Andrew Eagar and Sara Moledor, from Michigan State University’s Department of Plant Biology, discuss their research group’s new review paper: Setting the Stage for Plant-Soil Feedback: Mycorrhizal Influences over Conspecific Recruitment, Plant and Fungal Communities, and Coevolution
A holistic view of plant-soil feedback
Research over the last 20 years on plant-soil interactions has greatly advanced our understanding of these fascinating, dynamic, complex, and naturally hard-to-observe processes. For example, how soil nutrients influence plant growth is usually fairly intuitive: nutrient limitation can slow growth while abundant nutrients can boost growth. However, the process known as plant-soil feedback describes a much more complicated picture: a plant changes its soil conditions in such a way that it alters the performance of its offspring and neighbors. In essence, that maple tree and its seedlings in your backyard may be benefitting from, or struggling against, soil conditions that still hold the legacy of the plants that preceded it!
These beneficial or antagonistic soil conditions that contribute to plant fitness, and ultimately affect plant community composition and ecosystem services, are the work of mostly invisible yet ubiquitous microbes. Over time, any given plant will naturally accumulate antagonistic pathogens adapted to its particular species. The result of this pathogen accumulation is that any offspring growing in the same vicinity as conspecific adults may be at a serious disadvantage, experiencing lower growth and fitness. Other nearby plant species to whom those pathogens are not adapted generally have the upper hand. For a while, that is, until those plants grow in dominance and accumulate their own host-specific pathogens over time, continuing the ebb and flow of the negative plant-soil feedback cycle across plant communities.
There can also be positive plant-soil feedback, but those outcomes are far less common. In those cases, as a plant grows over time, so does its community of microbial mutualists – to a greater extent than the microbial antagonists in the system. The mutualists promote plant growth, which expands the plant’s access to soil resources and can boost plant defense. Mycorrhizae are a prime example of these plant mutualisms. In this symbiotic relationship between plants and fungi, plant-derived sugars are exchanged for the soil nutrients harvested by their mycorrhizal symbionts. As mycorrhizal fungi or other beneficial mutualists grow and accumulate in response to their host plant’s growth, a soil environment that benefits the plant’s offspring and other conspecifics is created that can give them a competitive advantage over other neighboring species.
The recently recognized role of mycorrhizas in structuring plant-soil feedback
Because microbial pathogens and mutualists are both abundant members of soil communities, both negative and positive feedback occur simultaneously in plant-soil systems. So, what determines whether a plant will experience net positive or negative plant-soil feedback? In our review paper, we were especially interested in connecting these divergent feedback outcomes with the dominant mycorrhizal type of tree communities. Trees of a given species typically partner with one of two types of mycorrhizal fungi: arbuscular mycorrhizal (AM) or ectomycorrhizal (ECM) fungi. Both types of mycorrhizal symbiosis promote the growth of their individual host tree and are beneficial for offspring and other conspecific individuals nearby. However, they have very different physiologies that can create distinct soil conditions encountered by all the plants in the surrounding neighborhood.
Trees that associate with arbuscular mycorrhizal (AM) fungi are dependent on saprotrophic microbes for release of nutrients from dead plant material. In essence, AM systems “subcontract” third-party saprotrophic microbes to transform soil organic matter into usable, inorganic nutrients, which the AM fungi can then take up and deliver to their tree hosts. The downside to this arrangement is that some of these saprotrophic microbes may be double-agents capable of acting pathogenically, thereby contributing to negative feedback. AM trees also appear to have weaker pathogen defenses and tissues higher in nitrogen compared to their ECM counterparts, which makes them an attractive target for pathogens.
On the other hand, many ECM fungi can access organic nutrient pools in soil organic matter directly, without the need of saprotrophic microbes to release inorganic nutrients. As such, ECM trees have privileged access to these nutrient pools, and by removing these nutrients from the soil, hinder the growth of potentially antagonistic microbes. Pathogens are further held at bay by the particular morphology of ECM fungi, in which root tips are enveloped in a hyphal sheath, providing a physical barrier defense that AM trees lack. Additionally, many ECM fungi grow as extensive underground mycelial networks, meaning that seeds falling from ECM trees have an easier time “plugging into” these mutualisms as they germinate and take root without having to invest much carbon. These characteristics collectively confer benefits that favor the build-up of mutualists instead of pathogens in ECM systems, resulting in plant-soil feedback between ECM trees and soil that is positive.
Where we are and where we’re going
This paints a picture of localized plant-soil feedback dynamics, but we wanted to go further and investigate how these patterns apply at larger scales. Most plants don’t grow in isolation and are instead surrounded by a community of other plants, including both conspecific and heterospecific individuals. Recent work has made us appreciate the capacity of plant mutualists and pathogens to associate with multiple plant species. Thus, the buildup of mutualistic and pathogenic microorganisms over time resulting from the persistence of any one plant has the potential to affect the direction (positive vs negative) and strength of plant-soil feedback of other nearby plants, regardless of their species identity. By thinking from the perspective of seedlings and juveniles that are growing in close vicinity to dominant adult trees, we can begin to understand how the microbes responsible for positive or negative feedback can “spill over” from the adult onto less dominant individuals.
In other words, the detrimental consequences of decomposers and pathogens accumulating under an individual AM tree have the potential to spill over onto neighboring trees (regardless of their relationship to one another), whereas the benefits accrued with the buildup of mutualists and suppression of saprotrophs and pathogens under an ECM tree may spill over onto their neighbors. These effects are likely stronger for neighbors of the same mycorrhizal type due to spillover of shared mutualists, but even individuals of mismatched mycorrhizal types would be affected by the spillover of pathogenic microbes. This has important consequences for juvenile recruitment in forests, with AM tree communities being more over-dispersed compared to ECM tree communities.
Collectively, dominant trees likely have an outsized impact on the soil environment encountered by the surrounding plant community and ultimately impact forest composition in ways that are difficult to see without careful study. Under global change, forests are expected to become more AM dominant as AM trees encroach into ECM-dominant systems. Our work highlights how these changes will also bring further unforeseen changes in belowground microbial communities that have the potential to disrupt established plant-soil feedback regimes and exacerbate the effects of global change in forested ecosystems. We also think that such spillover effects apply different selective pressures within plant communities, which may alter evolutionary trajectories in forest communities and represent an important area of future research.
Our paper provides an expanded and more detailed examination of the nuts and bolts of these complex mechanisms and interactions. With over 190 citations and a full A-Z bibliography, our review ties together many concepts of plant and soil ecology for a clearer vision of, and greater appreciation for, the fascinating and complex interactions that unfold belowground.
