Reviewing ecological implications of mycorrhizal fungal interactions in the Brassicaceae.

Mycorrhizal associations are plant-fungal mutualisms that are fairly ubiquitous and likely evolved multiple times in phylogenic history; however, some plant families have consistently been identified as non-mycorrhizal, including the Brassicaceae. In this paper, we reviewed the literature and DNA databases for potential mechanisms that preclude mycorrhizal symbioses in the Brassicaceae and for exceptions to the general observation of non-mycorrhizal status within this plant family. In instances of association between members of the Brassicaceae and arbuscular mycorrhizal fungi we posed hypotheses for why these interactions occur in the species and sites observed. Instances of inconsistent association with mycorrhizal fungi were attributed to inter- and intraspecific variations in plant biology, disagreements in vernacular, methodology contradicting historical mycorrhizal surveys, and association being a facultative, variable trait that is determined by species-site interactions. We propose further research on a) the extent of mycorrhizal association in the Brassicaceae, b) the molecular mechanisms dictating association, and c) whether Brassicaceae-mycorrhizal fungal interactions result in nutrient transfer, and their particular roles in the family's distribution across heterogeneous and harsh environments.

Specificity in plant-mycorrhizal fungal relationships: prevalence, parameterization, and prospects.

Species interactions exhibit varying degrees of specialization, ranging from generalist to specialist interactions. For many interactions (e.g., plant-microbiome) we lack standardized metrics of specialization, hindering our ability to apply comparative frameworks of specificity across niche axes and organismal groups. Here, we discuss the concept of plant host specificity of arbuscular mycorrhizal (AM) fungi and ectomycorrhizal (EM) fungi, including the predominant theories for their interactions: Passenger, Driver, and Habitat Hypotheses. We focus on five major areas of interest in advancing the field of plant-mycorrhizal fungal host specificity: phylogenetic specificity, host physiology specificity, functional specificity, habitat specificity, and mycorrhizal fungal-mediated plant rarity. Considering the need to elucidate foundational concepts of specificity in this globally important symbiosis, we propose standardized metrics and comparative studies to enhance our understanding. We also emphasize the importance of analyzing global mycorrhizal data holistically to draw meaningful conclusions and suggest a shift toward single-species analyses to unravel the complexities underlying these associations.

Symbiotic status alters fungal eco-evolutionary offspring trajectories.

Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.

Links Among Crop Diversification, Microbial Diversity, and Soil Organic Carbon: Mini Review and Case Studies.

Interactions between species above- and belowground are among the top factors that govern ecosystem functioning including soil organic carbon (SOC) storage. In agroecosystems, understanding how crop diversification affects soil biodiversity and SOC storage at the local scale remains a key challenge for addressing soil degradation and biodiversity loss that plague these systems. Yet, outcomes of crop diversification for soil microbial diversity and SOC storage, which are key indicators of soil health, are not always positive but rather they are highly idiosyncratic to agroecosystems. Using five case studies, we highlight the importance of selecting ideal crop functional types (as opposed to focusing on plant diversity) when considering diversification options for maximizing SOC accumulation. Some crop functional types and crop diversification approaches are better suited for enhancing SOC at particular sites, though SOC responses to crop diversification can vary annually and with duration of crop cover. We also highlight how SOC responses to crop diversification are more easily interpretable through changes in microbial community composition (as opposed to microbial diversity). We then develop suggestions for future crop diversification experiment standardization including (1) optimizing sampling effort and sequencing depth for soil microbial communities and (2) understanding the mechanisms guiding responses of SOC functional pools with varying stability to crop diversification. We expect that these suggestions will move knowledge forward about biodiversity and ecosystem functioning in agroecosystems, and ultimately be of use to producers for optimizing soil health in their croplands.

Coupling of plant and mycorrhizal fungal diversity: its occurrence, relevance, and possible implications under global change.

First principles predict that diversity at one trophic level often begets diversity at other levels, suggesting plant and mycorrhizal fungal diversity should be coupled. Local-scale studies have shown positive coupling between the two, but the association is less consistent when extended to larger spatial and temporal scales. These inconsistencies are likely due to divergent relationships of different mycorrhizal fungal guilds to plant diversity, scale dependency, and a lack of coordinated sampling efforts. Given that mycorrhizal fungi play a central role in plant productivity and nutrient cycling, as well as ecosystem responses to global change, an improved understanding of the coupling between plant and mycorrhizal fungal diversity across scales will reduce uncertainties in predicting the ecosystem consequences of species gains and losses.

Grass species identity shapes communities of root and leaf fungi more than elevation.

Fungal symbionts can buffer plants from environmental extremes and may affect host capacities to acclimate, adapt, or redistribute under environmental change; however, the distributions of fungal symbionts along abiotic gradients are poorly described. Fungal mutualists should be the most beneficial in abiotically stressful environments, and the structure of networks of plant-fungal interactions likely shift along gradients, even when fungal community composition does not track environmental stress. We sampled 634 unique combinations of fungal endophytes and mycorrhizal fungi, grass species identities, and sampling locations from 66 sites across six replicate altitudinal gradients in the western Colorado Rocky Mountains. The diversity and composition of leaf endophytic, root endophytic, and arbuscular mycorrhizal (AM) fungal guilds and the overall abundance of fungal functional groups (pathogens, saprotrophs, mutualists) tracked grass host identity more closely than elevation. Network structures of root endophytes become more nested and less specialized at higher elevations, but network structures of other fungal guilds did not vary with elevation. Overall, grass species identity had overriding influence on the diversity and composition of above- and belowground fungal endophytes and AM fungi, despite large environmental variation. Therefore, in our system climate change may rarely directly affect fungal symbionts. Instead, fungal symbiont distributions will most likely track the range dynamics of host grasses.

Understanding Organismal Capacity to Respond to Anthropogenic Change: Barriers and Solutions.

Global environmental changes induced by human activities are forcing organisms to respond at an unprecedented pace. At present we have only a limited understanding of why some species possess the capacity to respond to these changes while others do not. We introduce the concept of multidimensional phenospace as an organizing construct to understanding organismal evolutionary responses to environmental change. We then describe five barriers that currently challenge our ability to understand these responses: (1) Understanding the parameters of environmental change and their fitness effects, (2) Mapping and integrating phenotypic and genotypic variation, (3) Understanding whether changes in phenospace are heritable, (4) Predicting consistency of genotype to phenotype patterns across space and time, and (5) Determining which traits should be prioritized to understand organismal response to environmental change. For each we suggest one or more solutions that would help us surmount the barrier and improve our ability to predict, and eventually manipulate, organismal capacity to respond to anthropogenic change. Additionally, we provide examples of target species that could be useful to examine interactions between phenotypic plasticity and adaptive evolution in changing phenospace.

Soil organic carbon cycling in response to simulated soil moisture variation under field conditions.

The combination of extended dry periods and high intensity rainfall, common in the southeastern US, leads to greater variability in soil moisture and consequently increases uncertainty to microbial processes pertinent to soil carbon (C) mineralization. However, field-based findings on soil moisture sensitivity to soil C cycling are very limited. Therefore, a field experiment was conducted in 2018 and 2019 on a soybean (Glycine max L.) cropland in the southeastern US with three soil moisture treatments: drought (simulated using rainout-shelter from June to October in each year), rainfed (natural precipitation), and irrigated (irrigation and precipitation). Soil respiration was measured weekly from May to November in both years. Soil samples were collected multiple times each year from 0-5, 5-15, and 15-30 cm depths to determine microbial biomass C (MBC), extractable organic C (EOC), hydrolytic enzyme activities, and fungal abundance. The cumulative respiration under drought compared to other treatments was lower by 32% to 33% in 2018 and 38% to 45% in 2019. Increased MBC, EOC, and fungal abundance were observed under drought than other treatments. Specific enzyme activity indicated fewer metabolically active microbes under drought treatment compared to rainfed and irrigated treatments. Also, maintenance of enzyme pool was observed under drought condition. These results provide critical insights on microbial metabolism in response to soil moisture variation and how that influences different pools of soil C under field conditions.

Invasion-induced root-fungal disruptions alter plant water and nitrogen economies.

Despite widespread evidence that biological invasion influences both the biotic and abiotic soil environments, the extent to which these two pathways underpin the effects of invasion on plant traits and performance remains unknown. Leveraging a long-term (14-year) field experiment, we show that an allelochemical-producing invader affects plants through biotic mechanisms, altering the soil fungal community composition, with no apparent shifts in soil nutrient availability. Changes in belowground fungal communities resulted in high costs of nutrient uptake for native perennials and a shift in plant traits linked to their water and nutrient use efficiencies. Some plants in the invaded community compensate for the disruption of nutritional symbionts and reduced nutrient provisioning by sanctioning more nitrogen to photosynthesis and expending more water, which demonstrates a trade-off in trait investment. For the first time, we show that the disruption of belowground nutritional symbionts can drive plants towards alternative regions of their trait space in order to maintain water and nutrient economics.

Negative effects of an allelopathic invader on AM fungal plant species drive community-level responses.

The mechanisms causing invasive species impact are rarely empirically tested, limiting our ability to understand and predict subsequent changes in invaded plant communities. Invader disruption of native mutualistic interactions is a mechanism expected to have negative effects on native plant species. Specifically, disruption of native plant-fungal mutualisms may provide non-mycorrhizal plant invaders an advantage over mycorrhizal native plants. Invasive Alliaria petiolata (garlic mustard) produces secondary chemicals toxic to soil microorganisms including mycorrhizal fungi, and is known to induce physiological stress and reduce population growth rates of native forest understory plant species. Here, we report on a 11-yr manipulative field experiment in replicated forest plots testing if the effects of removal of garlic mustard on the plant community support the mutualism disruption hypothesis within the entire understory herbaceous community. We compare community responses for two functional groups: the mycorrhizal vs. the non-mycorrhizal plant communities. Our results show that garlic mustard weeding alters the community composition, decreases community evenness, and increases the abundance of understory herbs that associate with mycorrhizal fungi. Conversely, garlic mustard has no significant effects on the non-mycorrhizal plant community. Consistent with the mutualism disruption hypothesis, our results demonstrate that allelochemical producing invaders modify the plant community by disproportionately impacting mycorrhizal plant species. We also demonstrate the importance of incorporating causal mechanisms of biological invasion to elucidate patterns and predict community-level responses.

Codependency between plant and arbuscular mycorrhizal fungal communities: what is the evidence?

That arbuscular mycorrhizal (AM) fungi covary with plant communities is clear, and many papers report nonrandom associations between symbiotic partners. However, these studies do not test the causal relationship, or 'codependency', whereby the composition of one guild affects the composition of the other. Here we outline underlying requirements for codependency, compare important drivers for both plant and AM fungal communities, and assess how host preference - a pre-requisite for codependency - changes across spatiotemporal scales and taxonomic resolution for both plants and AM fungi. We find few examples in the literature designed to test for codependency and those that do have been conducted within plots or mesocosms. Also, while plants and AM fungi respond similarly to coarse environmental filters, most variation remains unexplained, with host identity explaining less than 30% of the variation in AM fungal communities. These results combined question the likelihood of predictable co-occurrence, and therefore evolution of codependency, between plant and AM fungal taxa across locations. We argue that codependency is most likely to occur in homogeneous environments where specific plant - AM fungal pairings have functional consequences for the symbiosis. We end by outlining critical aspects to consider moving forward.

Spatial and temporal turnover of soil microbial communities is not linked to function in a primary tropical forest.

The spatial and temporal linkages between turnover of soil microbial communities and their associated functions remain largely unexplored in terrestrial ecosystems. Yet defining these relationships and how they vary across ecosystems and microbial lineages is key to incorporating microbial communities into ecological forecasts and ecosystem models. To define linkages between turnover of soil bacterial and fungal communities and their function we sampled fungal and bacterial composition, abundance, and enzyme activities across a 3-ha area of wet tropical primary forest over 2 yr. We show that fungal and bacterial communities both exhibited temporal turnover, but turnover of both groups was much lower than in temperate ecosystems. Turnover over time was driven by gain and loss of microbial taxa and not changes in abundance of individual species present in multiple samples. Only fungi varied over space with idiosyncratic variation that did not increase linearly with distance among sampling locations. Only phosphorus-acquiring enzyme activities were linked to shifts in septate, decomposer fungal abundance; no enzymes were affected by composition or diversity of fungi or bacteria. Although temporal and spatial variation in composition was appreciable, because turnover of microbial communities did not alter the functional repertoire of decomposing enzymes, functional redundancy among taxa may be high in this ecosystem. Slow temporal turnover of tropical soil microbial communities and large functional redundancy suggests that shifts in abundance of particular functional groups may capture ecosystem function more accurately than composition in these heterogeneous ecosystems.

Fungal aerobiota are not affected by time nor environment over a 13-y time series at the Mauna Loa Observatory.

Fungi are ubiquitous and often abundant components of virtually all ecosystems on Earth, serving a diversity of functions. While there is clear evidence that fungal-mediated processes can influence environmental conditions, and in turn select for specific fungi, it is less clear how fungi respond to environmental fluxes over relatively long time frames. Here we set out to examine changes in airborne fungi collected over the course of 13 y, which is the longest sampling time to date. Air filter samples were collected from the Mauna Loa Observatory (MLO) on Hawaii Island, and analyzed using Illumina amplicon sequencing. As a study site, MLO is unique because of its geographic isolation and high elevation, making it an ideal place to capture global trends in climate and aerobiota. We found that the fungal aerobiota sampled at MLO had high species turnover, but compositional similarity did not decrease as a function of time between samples. We attribute these patterns to neutral processes such as idiosyncratic dispersal timing and trajectories. Furthermore, the composition of fungi at any given point was not significantly influenced by any local or global environmental variables we examined. This, and our additional finding of a core set of persistent fungi during our entire sampling period, indicates some degree of stability among fungi in the face of natural environmental fluctuations and human-associated global change. We conclude that the movement of fungi through the atmosphere is a relatively stochastic process.

Global imprint of mycorrhizal fungi on whole-plant nutrient economics.

Mycorrhizal fungi are critical members of the plant microbiome, forming a symbiosis with the roots of most plants on Earth. Most plant species partner with either arbuscular or ectomycorrhizal fungi, and these symbioses are thought to represent plant adaptations to fast and slow soil nutrient cycling rates. This generates a second hypothesis, that arbuscular and ectomycorrhizal plant species traits complement and reinforce these fungal strategies, resulting in nutrient acquisitive vs. conservative plant trait profiles. Here we analyzed 17,764 species level trait observations from 2,940 woody plant species to show that mycorrhizal plants differ systematically in nitrogen and phosphorus economic traits. Differences were clearest in temperate latitudes, where ectomycorrhizal plant species are more nitrogen use- and phosphorus use-conservative than arbuscular mycorrhizal species. This difference is reflected in both aboveground and belowground plant traits and is robust to controlling for evolutionary history, nitrogen fixation ability, deciduousness, latitude, and species climate niche. Furthermore, mycorrhizal effects are large and frequently similar to or greater in magnitude than the influence of plant nitrogen fixation ability or deciduous vs. evergreen leaf habit. Ectomycorrhizal plants are also more nitrogen conservative than arbuscular plants in boreal and tropical ecosystems, although differences in phosphorus use are less apparent outside temperate latitudes. Our findings bolster current theories of ecosystems rooted in mycorrhizal ecology and support the hypothesis that plant mycorrhizal association is linked to the evolution of plant nutrient economic strategies.

Altitudinal gradients fail to predict fungal symbiont responses to warming.

Climate change is shifting altitudinal species ranges, with potential to disrupt species interactions. Altitudinal gradient studies and warming experiments can both increase understanding of climate effects on species interactions, but few studies have used both together to improve predictions. We examined whether plant-fungal symbioses responded similarly to altitude and 23 yr of experimental warming. Root- and leaf-associated fungi, which can mediate plants' climate sensitivity, responded divergently to elevation vs. warming. Fungal colonization, diversity, and composition varied with altitude, but climate variables were generally weak predictors; other factors such as host plant identity, plant community composition, or edaphic variables likely drive fungal altitudinal distributions. Manipulated warming altered fungal colonization, but not composition or diversity. Leaf symbionts were more sensitive to climate and experimental warming than root symbionts. Altitudinal patterns and responses to warming differed among host plant species and fungal groups, indicating that predicting climate effects on symbioses will require tracking both host and symbiont identities. Combining experimental and observational methods can yield valuable insight into how climate change may alter plant-symbiont interactions, but our results indicate that altitude does not always serve as an adequate proxy for warming effects on fungal symbionts of plants.

Plant Identity Influences Foliar Fungal Symbionts More Than Elevation in the Colorado Rocky Mountains.

Despite colonizing nearly every plant on Earth, foliar fungal symbionts have received little attention in studies on the biogeography of host-associated microbes. Evidence from regional scale studies suggests that foliar fungal symbiont distributions are influenced both by plant hosts and environmental variation in climate and soil resources. However, previous surveys have focused on either one plant host across an environmental gradient or one gradient and multiple plant hosts, making it difficult to disentangle the influence of host identity from the influence of the environment on foliar endophyte communities. We used a culture-based approach to survey fungal symbiont composition in the leaves of nine C3 grass species along replicated elevation gradients in grasslands of the Colorado Rocky Mountains. In these ecosystems, the taxonomic richness and composition of foliar fungal symbionts were mostly structured by the taxonomic identity of the plant host rather than by variation in climate. Plant traits related to size (height and leaf length) were the best predictors of foliar fungal symbiont composition and diversity, and composition did not vary predictably with plant evolutionary history. The largest plants had the most diverse and distinctive fungal communities. These results suggest that across the ~ 300 m elevation range that we sampled, foliar fungal symbionts may indirectly experience climate change by tracking the shifting distributions of plant hosts rather than tracking climate directly.

Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence.

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant-soil feedback (PSF) on plant performance is poorly understood. Using a meta-analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter- vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide-treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter- to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low-resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.