Root traits explain rhizosphere fungal community composition among temperate grassland plant species

Abstract

Summary While it is known that interactions between plants and soil fungi drive many essential ecosystem functions, considerable uncertainty exists over the drivers of fungal community composition in the rhizosphere. Here, we examined the roles of plant species identity, phylogeny and functional traits in shaping rhizosphere fungal communities and tested the robustness of these relationships to environmental change. We conducted a glasshouse experiment consisting of 21 temperate grassland species grown under three different environmental treatments and characterised the fungal communities within the rhizosphere of these plants. We found that plant species identity, plant phylogenetic relatedness and plant traits all affected rhizosphere fungal community composition. Trait relationships with fungal communities were primarily driven by interactions with arbuscular mycorrhizal fungi, and root traits were stronger predictors of fungal communities than leaf traits. These patterns were independent of the environmental treatments the plants were grown under. Our results showcase the key role of plant root traits, especially root diameter, root nitrogen and specific root length, in driving rhizosphere fungal community composition, demonstrating the potential for root traits to be used within predictive frameworks of plant–fungal relationships. Furthermore, we highlight how key limitations in our understanding of fungal function may obscure previously unmeasured plant–fungal interactions.

Interactions between below‐ground traits and rhizosheath fungal and bacterial communities for phosphorus acquisition

“…In our study, the differences in carboxylate exudations and relationships between plant traits and microbial indicators per soil type for plants with overall similar P content between soils seem to reinforce this suggestion. The degree to which this plasticity in carboxylate exudations is controlled by plants in order to interact with microbial communities, rather than a consequence of root plasticity induced by soil properties, however, remains unclear (Sweeney et al., 2021). The increased P availability in soil with high Ca‐P concentration can be explained by the weathering effect of carboxylate on minerals such as apatite as well as the mobilisation of Ca from the Ca‐P surface and the Ca chelation by carboxylates, which, in turn, promotes the dissolution of Ca‐P (Jones & Darrah, 1994; Rosling et al., 2007; Ryan et al., 2001).…”

“…Several microbial groups such as phosphate solubilising bacteria, AMF or plant growth promoting rhizobacteria (PGPR) can contribute to plant P uptake via the mobilisation of organic P and unavailable inorganic P present in soils and their effect on root growth (Menezes‐Blackburn et al., 2018; Richardson et al., 2011). Plant P acquisition traits could also play an important role in shaping these bacterial and fungal communities notably via the release of root exudates (Bardgett, 2017; Legay et al., 2014; Sweeney et al., 2021), jointly influencing plant P acquisition and thus P cycling in agroecosystems. Our understanding of the role of plant traits and notably root exudates in shaping rhizosheath microbial communities for plant P acquisition, however, remains limited (Datta et al., 2020; Hunter et al., 2014; Martin et al., 2016).…”

“…Some cover crops species such as White Lupine for example have, however, been observed to strongly and consistently influence microbial communities and lead to lasting effects on P availability (Hallama et al., 2019; Marschner et al., 2002), prompting more studies on the role of plant–microbe interactions in increasing P availability in agroecosystems via cover cropping. Plant functional traits such as root exudates are likely key driver of these plant–microbe interactions, while phylogenetic patterns and effects of species identity also contribute (Barberán et al., 2015; Sweeney et al., 2021). A large diversity of plant exudates such as amino acids, organic acids, sugars, phenolic compounds and many secondary metabolites indeed play a role in shaping and communicating with soil microbial community composition and abundance (Datta et al., 2020; Eisenhauer et al., 2017; Harrison & Bardgett, 2010; Marschner et al., 2002; Micallef et al., 2009; Sasse et al., 2018), and, therefore, could influence P dynamics and availability in agroecosystems.…”

Root functional traits explain root exudation rate and composition across a range of grassland species

“…We chose 17 common perennial European grassland species that co-occur in the area where the soil was collected (Sweeney et al 2020). These represent the functional groups of grasses, forbs and legumes (Table 1), and were grown in two separate experiments: one containing 13 (total number of individuals n = 140) and one containing four species (n = 20).…”

“…diameter displays large degree of influence over other root traits (Ma et al, 2018) and, along with cortex fraction size, is an important driver of 'outsourcing' nutrient acquisition to rhizosphere microbes (Bergmann et al, 2020). Importantly, high root diameter determines the strength of relationship between plants and rhizosphere fungi (Sweeney et al, 2020), including greater association with beneficials and a reduction in pathogens. High specific exudation rate, despite being metabolically costly and hence more associated with exploitative growth, might serve a vital function in providing nutrition to symbionts and potential biocidal exudates to aggressors.…”