Effects of Short- and Long-Term Variation in Resource Conditions on Soil Fungal Communities and Plant Responses to Soil Biota

Soil biota can strongly influence plant performance with effects ranging from negative to positive. However, shifts in resource availability can influence plant responses, with soil pathogens having stronger negative effects in high-resource environments and soil mutualists, such as arbuscular mycorrhizal fungi (AMF), having stronger positive effects in low-resource environments. Yet the relative importance of long-term vs. short-term variation in resources on soil biota and plant responses is not well-known. To assess this, we grew the perennial herb Asclepias speciosa in a greenhouse experiment that crossed a watering treatment (wet vs. dry treatment) with a manipulation of soil biota (live vs. sterilized soil) collected from two geographic regions (Washington and Minnesota) that vary greatly in annual precipitation. Because soil biota can influence many plant functional traits, we measured biomass as well as resource acquisition (e.g., root:shoot, specific leaf area) and defense (e.g., trichome and latex production) traits. Due to their important role as mutualists and pathogens, we also characterized soil fungal communities in the field and greenhouse and used curated databases to assess fungal composition and potential function. We found that the experimental watering treatment had a greater effect than soil biota origin on plant responses; most plant traits were negatively affected by live soils under wet conditions, whereas responses were neutral or positive in live dry soil. These consistent differences in plant responses occurred despite clear differences in soil fungal community composition between inoculate origin and watering treatments, which indicates high functional redundancy among soil fungi. All plants grown in live soil were highly colonized by AMF and root colonization was higher in wet than dry soil; root colonization by other fungi was low in all treatments. The most parsimonious explanation for negative plant responses in wet soil is that AMF became parasitic under conditions that alleviated resource limitation. Thus, plant responses appeared driven by shifts within rather than between fungal guilds, which highlights the importance of coupling growth responses with characterizations of soil biota to fully understand underlying mechanisms. Collectively these results highlight how short-term changes in environmental conditions can mediate complex interactions between plants and soil biota.