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IntroductionClimate change and plant biodiversity loss have large impacts on terrestrial ecosystem function, with the soil microbiome being primary mediators of these effects. The soil microbiome is a complex system, consisting of multiple functional groups with contrasting life histories. Most studies of climate forces and plant biodiversity effects on microbiome consider the perturbations and the microbial functional groups in isolation preventing us from understanding the full picture of the relative and differential impacts of perturbations on microbial functional groups. MethodsWe measured changes in multiple microbial communities with different functionality, including plant mutualists and pathogens, after three growing seasons in a full-factorial experiment manipulating precipitation (50%, 150% of ambient), plant diversity, and plant composition. Using amplicon sequencing to characterize the response of fungi, arbuscular mycorrhizal fungi, bacteria and oomycetes, and we found that composition of all microbial groups differentiated strongly between precipitation treatments. ResultsOomycete and bacterial diversity increased with 150% precipitation, while AM and saprotroph fungal diversity decreased. Microbial differentiation in response to plant family and plant species composition was stronger after the third growing season than observed after year one. However, microbial response to plant species richness was weaker in year three. Microbiome response to plant composition was largely independent of the response to precipitation, except for oomycetes, which had greater response to plant composition in high precipitation. DiscussionThese findings build upon prior findings that these microbial community members differentially respond to plant community compositional treatments, by measuring the response over 3 years and with the addition of precipitation treatments. We find that both changes in climate and plant composition can drive major differences in soil microbiome composition, which can feed back on plant community structure and alter ecosystem function. 

Societal Impact StatementAgricultural practices have had a negative impact on the physical, chemical, and biological components of soil. Perennial cropping systems that facilitate positive soil microbial interactions could not only rebuild soils but also sustain productivity through expected variations in environmental conditions. Here, we show the presence of arbuscular mycorrhizal (AM) fungi, soil symbionts that can improve host performance and soil health, increased the growth of intermediate wheatgrass, a novel perennial grain crop, in populations that have been increasingly bred for desirable agricultural characteristics. The right pairing of intermediate wheatgrass and a beneficial AM fungal community could lead to more sustainable agroecosystems. SummaryIntermediate wheatgrass (IWG) is a novel perennial grain that can provide many soil health benefits in agroecosystems; however, little is known about how selection for agronomic traits has impacted interactions with soil biota. Here, we assess how the selection for agronomic traits in IWG has impacted its relationship with arbuscular mycorrhizal (AM) fungi.First, growth response to AM fungi was compared across five generations of IWG with varying degrees of selection. Second, variation in AM fungal responsiveness was compared among genets of IWG individuals within a more advanced generation. Finally, a meta‐analysis was performed on all published studies exploring AM fungal inocula effects on IWG performance to increase understanding of selection effects.AM fungal responsiveness increased with selection for agronomic traits, responsiveness varied among genets in the advanced generation, and a majority of genets performed better in the presence of AM fungi. The meta‐analysis supported the findings that AM fungal responsiveness has increased with selection in IWG.Further studies are needed to realize the combined potential soil health and sustainability benefits of IWG and AM fungi, including assessment of symbiotic benefits beyond biomass production, identification of IWG traits correlated with responsiveness, and characterization of AM fungal community response to IWG. 

Societal Impact StatementCrop genetic resources, particularly seeds held in ex situ germplasm collections, have enormous value in breeding climate‐resilient crops. Much of this value accrues from information associated with germplasm accessions. Here, we argue that flavor, culinary attributes, and other traditional ecological knowledge (TEK) are important characteristics alongside genomic information and high‐throughput phenotypes. We explore both the value of this information and the potential risks of exploitation of sensitive TEK. We also examine the potential of in situ conservation to preserve not just the genetic diversity of crops, but the TEK associated with them. SummaryCrop genetic diversity is essential for meeting the challenges posed to agriculture by a rapidly changing climate. Harnessing that diversity requires well‐organized information, often held by ex situ genebanks and associated databases. However, the characterization of crop germplasm often lacks information on its cultural and culinary background, specifically its flavor or taste. For most crops, characterization data is lacking, but when it is present it is more likely to include whole genome information, high‐throughput estimation of growth characteristics, and chemical profiles indicating flavor rather than details on the dishes for which particular varieties are favored or how smallholder farms have grown particular accessions. This loss of cultural and culinary information, and the broader loss of traditional ecological knowledge (TEK), is more than just missing information. It is a loss of legacy when landraces are no longer grown by the communities that developed them. In the face of climate change, TEK has great value for developing more sustainable or resilient practices. And with increasingly global palettes, we must balance consumers enjoying dishes from new crops with the appropriation of culturally meaningful foods. Our aim here is to explore this flavor gap, to understand the risks in sharing data and the benefits of honoring long‐established uses. We emphasize the importance of ensuring the fair representation of diverse peoples in genebanks and consider both ex situ and in situ conservation approaches. Finally, we analyze the impact of modern breeding choices on culinary diversity, emphasizing the preservation of ancestral knowledge and flavor profiles. 

ABSTRACT Fire is a common ecological disturbance that structures terrestrial ecosystems and biological communities. The ability of fires to contribute to ecosystem heterogeneity has been termed pyrodiversity and has been directly linked to biodiversity (i.e., the pyrodiversity–biodiversity hypothesis). Since climate change models predict increases in fire frequency, understanding how fire pyrodiversity influences soil microbes is important for predicting how ecosystems will respond to fire regime changes. Here we tested how fire frequency‐driven changes in burn patterns (i.e., pyrodiversity) influenced soil microbial communities and diversity. We assessed pyrodiversity effects on soil microbes by manipulating fire frequency (annual vs. biennial fires) in a tallgrass prairie restoration and evaluating how changes in burn patterns influenced microbial communities (bacteria and fungi). Annual burns produced more heterogeneous burn patterns (higher pyrodiversity) that were linked to shifts in fungal and bacterial community composition. While fire frequency did not influence microbial (bacteria and fungi) alpha diversity, beta diversity did increase with pyrodiversity. Changes in fungal community composition were not linked to burn patterns, suggesting that pyrodiversity effects on other ecosystem components (e.g., plants and soil characteristics) influenced fungal community dynamics and the greater beta diversity observed in the annually burned plots. Shifts in bacterial community composition were linked to variation in higher severity burn pattern components (grey and white ash), suggesting that thermotolerance contributed to the observed changes in bacterial community composition and lower beta diversity in the biennially burned plots. This demonstrates that fire frequency‐driven increases in pyrodiversity augment biodiversity and may influence productivity in fire‐prone ecosystems. 

Abstract Restoration of soil microbial communities, and microbial mutualists in particular, is increasingly recognized as critical for the successful restoration of grassland plant communities. Although the positive effects of restoring arbuscular mycorrhizal fungi during the restoration of these systems have been well documented, less is known about the potential importance of nitrogen‐fixing rhizobium bacteria, which associate with legume plant species that comprise an essential part of grassland plant communities, to restoration outcomes. In a series of greenhouse and field experiments, we examined the effects of disturbance on rhizobium communities, how plant interactions with these mutualists changed with disturbance, and whether rhizobia can be used to enhance the establishment of desirable native legume species in degraded grasslands. We found that agricultural disturbance alters rhizobium communities in ways that affect the growth and survival of legume species. Native legume species derived more benefit from interacting with rhizobia than did non‐native species, regardless of rhizobia disturbance history. Additionally, slow‐growing, long‐lived legume species received more benefits from associating with rhizobia from undisturbed native grasslands than from associating with rhizobia from more disturbed sites. Together, this suggests that native rhizobia may be key to enhancing the restoration success of legumes in disturbed habitats. 

Abstract To improve cover crops such as peas (Pisum sativum), as rotational partners, intraspecific variation for cover cropping traits such as nutrient mobilization, carbon deposition, and beneficial microbial recruitment must be identified. The majority of research on cover crops has focused on interspecies comparisons for cover cropping variation with minimal research investigating intraspecies variation. To address if variation of cover cropping traits is present within a cover cropping species, we grew 15 diverse accessions (four modern cultivars, three landraces, and eight wild accessions) of pea in a certified organic setting. We measured various cover cropping traits, such as nutrient mobilization, soil organic matter deposition, and microbial recruitment, and quantified the effect of pea accession on the growth and yield of a subsequently planted crop of corn (Zea mays). We discovered that the domestication history of pea has a significant impact on soil properties. Specifically, domesticated peas (modern cultivars and landraces) had higher average plant–soil feedback values for amounts of nitrogen, carbon, and manganese compared to wild peas. Additionally, no variation for prokaryotic recruitment (α‐ and β‐diversity) was observed within pea; however, we did observe significant variation for fungal recruitment (α‐ and β‐diversity) due to domestication and accession. Our results demonstrate that there is variation present in peas, and likely all crops, that can be selected to improve them as rotational partners to ultimately boost crop yields in sustainable agroecosystems. 

Abstract Continuous land disturbance could negatively impact microbial community, but perennial crops can potentially reverse this negativity. The objective of this study was to evaluate the effects of Kernza (Thinopyrum intermedium) and alfalfa (Medicago sativaL.) on soil microbial structure and stress condition using the phospholipid fatty acid profiling. The study was conducted at the Ross Jones Research Farm, University of Missouri and consisted of four treatments: Kernza fertilized, Kernza unfertilized, Kernza and alfalfa intercrop, and alfalfa monocrop with four replications. Treatments were established in September 2021 on 18.3 m × 18.3 m plots. Soils from 0‐ to 5‐cm and 5‐ to 15‐cm depths were sampled in September 2021 (before treatments were placed) and 2022 and analyzed for microbial communities. All microbial communities increased after 1 year with the perennial crops. Since differences were not significant among treatments in 2022, this may lead to positive impacts of perennial crops on microbial communities, irrespective of the crop species and management. Moreover, community structure modifications were also observed with the perennial crops, irrespective of the species and management, as evidenced with changes in bacterial community indices in 2022. While fungi/bacteria ratio increased, Gram‐positive/Gram‐negative bacteria ratio decreased in 2022, suggesting a reduction in microbial stress, which can be attributed to ecological functions of the perennial crops. The study showed improvements in soil microbial biomass and modifications in microbial community structure after 1 year of Kernza and alfalfa. As the system matures, relative benefits of management (fertilization and intercropping) and plant species may be realized. 

Abstract Many of the disturbance‐sensitive, late successional plant species in grasslands respond to arbuscular mycorrhizal (AM) fungi more positively via growth and establishment than plants that readily establish in disturbed areas (i.e. early successional species). Inoculation with AM fungi can therefore aid the establishment of late successional species in disturbed areas. If the differential benefit of AM fungi to late versus early successional plants is context‐dependent, however, this advantage could be diminished in high phosphorus (P) post‐agricultural soils or in future climates with altered precipitation.In this greenhouse experiment, we tested if late successional plant species are less plastic in their reliance on AM fungi than early successional plants by growing 17 plant species of different successional status (9 early and 8 late successional) in full factorial combinations of inoculated or uninoculated with AM fungi, with ambient or high P levels, and with low or high levels of water.AM fungi positively affected the biomass of the 17 grassland plant species, but across all environments, late successional plant species generally responded more positively to AM fungi than early successional plants species.AM fungal growth promotion and change in below‐ground biomass allocation was generally diminished with P fertilizer across all plant species, and while there was significant variation among plant species in the sensitivity of AM fungal responsiveness to P fertilization, this differential sensitivity was not predicted by plant successional status.The role of AM fungi in plant growth promotion was not generally altered by variation in watering, however late successional plant species allocated a greater proportion of their biomass below‐ground in response to AM fungi in low versus high water conditions.Synthesis. Overall greater responsiveness to arbuscular mycorrhizal (AM) fungi by late successional species is consistent with an important role of AM fungi in plant succession, even while AM fungi are less impactful overall in high P soils. However, the increase in responsiveness of below‐ground allocation of late successional species to AM fungi in low water conditions suggests that successional dynamics may be more dependent on AM fungi in future climates that feature greater propensity for drought. 

Abstract Productivity benefits from diversity can arise when compatible pathogen hosts are buffered by unrelated neighbors, diluting pathogen impacts. However, the generality of pathogen dilution has been controversial and rarely tested within biodiversity manipulations. Here, we test whether soil pathogen dilution generates diversity- productivity relationships using a field biodiversity-manipulation experiment, greenhouse assays, and feedback modeling. We find that the accumulation of specialist pathogens in monocultures decreases host plant yields and that pathogen dilution predicts plant productivity gains derived from diversity. Pathogen specialization predicts the strength of the negative feedback between plant species in greenhouse assays. These feedbacks significantly predict the overyielding measured in the field the following year. This relationship strengthens when accounting for the expected dilution of pathogens in mixtures. Using a feedback model, we corroborate that pathogen dilution drives overyielding. Combined empirical and theoretical evidence indicate that specialist pathogen dilution generates overyielding and suggests that the risk of losing productivity benefits from diversity may be highest where environmental change decouples plant-microbe interactions. 

Abstract Symbiont diversity can have large effects on plant growth but the mechanisms generating this relationship remain opaque. We identify three potential mechanisms underlying symbiont diversity–plant productivity relationships: provisioning with complementary resources, differential impact of symbionts of varying quality and interference between symbionts. We connect these mechanisms to descriptive representations of plant responses to symbiont diversity, develop analytical tests differentiating these patterns and test them using meta‐analysis. We find generally positive symbiont diversity–plant productivity relationships, with relationship strength varying with symbiont type. Inoculation with symbionts from different guilds (e.g. mycorrhizal fungi and rhizobia) yields strongly positive relationships, consistent with complementary benefits from functionally distinct symbionts. In contrast, inoculation with symbionts from the same guild yields weak relationships, with co‐inoculation not consistently generating greater growth than the best individual symbiont, consistent with sampling effects. The statistical approaches we outline, along with our conceptual framework, can be used to further explore plant productivity and community responses to symbiont diversity, and we identify critical needs for additional research to explore context dependency in these relationships.