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  1. Abstract

    Plants affect associated biotic and abiotic edaphic factors, with reciprocal feedbacks from soil characteristics affecting plants. These two‐way interactions between plants and soils are collectively known as plant–soil feedbacks (PSFs). The role of phylogenetic relatedness and evolutionary histories have recently emerged as a potential driver of PSFs, although the strength and direction of feedbacks among sympatric congeners are not well‐understood. We examined plant–soil feedback responses ofAsclepias syriaca, a common clonal milkweed species, with several sympatric congeners across a gradient of increasing phylogenetic distances (A. tuberosa,A. viridis,A. sullivantii, andA. verticillata, respectively). Plant–soil feedbacks were measured through productivity and colonization by arbuscular mycorrhizal (AM) fungi.Asclepias syriacaproduced less biomass in soils conditioned by the most phylogenetically distant species (A. verticillata), relative to conspecific‐conditioned soils. Similarly, arbuscular mycorrhizal (AM) fungal colonization ofA. syriacaroots was reduced when grown in soils conditioned byA. verticillata, compared with colonization in plants grown in soil conditioned by any of the other threeAsclepiasspecies, indicating mycorrhizal associations are a potential mechanism of observed positive PSFs. This display of differences between the most phylogenetically distant, but not close or intermediate, paring(s) suggests a potential phylogenetic threshold, although other exogenous factors cannot be ruled out. Overall, these results highlight the potential role of phylogenetic distance in influencing positive PSFs through mutualists. The role of phylogenetic relatedness and evolutionary histories have recently emerged as a potential driver of plant–soil feedbacks (PSFs), although the strength and direction of feedbacks among sympatric congeners are not well‐understood. Congeneric, sympatric milkweeds typically generated positive PSFs in terms of productivity and AM fungal colonization, suggesting the low likelihood of coexistence among tested pairs, with a strength of feedback increasing as the phylogenetic distance increases.

     
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  2. There has been a surge in industries built on the production of arbuscular mycorrhizal (AM) fungal-based inoculants in the past few decades. This is not surprising, given the positive effects of AM fungi on plant growth and nutritional status. However, there is growing concern regarding the quality and efficacy of commercial inoculants. To assess the potential benefits and negative consequences of commercial AM fungal inoculants in grasslands, we conducted a controlled growth chamber study assessing the productivity and AM fungal root colonization of nine grassland plant species grown in grassland soil with or without one of six commercial AM fungal products. Our research showed no evidence of benefit; commercial inoculants never increased native plant biomass, although several inoculants decreased the growth of native species and increased the growth of invasive plant species. In addition, two commercial products contained excessive levels of phosphorus or nitrogen and consistently reduced AM fungal root colonization, indicating an unintentional de-coupling of the symbiosis. As there is little knowledge of the ecological consequences of inoculation with commercial AM fungal products, it is critical for restoration practitioners, scientists, and native plant growers to assess the presence of local AM fungal communities before investing in unnecessary, or possibly detrimental, AM fungal products. 
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  3. Human land use disturbance is a major contributor to the loss of natural plant communities, and this is particularly true in areas used for agriculture, such as the Midwestern tallgrass prairies of the United States. Previous work has shown that arbuscular mycorrhizal fungi (AMF) additions can increase native plant survival and success in plant community restorations, but the dispersal of AMF in these systems is poorly understood. In this study, we examined the dispersal of AMF taxa inoculated into four tallgrass prairie restorations. At each site, we inoculated native plant species with greenhouse-cultured native AMF taxa or whole soil collected from a nearby unplowed prairie. We monitored AMF dispersal, AMF biomass, plant growth, and plant community composition, at different distances from inoculation. In two sites, we assessed the role of plant hosts in dispersal, by placing known AMF hosts in a “bridge” and “island” pattern on either side of the inoculation points. We found that AMF taxa differ in their dispersal ability, with some taxa spreading to 2-m in the first year and others remaining closer to the inoculation point. We also found evidence that AMF spread altered non-inoculated neighboring plant growth and community composition in certain sites. These results represent the most comprehensive attempt to date to evaluate AMF spread. 
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  4. Losses of grasslands have been largely attributed to widespread land‐use changes, such as conversion to row‐crop agriculture. The remaining tallgrass prairie faces further losses due to biological invasions by non‐native plant species, often with resultant ecosystem degradation. Of critical concern for conservation, restoration of native grasslands has been met with little success following eradication of non‐native plants. In addition to the direct and indirect effects of non‐native invasive plants on beneficial soil microbes, management practices targeting invasive species may also negatively affect subsequent restoration efforts. To assess mechanisms limiting germination and survival of native species and to improve native species establishment, we established six replicate plots of each of the following four treatments: (1) inoculated with freshly collected prairie soil with native seeds; (2) inoculated with steam‐pasteurized soil with native seeds; (3) noninoculated with native seeds; or (4) noninoculated/nonseeded control. Inoculation with whole soil did not improve seed germination; however, addition of whole soil significantly improved native species survival, compared to pasteurized soil or noninoculated treatments. Inoculation with whole soil significantly decreased reestablishment of non‐native invasiveBothriochloa bladhii(Caucasian bluestem); at the end of the growing season, plots receiving whole soil consisted of approximately 30%B. bladhiicover, compared to approximately 80% in plots receiving no soil inoculum. Our results suggest invasion and eradication efforts negatively affect arbuscular mycorrhizal hyphal and spore abundances and soil aggregate stability, and inoculation with locally adapted soil microbial communities can improve metrics of restoration success, including plant species richness and diversity, while decreasing reinvasion by non‐native species.

     
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  5. Abstract

    The plant microbiome is critical to plant health and is degraded with anthropogenic disturbance. However, the value of re‐establishing the native microbiome is rarely considered in ecological restoration. Arbuscular mycorrhizal (AM) fungi are particularly important microbiome components, as they associate with most plants, and later successional grassland plants are strongly responsive to native AM fungi.

    With five separate sites across the United States, we inoculated mid‐ and late successional plant seedlings with one of three types of native microbiome amendments: (a) whole rhizosphere soil collected from local old‐growth, undisturbed grassland communities in Illinois, Kansas or Oklahoma, (b) laboratory cultured AM fungi from these same old‐growth grassland sites or (c) no microbiome amendment. We also seeded each restoration with a diverse native seed mixture. Plant establishment and growth was followed for three growing seasons.

    The reintroduction of soil microbiome from native ecosystems improved restoration establishment.

    Including only native arbuscular mycorrhizal fungal communities produced similar improvements in plant establishment as what was found with whole soil microbiome amendment. These findings were robust across plant functional groups.

    Inoculated plants (amended with either AM fungi or whole soil) also grew more leaves and were generally taller during the three growing seasons.

    Synthesis and applications. Our research shows that mycorrhizal fungi can accelerate plant succession and that the reintroduction of both whole soil and laboratory cultivated native mycorrhizal fungi can be used as tools to improve native plant restoration following anthropogenic disturbance.

     
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  6. Societal Impact Statement Summary

    Plant–mycorrhizal interactions are not typically assessed in crop breeding programs. Our experiment addresses this by determining host‐plant outcomes of newly developed synthetic (agronomic) populations compared with parent lines, following low‐input selective breeding. Assessing the potential of low‐input breeding to enhance crop mycorrhizal benefits is a critical step toward more sustainable agricultural production.

    We compared four synthetic populations ofPanicum virgatum, from a low‐input biofuel breeding program at Oklahoma State University, to corresponding parent lines. Plants were grown in a greenhouse in native prairie soils that were either steam‐pasteurized (nonmycorrhizal) or non‐steamed (mycorrhizal).

    We assessed shoot and root biomass, shoot P concentration and P content, mycorrhizal growth response (MGR), and mycorrhizal phosphorous response (MPR). Importantly, we provide novel evidence that low‐input selective breeding increased mycorrhizal reliance of switchgrass synthetics compared to parent lines, with implications for global agricultural systems.

    There are substantial opportunities for plant traits associated with increased MGR and MPR to be transferred to a wide array of crops. Our findings indicate low‐input selective breeding can improve MGR and MPR. We propose these traits serve as a useful proxy for host‐plant mycorrhizal reliance, facilitating successful hologenome breeding to reduce fertilizer requirements.

     
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