Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be "enslaved." Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.

https://science.sciencemag.org/content/sci/333/6044/880.full.pdf

Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis

Almost all land plants form symbiotic associations with mycorrhizal fungi. These below-ground fungi play a key role in terrestrial ecosystems as they regulate nutrient and carbon cycles, and influence soil structure and ecosystem multifunctionality. Up to 80% of plant N and P is provided by mycorrhizal fungi and many plant species depend on these symbionts for growth and survival. Estimates suggest that there are c. 50 000 fungal species that form mycorrhizal associations with c. 250 000 plant species. The development of high-throughput molecular tools has helped us to better understand the biology, evolution, and biodiversity of mycorrhizal associations. Nuclear genome assemblies and gene annotations of 33 mycorrhizal fungal species are now available providing fascinating opportunities to deepen our understanding of the mycorrhizal lifestyle, the metabolic capabilities of these plant symbionts, the molecular dialogue between symbionts, and evolutionary adaptations across a range of mycorrhizal associations. Large-scale molecular surveys have provided novel insights into the diversity, spatial and temporal dynamics of mycorrhizal fungal communities. At the ecological level, network theory makes it possible to analyze interactions between plant-fungal partners as complex underground multi-species networks. Our analysis suggests that nestedness, modularity and specificity of mycorrhizal networks vary and depend on mycorrhizal type. Mechanistic models explaining partner choice, resource exchange, and coevolution in mycorrhizal associations have been developed and are being tested. This review ends with major frontiers for further research.

https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.13288

Mycorrhizal ecology and evolution: the past, the present, and the future

Plant genomes contribute to the structure and function of the plant microbiome, a key determinant of plant health and productivity. High-throughput technologies are revealing interactions between these complex communities and their hosts in unprecedented detail.

The plant microbiome.

Despite the fact that arbuscular mycorrhizal (AM) associations are among the most ancient, abundant and important symbioses in terrestrial ecosystems, there are currently few unifying theories that can be used to help understand the factors that control their structure and function. This review explores how a stoichiometric perspective facilitates integration of three complementary ecological and evolutionary models of mycorrhizal structure and function. AM symbiotic function should be governed by the relative availability of carbon, nitrogen and phosphorus (trade balance model) and allocation to plant and fungal structures should depend on the availabilities of these resources (functional equilibrium model). Moreover, in an evolutionary framework, communities of plants and AM fungi are predicted to adapt to each other and their local soil environment (co-adaptation model). Anthropogenic enrichment of essential resources in the environment is known to impact AM symbioses. A more predictive theory of AM structure and function will help us to better understand how these impacts may influence plant communities and ecosystem properties.

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Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales

Microorganisms have critical roles in the functioning of soil in nutrient cycling, structural formation, and plant interactions, both positive and negative These roles are important in reestablishing function and biodiversity in ecosystem restoration Measurement of the community indicates the status of the system in relation to restoration targets and the effectiveness of management interventions, and manipulation of the community shows promise in the enhancement of the rate of recovery of degraded systems

http://science.sciencemag.org/content/sci/325/5940/573.full.pdf

Soil microbial communities and restoration ecology: facilitators or followers?

Mutualisms, beneficial interactions between species, are expected to be unstable because delivery of benefit likely involves fitness costs and selection should favour partners that deliver less benefit. Yet, mutualisms are common and persistent, even in the largely promiscuous associations between plants and soil microorganisms such as arbuscular mycorrhizal fungi. In two different systems, we demonstrate preferential allocation of photosynthate by host plants to the more beneficial of two AM fungal symbionts. This preferential allocation could allow the persistence of the mutualism if it confers sufficient advantage to the beneficial symbiont that it overcomes the cost of mutualism. We find that the beneficial fungus does increase in biomass when the fungi are spatially separated within the root system. However, in well-mixed fungal communities, non-beneficial fungi proliferate as expected from their reduced cost of mutualism. Our findings suggest that preferential allocation within spatially structured microbial communities can stabilize mutualisms between plants and root symbionts.

Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism.

The variability in the type of ecosystem degradation and the specificity of restoration goals can challenge restorationists’ ability to generalize about approaches that lead to restoration success. The discipline of soil ecology, which emphasizes both soil organisms and ecosystem processes, has generated a body of knowledge that can be generally useful in improving the outcomes of restoration despite this variability. Here, we propose that the usefulness of this soil ecological knowledge (SEK) for restoration is best considered in the context of the severity of the original perturbation, the goals of the project, and the resilience of the ecosystem to disturbance. A straightforward manipulation of single physical, chemical, or biological components of the soil system can be useful in the restoration of a site, especially when the restoration goal is loosely defined in terms of the species and processes that management seeks to achieve. These single-factor manipulations may in fact produce cascading effects on several ecosystem attributes and can result in unintended recovery trajectories. When complex outcomes are desired, intentional and holistic integration of all aspects of the soil knowledge is necessary. We provide a short roster of examples to illustrate that SEK benefits management and restoration of ecosystems and suggest areas for future research.

/pdf/integrating-soil-ecological-knowledge-into-restoration-3qjn077hpi.pdf

Integrating Soil Ecological Knowledge into Restoration Management

Soil microbial communities contribute to ecosystem function and structure plant communities, but are altered by anthropogenic disturbance. Successful restoration may require microbial community restoration. Inoculation of plants with arbuscular mycorrhizal fungi (AMF) may improve ecological restoration, but AMF species that are locally adapted to native plant communities are often unavailable and commercially propagated AMF are not necessarily locally adapted to the desired plant community target. The disconnect between readily available commercial fungi and later-successional plants may inhibit successful establishment of the restoration. We tested this concept using four mid- to late successional prairie plant species planted with one of three inoculum sources: a locally adapted AMF mix cultured from native prairie, a non-locally adapted commercial AMF product, or a sterilized background soil control. The inoculated plants (termed nurse plants) were planted in the middle of field plots. In each plot, un...

https://esajournals.onlinelibrary.wiley.com/doi/pdf/10.1890/ES15-00152.1

Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species

The persistence of mutualisms is paradoxical, as there are fitness incentives for exploitation. This is particularly true for plant-microbe mutualisms like arbuscular mycorrhizae (AM), which are promiscuously horizontally transmitted. Preferential allocation by hosts to the best mutualist can stabilize horizontal mutualisms; however, preferential allocation is imperfect, with its fidelity likely depending on the spatial structure of symbionts in plant roots. In this study we tested AM mutualisms’ dependence on two dimensions of spatial structure—the initial spatial association of fungi and the ease of fungal dispersal—through three complementary experiments. We found that fitness of the beneficial AM fungus increased when fungi were initially separate, while initial spatial mixing benefited the fitness of the nonbeneficial fungus. These effects were strongest when dispersal was limited and hosts could discriminate. Additionally, we found that changes in AM fungal proportional abundance induced by spatial structure in roots of a preferentially allocating host produced positive feedbacks on plant growth, showing that interactions between spatial structure and host choice can determine the direction of plant-soil feedbacks. Our results suggest that symbiont spatial structure within plant roots may act as an important modifier of plant preferential allocation and the dynamics of mycorrhizal mutualisms, with potentially cascading effects on plant-plant interactions.

Spatial Structure within Root Systems Moderates Stability of Arbuscular Mycorrhizal Mutualism and Plant-Soil Feedbacks

/pdf/knowing-when-native-regeneration-is-for-you-and-what-you-2ey9gf5p.pdf

Sarah Richardson

Papers

Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism.

Integrating Soil Ecological Knowledge into Restoration Management

Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species

Spatial Structure within Root Systems Moderates Stability of Arbuscular Mycorrhizal Mutualism and Plant-Soil Feedbacks

Knowing when native regeneration is for you, and what you should do about it. The Aotearoa New Zealand context