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 invasive
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Bothriochloa bladhii (Caucasian bluestem); at the end of the growing season, plots receiving whole soil consisted of approximately 30%B. bladhii cover, 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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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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Societal Impact Statement Agriculture touches all aspects of society and global environmental health. Dwindling phosphorous reserves are a looming crisis for civilization, and soil erosion typically far outpaces pedogenesis. Improving plant–mycorrhizal symbioses can enhance sustainable agriculture because mycorrhizas typically improve host‐plant nutrition and stabilize soils. Selective breeding of plants that gain greater benefits from mycorrhizas can provide considerable economic and environmental benefits. Our assessments demonstrate switchgrass genetic improvement increased or maintained production of two populations, and low‐input breeding increased mycorrhizal responsiveness, compared to parent lines. Selecting for increased mycorrhizal reliance may be an effective strategy for more sustainable and economical agricultural production.
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 of
Panicum 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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Abstract Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.
