Crop Productivity Boosters: Native Mycorrhizal Fungi from an Old-Growth Grassland Benefits Tomato (Solanum lycopersicum) and Pepper (Capsicum annuum) Varieties in Organically Farmed Soils.

This paper investigates the response of five tomato and five pepper varieties to native arbuscular mycorrhizal (AM) fungal inoculation in an organic farming system. The field experiment was conducted across a growing season at a working organic farm in Lawrence, KS, USA. The researchers hypothesized that native AM fungi inoculation would improve crop biomass production for both crop species, but that the magnitude of response would depend on crop cultivar. The results showed that both crops were significantly positively affected by inoculation. AM fungal inoculation consistently improved total pepper biomass throughout the experiment (range of +2% to +8% depending on the harvest date), with a +3.7% improvement at the final harvest for inoculated plants. An interaction between pepper variety and inoculation treatment was sometimes observed, indicating that some pepper varieties were more responsive to AM fungi than others. Beginning at the first harvest, tomatoes showed a consistent positive response to AM fungal inoculation among varieties. Across the experiment, AM fungi-inoculated tomatoes had +10% greater fruit biomass, which was driven by a +20% increase in fruit number. The study highlights the potential benefits of using native AM fungi as a soil amendment in organic farmed soils to improve pepper and tomato productivity.

Native Microbes Amplify Native Seedling Establishment and Diversity While Inhibiting a Non-Native Grass.

Although several studies have shown increased native plant establishment with native microbe soil amendments, few studies have investigated how microbes can alter seedling recruitment and establishment in the presence of a non-native competitor. In this study, the effect of microbial communities on seedling biomass and diversity was assessed by seeding pots with both native prairie seeds and a non-native grass that commonly invades US grassland restorations, Setaria faberi. Soil in the pots was inoculated with whole soil collections from ex-arable land, late successional arbuscular mycorrhizal (AM) fungi isolated from a nearby tallgrass prairie, with both prairie AM fungi and ex-arable whole soil, or with a sterile soil (control). We hypothesized (1) late successional plants would benefit from native AM fungi, (2) that non-native plants would outcompete native plants in ex-arable soils, and (3) early successional plants would be unresponsive to microbes. Overall, native plant abundance, late successional plant abundance, and total diversity were greatest in the native AM fungi+ ex-arable soil treatment. These increases led to decreased abundance of the non-native grass S. faberi. These results highlight the importance of late successional native microbes on native seed establishment and demonstrate that microbes can be harnessed to improve both plant community diversity and resistance to invasion during the nascent stages of restoration.

Arbuscular Mycorrhizal Fungi Taxa Show Variable Patterns of Micro-Scale Dispersal in Prairie Restorations.

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.

Microbial mediators of plant community response to long-term N and P fertilization: Evidence of a role of plant responsiveness to mycorrhizal fungi.

Climate changes and anthropogenic nutrient enrichment widely threaten plant diversity and ecosystem functions. Understanding the mechanisms governing plant species turnover across nutrient gradients is crucial to developing successful management and restoration strategies. We tested whether and how soil microbes, particularly arbuscular mycorrhizal fungi (AMF), could mediate plant community response to a 15 years long-term N (0, 4, 8, and 16 g N m-2  year-1 ) and P (0 and 8 g N m-2  year-1 ) enrichment in a grassland system. We found N and P enrichment resulted in plant community diversity decrease and composition change, in which perennial C4  graminoids were dramatically reduced while annuals and perennial forbs increased. Metabarcoding analysis of soil fungal community showed that N and P changed fungal diversity and composition, of which only a cluster of AMF identified by the co-occurrence networks analysis was highly sensitive to P treatments and was negatively correlated with shifts in percentage cover of perennial C4  graminoids. Moreover, by estimating the mycorrhizal responsiveness (MR) of 41 plant species in the field experiment from 264 independent tests, we found that the community weighted mean MR of the plant community was substantially reduced with nutrient enrichment and was positively correlated with C4  graminoids percentage cover. Both analyses of covariance and structural equation modeling indicated that the shift in MR rather than AMF composition change was the primary predictor of the decline in perennial C4  graminoids, suggesting that the energy cost invested by C4 plants on those sensitive AMF might drive the inferior competitive abilities compared with other groups. Our results suggest that shifts in the competitive ability of mycorrhizal responsive plants can drive plant community change to anthropogenic eutrophication, suggesting a functional benefit of mycorrhizal mutualism in ecological restoration following climatic or anthropogenic degradation of soil communities.

Abiotic and biotic context dependency of perennial crop yield.

Perennial crops in agricultural systems can increase sustainability and the magnitude of ecosystem services, but yield may depend upon biotic context, including soil mutualists, pathogens and cropping diversity. These biotic factors themselves may interact with abiotic factors such as drought. We tested whether perennial crop yield depended on soil microbes, water availability and crop diversity by testing monocultures and mixtures of three perennial crop species: a novel perennial grain (intermediate wheatgrass-Thinopyrum intermedium-- that produces the perennial grain Kernza®), a potential perennial oilseed crop (Silphium intregrifolium), and alfalfa (Medicago sativa). Perennial crop performance depended upon both water regime and the presence of living soil, most likely the arbuscular mycorrhizal (AM) fungi in the whole soil inoculum from a long term perennial monoculture and from an undisturbed native remnant prairie. Specifically, both Silphium and alfalfa strongly benefited from AM fungi. The presence of native prairie AM fungi had a greater benefit to Silphium in dry pots and alfalfa in wet pots than AM fungi present in the perennial monoculture soil. Kernza did not benefit from AM fungi. Crop mixtures that included Kernza overyielded, but overyielding depended upon inoculation. Specifically, mixtures with Kernza overyielded most strongly in sterile soil as Kernza compensated for poor growth of Silphium and alfalfa. This study identifies the importance of soil biota and the context dependence of benefits of native microbes and the overyielding of mixtures in perennial crops.

Local adaptation of mycorrhizae communities changes plant community composition and increases aboveground productivity.

Soil microbial communities can have an important role in the adaptation of plants to their local abiotic soil conditions and in mediating plant responses to environmental stress. This has been clearly demonstrated for individual plant species, but it is unknown how locally adapted microbes may affect plant communities. It is possible that the adaptation of microbial communities to local conditions can shape plant community composition. Additionally, it is possible that the effects of locally adapted microorganisms on individual plant species could be altered by co-occurring plant species. We tested these possibilities in plant community mesocosms with soils and mycorrhizal fungi (AMF) from three locations. We found that plant community biomass responded positively to local adaptation of AMF to soil conditions. Plant community composition also changed in response to local adaptation of AMF. Unexpectedly, the strongest benefits of locally adapted AMF went to early successional plant species that have the highest relative growth rates and the lowest responsiveness to the presence of AMF. Late successional plants that responded positively overall to the presence of AMF were often suppressed in communities with local AMF, perhaps because of strong competition from fast growing plant species. These results show that local adaptation of soil microbial communities can shape plant community composition, and the benefits that plants derive from locally adapted microorganisms can be reshaped by the competitive context in which these associations occur.

Sensitivity to AMF species is greater in late-successional than early-successional native or nonnative grassland plants.

Sensitivity of plant species to individual arbuscular mycorrhizal (AM) fungal species is of primary importance to understanding the role of AM fungal diversity and composition in plant ecology. Currently, we do not have a predictive framework for understanding which plant species are sensitive to different AM fungal species. In two greenhouse studies, we tested for differences in plant sensitivity to different AM fungal species and mycorrhizal responsiveness across 17 grassland plant species of North America that varied in successional stage, native status, and plant family by growing plants with different AM fungal treatments including eight single AM fungal isolates, diverse mixtures of AM fungi, and non-inoculated controls. We found that late successional grassland plant species were highly responsive to AM fungi and exhibited stronger sensitivity in their response to individual AM fungal taxa compared to nonnative or early successional native grassland plant species. We confirmed these results using a meta-analysis that included 13 experiments, 37 plant species, and 40 fungal isolates (from nine publications and two greenhouse experiments presented herein). Mycorrhizal responsiveness and sensitivity of response (i.e., variation in plant biomass response to different AM fungal taxa) did not differ by the source of fungal inocula (i.e., local or not local) or plant family. Sensitivity of plant response to AM fungal species was consistently correlated with the average mycorrhizal response of that plant species. This study identifies that AM fungal identity is more important to the growth of late successional plant species than early successional or nonnative plant species, thereby predicting that AM fungal composition will be more important to plant community dynamics in late successional communities than in early successional or invaded plant communities.

Ecology of Floristic Quality Assessment: testing for correlations between coefficients of conservatism, species traits and mycorrhizal responsiveness.

Many plant species are limited to habitats relatively unaffected by anthropogenic disturbance, so protecting these undisturbed habitats is essential for plant conservation. Coefficients of conservatism (C values) were developed as indicators of a species' sensitivity to anthropogenic disturbance, and these values are used in Floristic Quality Assessment as a means of assessing natural areas and ecological restoration. However, assigning of these values is subjective and improved quantitative validation of C values is needed. We tested whether there are consistent differences in life histories between species with high and low C values. To do this, we grew 54 species of tallgrass prairie plants in a greenhouse and measured traits that are associated with trade-offs on the fast-slow continuum of life-history strategies. We also grew plants with and without mycorrhizal fungi as a test of these species' reliance on this mutualism. We compared these traits and mycorrhizal responsiveness to C values. We found that six of the nine traits we measured were correlated with C values, and together, traits predicted up to 50 % of the variation in C values. Traits including fast growth rates and greater investment in reproduction were associated with lower C values, and slow growth rates, long-lived leaves and high root:shoot ratios were associated with higher C values. Additionally, plants with high C values and a slow life history were more responsive to mutualisms with mycorrhizal fungi. Overall, our results connect C values with life-history trade-offs, indicating that high C value species tend to share a suite of traits associated with a slow life history.

Mycorrhizal response trades off with plant growth rate and increases with plant successional status.

Early-successional plant species invest in rapid growth and reproduction in contrast to slow growing late-successional species. We test the consistency of "trade-offs between plant life history and responsiveness on arbuscular mycorrhizal fungi. We selected four very early-, seven early-, 11 middle-, and eight late-successional plant species from six different families and functional groups and grew them with and without a mixed fungal inoculum and compared root architecture, mycorrhizal responsiveness, and plant growth rate. Our results indicate mycorrhizal responsiveness increases with plant successional stage and that this effect explains more variation in mycorrhizal response than is explained by phylogenetic relatedness. The mycorrhizal responsiveness of individual plant species was positively correlated with mycorrhizal root infection and negatively correlated with average plant mass and the number of root tips per unit mass, indicating that both plant growth rate and root architecture trade off with investment in mycorrhizal mutualisms. Because late-successional plants are very responsive to mycorrhizal fungi, our results suggest that fungal community dynamics may be an important driver of plant succession.

Reduced drought tolerance during domestication and the evolution of weediness results from tolerance-growth trade-offs.

The increased reproductive potential, size, shoot allocation, and growth rate of weedy plants may result from reduced resource allocation to other aspects of plant growth and defense. To investigate whether changes in resource allocation occurred during domestication or the evolution of weediness, we compared the mycorrhizal responsiveness, growth, and drought tolerance of nine native ruderal, nine agriculturally weedy (four U.S. weedy and five Australian weedy), and 14 domesticated populations (eight ancient landraces and six improved cultivars) of the common sunflower (Helianthus annuus). Domesticated sunflower cultivars were less drought tolerant, but had higher plant growth and fecundity and coarser roots than wild populations. There were no changes in level of drought tolerance between improved cultivars and ancient landrace plants, but there was an increase in allocation to flowers with recent selection. Weedy populations were intermediate between domesticated cultivars and native ruderal populations for plant growth rate, root architecture, and drought tolerance. Weedy populations benefited most from mycorrhizal inoculation by having fewer wilted leaves and wetter soil. Overall, we found that trade-offs between drought tolerance and several aspects of plant growth, including growth rate, allocation to flowering, and root architecture, govern evolution during sunflower domestication and the invasion of disturbed habitat.