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

Abstract

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.

Soil moisture and competition determine soil biota effects on invasive Centaurea stoebe

“…Soil biota also reduced C. stoebe leaf mass area (LMA), while soil biota effects on root to shoot ratios depended on soil moisture and presence of a competitor. Similar changes in LMA have been observed previously (Hahn et al, 2018) and could be caused by AM fungi, because LMA decreases when carbon availability is lowered (Poorter et al, 2009) and AM fungal colonization induces a substantial carbon-sink (Drigo et al, 2010). Soil biota significantly reduced root to shoot ratios of C. stoebe which fits with early observations of AM fungi reducing root to shoot ratios in C. stoebe (Marler, Zabinski, Wojtowicz, et al, 1999), possibly because AM fungi substitute for some root functions.…”

“…Further, we also chose to pool our soil inoculum from gradient end points to ensure compatible mutualists and pathogens were present. This precluded assessments of potential soil biota adaptations to soil moisture environments, which has been shown in some studies (Remke et al, 2021) but not others (Hahn et al, 2018). Finally, our study relied on shifts in relative sequence abundance, which may or may not reflect actual function.…”

Conditionality of Soil Microbial Mediation of Plant Phenotype

“…Despite the breadth of research on plant-soil biota relationships, the role of soil microbial communities on plant phenotype is heavily limited by the scarcity of knowledge of these relationships on traits such as physiology and reproduction. Of over 70 recent studies that have examined plant phenotype in response to unmanipulated and sterilized soil microbial treatments, only four studies have examined traits related to physiology (Hahn et al, 2018;Mursinoff & Tack, 2017;Siefert et al, 2018;Xi et al, 2018) and two have examined reproductive traits (Bauer & Flory, 2011;Dudenhöffer et al, 2018). In this study we found that neither SLA nor timing of ower bud formation responded to soil microbiome origin treatments, indicating that not all plant phenotypes are in part mediated by soil microbes.…”

Coming to Common Ground: The Challenges of Applying Ecological Theory Developed Aboveground to Rhizosphere Interactions

“…The largescale chemical analysis of the rhizomicrobiome, combined metagenomics, metatranscriptomics, metaproteomics and imaging mass spectrometry approaches (MSI) will help to understand the mechanisms involved in the communication between different members of the soil community (Oburger and Schmidt, 2016). Similarly, molecular databases such as Funguild and PICRUSt offer a promising framework to link taxa to function using 16S rRNA gene sequences (Langille et al, 2013;Tedersoo et al, 2014;Hahn et al, 2018). Given the spatial resolution required to investigate rhizosphere interactions (from cm to sub µm), the unpredictability of field conditions, and the instrumental limitations (e.g., immobility) most studies seek to simulate field conditions in semi-artificial experimental conditions (Oburger and Schmidt, 2016).…”