. We found that maize roots distributed away from neighboring wheat roots but not from other roots. Root length of maize was reduced by 37
Long-term research in grassland biodiversity experiments has provided empirical evidence that ecological and evolutionary processes are intertwined in determining both biodiversity–ecosystem functioning (BEF) and biodiversity–stability relationships. Focusing on plant diversity, we hypothesize that multifunctional stability is highest in high-diversity plant communities and that biodiversity–stability relationships increase over time due to a variety of forms of ecological complementarity including the interaction with other biota above and below ground. We introduce the multiple-mechanisms hypothesis of biodiversity–stability relationships suggesting that it is not an individual mechanism that drives long-term biodiversity effects on ecosystem functioning and stability but that several intertwined processes produce increasingly positive ecosystem effects. The following six mechanisms are important. Low-diversity plant communities accumulate more plant antagonists over time (1), and use resources less efficiently and have more open, leaky nutrient cycles (2). Conversely, high-diversity plant communities support a greater diversity and activity of beneficial interaction partners across trophic levels (3); diversify in their traits over time and space, within and across species, to optimize temporal (intra- and interannual) and spatial complementarity (4), create a more stable microclimate (5), and foster higher top-down control of aboveground and belowground herbivores by predators (6). In line with the observation that different species play unique roles in ecosystems that are dynamic and multifaceted, the particular mechanism contributing most to the higher performance and stability of diverse plant communities might differ across ecosystem functions, years, locations, and environmental change scenarios. This indicates “between-context insurance” or “across-context complementarity” of different mechanisms. We introduce examples of experiments that will be conducted to test our hypotheses and which might inspire additional work.
Intensive agriculture often comes at the expense of soil health. A shift towards practices that foster soil health will support yield and defences against pests and diseases. Growing crops in monoculture is the standard in modern agriculture, though strip-cropping, in which different crops are planted in strips, is a promising strategy in the transition towards sustainable agriculture. Increasing crop diversity is hypothesized to positively influence arbuscular mycorrhizal fungi (AMF), thereby enhancing soil health, but the mechanisms by which AMF-plant symbioses contribute to higher yields and reduced pest populations in strip-cropping systems remain unclear. We used a green-house experiment with potato plants to explore the soil legacy effects of mono-cropping versus strip-cropping systems, AMF inoculation and aphid infestation on AMF root colonization, the induction of plant defences (untargeted LCMS-based metabolomics), aphid population size and potato yield. We found that potato plants grown in strip-cropping soil had higher AMF colonization than plants grown in mono-cropping soil. Potato plants grown in strip-cropping soil also had higher shoot nitrogen content, increased solamargine levels, and reduced aphid populations. AMF root colonization was only enhanced by the addition of commercial AMF in mono-cropping soils. Potato plant metabolites were affected by strip-cropping soil, including jasmonic acid (JA) derivatives. Structural equation models revealed that strip-cropping soil directly reduced aphid populations and also had a negative direct effect on the JA precursor OPC-8, and hydroxyJA-glucosides, indicating complex effects of strip-cropping soils on JA-inducible plant defences. Indirect benefits of strip-cropping soil and AMF inoculation on tuber yield were mediated by their direct positive effects on plant nitrogen content. Our results emphasize the potential of strip-cropping to enhance AMF root colonization in the field. We show that soil legacy effects of strip-cropping alter the plant metabolome in ways that suppress of aphid populations. Strip-cropping legacy effects are the result of crop diversity, crop neighbour and edge effects resulting from crop management practices. While the mechanisms by which soil from strip-cropping supresses pest populations still need to be identified, our study underscores the potential for strip-cropping to enhance pest control and yield via soil mediated processes. Read the free Plain Language Summary for this article on the Journal blog.
Cover crops are used in agriculture to minimize soil erosion, prevent nutrient leaching and increase soil organic matter content. Cover crops can also be grown to stimulate the soil microbial community to improve soil bio-logical conditions. Despite their widespread use, little is known about the impact of different cover crop species on the composition and activity of the soil microbiome. Here we investigate the effect of distinct cover crop species on the rhizosphere microbiome and characterize both the resident (ribosomal (r)DNA-based) and the potentially active (rRNA-based) fractions of the bacterial, fungal, protist and metazoan communities in the cover crops rhizosphere. We conducted a field experiment using 70-l bottomless containers in which we grew ten monocultures of commonly used cover crop species belonging to five plant families, and an unplanted control treatment (fallow). The total DNA and RNA were extracted from soil and the bacterial, fungal, protistan and metazoan communities were characterized using Illumina MiSeq sequencing. We found that all cover crop species significantly impacted the resident and the potentially active microbial communities in their rhizo-spheres. Cover crops exerted distinct selection strengths on the native microbial communities. For individual cover crops, the impacts on the resident and the potentially active microbial communities differed while showing similar overall tendencies. Oilseed radish (Brassicaceae) was shown to provoke the strongest microbial shifts, in part attributable to a promotion of the bacterial family Pseudomonadaceae and a repression of Microascaceae in the rhizosphere. Lentil (Fabaceae) induced a widespread stimulation of fungal taxa, including Trichocomaceae and fungal members of the Glomerales order, whereas black oat and hybrid ryegrass (both Poaceae) gave rise to relatively mild changes in the soil microbial communities. Analyses of rRNA-based rhizobiome data revealed that, except for phacelia, all cover crops induced an increase in microbial network complexity as compared to the fallow control. Data presented here provide a broad baseline for the effects of cover crops on four organismal groups, which may facilitate future cover crop selection to advance soil health.
Soil-borne fungal plant pathogens lead to worldwide economic yield losses. However, despite the agricultural importance of the North China Plain (NCP), little is known about the occurrence and severity of soil-borne fungal pathogens that could potentially affect the yields of three main crops in this area: wheat, maize and soybean. By combining searches in public databases, we identified a set of main soil-borne fungal pathogen species potentially affecting crop production in the NCP. We investigated their distribution patterns at three scales: globally, in China and in the NCP, and evaluated how these patterns were determined by a range of variables related to climate, spatial drivers and crop area density of the three crop species. We found 25 main soil-borne fungal pathogens that could potentially affect the yields of wheat, maize and soybean in the NCP. Twenty of these fungal pathogens were prevalent across the globe, and 13 were very frequent in the NCP. Significant positive relationships between pathogen prevalence and crop area density were only found for two specialist pathogens. Our work provides an overview of the main soil-borne fungal pathogens in one of China’s most intensively cultivated regions, shedding light on potential, previously overlooked, fungal threats for agricultural production in the area. This baseline information may contribute to the development of sustainable management strategies aimed at mitigating disease outbreaks caused by soil-borne pathogens in the future.
Apart from improving the physical and chemical condition of arable soils, cover crops have the potential to boost and activate selected soil microbiota that could contribute to improved nutrient cycling and strengthened disease suppressiveness. However, a main crop can only benefit from cover crop-induced microbial shifts if these persist until the onset of the main growing season. Here, we map the persistence of microbiome changes by cover crops over time. We performed a field experiment on a sandy soil with ten different cover crop monocultures belonging to five plant families, one cover crop mixture and a fallow control. Cover crops were grown for 4.5 months under field conditions in 70-L bottomless containers in a random block design with eight replications. We studied the total (DNA-based) and the potentially active (RNA-based) microbial fractions at the onset of the main growing season, and just after the harvest of the main crop, potato (respectively 3.5 and 10 months after cover crop termination), through MiSeq sequencing. All cover crops tested induced shifts in the soil microbiome that lasted at least until the onset of the main growing season. Cover crop treatments gave rise to species and even cultivar-specific microbial footprints, and - although roughly the same trends were observed - DNA-based microbial shifts were not necessarily paralleled by similar changes at RNA level. We conclude that cover crops have the potential to act as handles to steer the soil microbiome in a way that is supportive of sustainable crop production.
Root-associated fungi could play a role in determining both the positive relationship between plant diversity and productivity in experimental grasslands, and its strengthening over time. This hypothesis assumes that specialized pathogenic and mutualistic fungal communities gradually assemble over time, enhancing plant growth more in species-rich than in species-poor plots. To test this hypothesis, we used high-throughput amplicon sequencing to characterize root-associated fungal communities in experimental grasslands of 1 and 15 years of age with varying levels of plant species richness. Specifically, we tested whether the relationship between fungal communities and plant richness and productivity becomes stronger with the age of the experimental plots. Our results showed that fungal diversity increased with plant diversity, but this relationship weakened rather than strengthened over the two time points. Contrastingly, fungal community composition showed increasing associations with plant diversity over time, suggesting a gradual build-up of specific fungal assemblages. Analyses of different fungal guilds showed that these changes were particularly marked in pathogenic fungi, whose shifts in relative abundance are consistent with the pathogen dilution hypothesis in diverse plant communities. Our results suggest that root-associated fungal pathogens play more specific roles in determining the diversity-productivity relationship than other root-associated plant symbionts.
Recent studies on root traits have shown that there are two axes explaining trait variation belowground: the collaboration axis with mycorrhizal partners and the conservation ('fast - slow') axis. However, it is yet unknown whether these trait axes affect the assembly of soilborne fungi. We expect saprotrophic fungi to link to the conservation axis of root traits, whereas pathogenic and arbuscular mycorrhizal fungi link to the collaboration axis, but in opposite directions, as arbuscular mycorrhizal fungi might provide pathogen protection. To test these hypotheses, we sequenced rhizosphere fungal communities and measured root traits in monocultures of 25 grassland plant species, differing in age. Within the fungal guilds, we evaluated fungal species richness, relative abundance and community composition. Contrary to our hypotheses, fungal diversity and relative abundance were not strongly related to the root trait axes. However, saprotrophic fungal community composition was affected by the conservation gradient and pathogenic community composition by the collaboration gradient. The rhizosphere AMF community composition did not change along the collaboration gradient, even though the root trait axis was in line with the root mycorrhizal colonization rate. Overall, our results indicate that in the long term, the root trait axes are linked with fungal community composition.
Background Plant–soil feedback (PSF) has gained increasing interest in agricultural systems. An important question is whether PSF differs between different cropping systems. Few attempts have yet been made to identify the pathogen species involved in negative PSF. Here, we hypothesize that the strength of negative PSF experienced by a crop species is determined by the relative abundance of host-specific soil-borne pathogenic fungi, that is in turn driven by the crop’s relative abundance (in time). Methods We performed a PSF experiment, with different soils originating from three cropping systems in the North China Plain and three crop species (wheat, maize, soybean) in a full factorial design. Soil fungal community composition and relative abundance of fungal (pathogen) species in each treatment was identified by metabarcoding using ITS (Internal Transcribed Spacer) sequencing. Results PSF ranged from negative for wheat, neutral to negative for soybean and neutral to positive for maize, but the former density of a crop in a particular cropping system did not affect the strength of PSF experienced by each of the three. No relationships between fungal pathogen abundance and PSF were found, but we did find a surprisingly large enrichment across steps of the experiment of Chaetomium spp., a known cellulose-degrading fungus. This may be explained by addition of filter paper on the bottom of the pots. Conclusions Our results suggest that the strength of PSF in these crops is not related to the relative abundance of specific fungal pathogens. However, we cannot rule out that our results were affected by the high abundance of one particular cellulose-degrading fungus. This highlights both the need to stop the practice of using filter paper in pot experiments, as well as the relevance of assessing the identity, relative abundance and potential functions of fungal taxa in PSF experiments.
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.