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The importance of plant soil feedbacks (PSF) for above- and belowground multitrophic interactions is well recognized. However, most studies only condition soil for a short time before testing the feedback response. Here we investigate the influence of time of conditioning on soil microbiome composition, plant growth and metabolomics, and plant-insect interactions. We used soil collected from large outdoor mesocosms with monocultures of six species and investigated the temporal changes in the soil over a full year. Every two months we assessed the legacy effects of the soils on plant growth of one of the species (Jacobaea vulgaris) in a climate-controlled chamber. Each time we used tissue culture plants that were genetically identical. We also measured leaf herbivore performance and leaf metabolomes, as well as the abiotic and biotic soil properties. We show that the monoculture soils harboured different microbiomes, but that these varied over time. Growth of the test plants also varied over time and plants grew consistently less well in their own soil. The soil legacy effects on the leaf metabolome were less consistent and varied strongly over time. Networking analysis showed that soil bacteria had stronger effects on the leaf metabolome than fungi early on. However, after twelve months of conditioning only soil fungal community composition explained the metabolomic profiles of the leaves. Insect herbivory was not affected by soil conditioning, but decreased with increasing time of conditioning. Synthesis: Our results show that the biomass response of the test plants to soil conditioning remained consistent throughout the year, even though both the soil microbiome and leaf metabolomic responses to conditioned soil varied greatly over time. These soil-induced changes in the metabolome of plants over time can be an important driver of above-ground multitrophic interactions in nature. Our study demonstrates that the duration of conditioning has a strong

Plant-soil feedbacks are shaped by microbial legacies that plants leave in the soil. We tested the persistence of these legacies after subsequent colonization by the same or other plant species using 6 typical grassland plant species. Soil fungal legacies were detectable for months, but the current plant effect on fungi amplified in time. By contrast, in bacterial communities, legacies faded away rapidly and bacteria communities were influenced strongly by the current plant. However, both fungal and bacterial legacies were conserved inside the roots of the current plant species and their composition significantly correlated with plant growth. Hence, microbial soil legacies present at the time of plant establishment play a vital role in shaping plant growth even when these legacies have faded away in the soil due the growth of the current plant species. We conclude that soil microbiome legacies are reversible and versatile, but that they can create plant-soil feedbacks via altering the endophytic community acquired during early ontogeny.

Soil legacies mediated by plant species-specific microbial communities are major drivers of plant community dynamics. Most soil legacy studies focus on the role of pathogens and mutualists in driving these processes, while much less is known about plant litter-mediated changes to the soil microbial community. Here, we used an existing plant-soil feedback field experiment in which plant communities with different growth strategies (i.e., fast versus slow) and different proportions of functional groups (i.e., grasses versus forbs) were allowed to condition the soil over contrasting temporal scales (i.e., one versus two years) in a natural grassland. In the feedback phase, we removed the existent plant community, and replaced it with a standardized response plant community. We then tested the legacy effects of these different soil conditioning treatments on decomposition processes, nutrient cycling and soil decomposer community composition. Soil legacy effects on decomposition and the soil decomposer community composition were most evident right after the start of the feedback phase, but disappeared soon after the new community established. The soil conditioning time and years since disturbance affected most of the soil functions consistently, while no strong effects of plant functional group and plant growth strategy were found. We conclude that after disturbance, it is recovery time, not soil legacy effects, that is the most important factor driving soil functions.

In response to environmental conditions, plants can alter the performance of the next generation through maternal effects. Since plant–soil feedbacks (PSFs) influence soil conditions, PSFs likely create such intergenerational effects. We grew monocultures of three grass and three forb species in outdoor mesocosms. We then grew one of the six species, Hypochaeris radicata, in the conditioned soils and collected their seeds. We measured seed weight, carbon and nitrogen concentration, germination and seedling performance when grown on a common soil. We did not detect functional group intergenerational effects, but soils conditioned by different plant species affected H. radicata seed C to N ratios. There was a relationship between parent biomass in the differently conditioned soils and the germination rates of the offspring. However, these effects did not change offspring performance on a common soil. Our findings show that PSF effects changed seed quality and initial performance in a common grassland forb. We discuss the implications of our findings for multi‐generational plant–soil interactions, and highlight the need to further explore how PSF effects shape plant community dynamics over different generations and across a broad range of species and functional groups.

Changes in plant community composition can have long‐lasting consequences for ecosystem functioning. However, how the duration of plant growth of functionally distinct grassland plant communities influences abiotic and biotic soil properties and thus ecosystem functions is poorly known. In a field experiment, we established identical experimental subplots in two successive years comprising of fast‐ or slow‐growing grass and forb community mixtures with different forb:grass ratios. After one and two years of plant growth, we measured above‐ and belowground biomass, soil abiotic characteristics (pH, organic matter, soil nutrients), soil microbial properties (respiration, biomass, community composition), and nematode abundance. Fast‐ and slow‐growing plant communities did not differ in above‐ and belowground biomass. However, fast‐ and slow‐growing plant communities created distinct soil bacterial communities, whereas soil fungal communities differed most in 100% forb communities compared to other forb:grass ratio mixtures. Moreover, soil nitrate availability was higher after two years of plant growth, whereas the opposite was true for soil ammonium concentrations. Furthermore, total nematodes and especially bacterial‐feeding nematodes were more abundant after two years of plant growth. Our results show that plant community composition is a driving factor in soil microbial community assembly and that the duration of plant growth plays a crucial role in the establishment of plant community and functional group composition effects on abiotic and biotic soil ecosystem functioning under natural field conditions.

Understanding the causes of variation in foliar plant metabolomes is essential for our understanding of ecological interactions between plants and other organisms. It is well-accepted that foliar herbivory alters metabolites in leaves. However, soil (micro)organisms can also induce such changes. 2. We generated plant-specific soil legacies by growing 12 plant species individually in a common starting soil. Then we planted all plant species in all soils and exposed a subset to foliar herbivory. We then used 1 H nuclear magnetic resonance to analyse the shoot metabolomes of all responding plants. 3. Above-ground herbivory and soil legacies altered shoot metabolomes. In most plant species, soil legacy more strongly affected shoot metabolomes than foliar herbivory. 4. Synthesis. Our results show that plant-induced changes in soil alter metabolomes of plants that grow later in those soils. Such below-ground legacy effects can have far-stretching consequences for above-ground multitrophic interactions as these often depend on the plant chemical composition. Recently, plant–soil feedbacks have received considerable attention in ecological studies, and our study now highlights that these feedbacks can be an important determinant of the often unexplained intraspecific variation in chemical composition among plants.

Soil legacy effects are commonly highlighted as drivers of plant community dynamics and species co‐existence. However, experimental evidence for soil legacy effects of conditioning plant communities on responding plant communities under natural conditions is lacking. We conditioned 192 grassland plots using six different plant communities with different ratios of grasses and forbs and for different durations. Soil microbial legacies were evident for soil fungi, but not for soil bacteria, while soil abiotic parameters did not significantly change in response to conditioning. The soil legacies affected the composition of the succeeding vegetation. Plant communities with different ratios of grasses and forbs left soil legacies that negatively affected succeeding plants of the same functional type. We conclude that fungal‐mediated soil legacy effects play a significant role in vegetation assembly of natural plant communities.

Abiotic and biotic properties of soil can influence growth and chemical composition of plants. Although it is well-known that soil microbial composition can vary greatly spatially, how this variation affects plant chemical composition is poorly understood. We grew genetically identical Jacobaea vulgaris in sterilized soil inoculated with live soil collected from four natural grasslands and in 100% sterilized soil. Within each grassland we sampled eight plots, totalling 32 different inocula. Two samples per plot were collected, leading to three levels of spatial variation: within plot, between and within grasslands. The leaf metabolome was analysed with 1H Nuclear magnetic resonance spectroscopy (NMR) to investigate if inoculation altered the metabolome of plants and how this varied between and within grasslands. Inoculation led to changes in metabolomics profiles of J. vulgaris in two out of four sites. Plants grown in sterilized and inoculated soils differed in concentrations of malic acid, tyrosine, trehalose and two pyrrolizidine alkaloids (PA). Metabolomes of plants grown in inoculated soils from different sites varied in glucose, malic acid, trehalose, tyrosine and in one PA. The metabolome of plants grown in soils with inocula from the same site was more similar than with inocula from distant sites. We show that soil influences leaf metabolomes. Performance of aboveground insects often depends on chemical composition of plants. Hence our results imply that soil microbial communities, via affecting aboveground plant metabolomes, can impact aboveground plant-insect food chains but that it is difficult to make general predictions due to spatial variation in soil microbiomes.

Microorganisms are found everywhere and have critical roles in most ecosystems, but compared to plants and animals, little is known about their temporal dynamics. Here, we investigated the temporal stability of bacterial and fungal communities in the soil and how their temporal variation varies between grasses and forb species. We established 30 outdoor mesocosms consisting of six plant monocultures and followed microbial communities for an entire year in these soils. We demonstrate that bacterial communities vary greatly over time and that turnover plays an important role in shaping microbial communities. We further show that bacterial communities rapidly shift from one state to another and that this is related to changes in the relative contribution of certain taxa rather than to extinction. Fungal soil communities are more stable over time, and a large part of the variation can be explained by plant species and by whether they are grasses or forbs. Our findings show that the soil bacterial community is shaped by time, while plant group and plant species-specific effects drive soil fungal communities. This has important implications for plant-soil research and highlights that temporal dynamics of soil communities cannot be ignored in studies on plant-soil feedback and microbial community composition and function. IMPORTANCE Our findings highlight how soil fungal and bacterial communities respond to time, season, and plant species identity. We found that succession shapes the soil bacterial community, while plant species and the type of plant species that grows in the soil drive the assembly of soil fungal communities. Future research on the effects of plants on soil microbes should take into consideration the relative roles of both time and plant growth on creating soil legacies that impact future plants growing in the soil. Understanding the temporal (in)stability of microbial communities in soils will be crucial for predicting soil microbial composition