Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome

Abstract

Plant genetic variation, through its phenotypic display, can determine the composition of below ground microbial communities. Variation within a species is increasingly acknowledged to have substantial ecological consequences, particularly through trophic cascades. We hypothesized that the intraspecific genotypic variation of the tree host might impact the phylogenetic composition of its rhizospheric microbial communities, by favouring particular clades, that might be further reflected in ecosystem process rates. We tested whether the intraspecific genotypic variation of Pinus pinaster modulates nutrient cycling by determining the phylogenetic structure of its symbiotic ectomycorrhizal fungi and rhizospheric bacteria. We sequenced fungal and bacterial molecular markers and reconstructed phylogenies in the rhizosphere of P. pinaster trees belonging to three genotypic variants (Mediterranean, Atlantic, African) in three 45‐year‐old common garden experiments, and measured seven soil enzymatic activities. Local effects, based on differences in elevation and soil conditions across sites, were strong predictors of the ectomycorrhizal and bacterial communities thriving in tree’s rhizosphere. Across‐site variation also explained differences in phosphorus cycling. We detected, however, a significant effect of the plant genotype on the phylogenetic structure of the root‐associated microbiota that was consistent across sites. The most productive Mediterranean plant genotype sheltered the most distinct root microbiome, with the dominant Basidiomycetes and Proteobacteria having a strong influence on the phylogenetic microbial community structure and associating with an enhanced hydrolysis of celluloses, hemicelluloses and chitin. Beneath the less productive Atlantic genotype, the less abundant Ascomycetes and up to thirteen bacterial phyla shaped the phylogenetic microbial structure, and predicted the rates of peptidase. Ectomycorrhizal fungi explained the activity of cellulases and protease, and bacteria that of hemicellulases and chitinase, suggesting functional complementarity. Synthesis. This is the first report using three‐replicated long‐term common gardens in mature forests to disentangle plant genotype‐ and site‐specific drivers of the rhizospheric microbiome and its enzymatic potential. We concluded that intraspecific variation in primary producers leaves a phylogenetic signature in mutualists and decomposers that further modulate key steps in carbon and nitrogen cycles. These results emphasize the ecological relevance of plant intraspecific diversity in determining essential plant–soil feedbacks that control ecosystem productivity and performance.

Geology and climate influence rhizobiome composition of the phenotypically diverse tropical tree Tabebuia heterophylla

“…Thus, the rhizosphere will be dominated by microbes with the metabolic capacity to degrade those compounds in addition to other structural compounds such as lignin, commonly found within the plant litter [46,47]. These degradation processes are essential for plant nutrient cycling, [48] biogeochemical cycles (e.g. nitrogen, phosphorus, calcium) and water uptake [49].…”

History sets the stage: Macroevolutionary influence on biotic interactions

“…3) How does evolutionary history influence community, ecosystem, and global ecological processes and patterns? Four contributions focus on plant–soil interactions, including the mycorrhiza (Jacquemyn & Merckx, ; Shefferson et al, ) and more general rhizosphere interactions (Perez‐Izquierdo et al ; Schroeder et al ). Another two focus on above‐ground herbivory (Coley et al ; Foisy et al ).…”

“…Three contributions address this theme. First, Pérez‐Izquierdo et al () ask whether genetic variation within a tree species influences the phylogenetic composition of soil microbial communities within the root zone. They used three long‐term common gardens using three genetic variants of the maritime pine, Pinus pinaster , and found impacts on microbial phylogenetic structure of plant genetic variation, as well as of elevation and soil conditions.…”

Ectomycorrhizal fungal diversity decreases in Mediterranean pine forests adapted to recurrent fires

“…More generally, fire drastically disrupts the species composition of the mycorrhizal communities, usually leading to their simplification with the dominance of pioneer fungi (Buscardo et al., 2015; Dove & Hart, 2017; Rincón et al., 2014; de Román & de Miguel, 2005; Torres & Honrubia, 1997). Additionally, because intraspecific plant genotypic and phenotypic variation affects the structure of their associated ECM fungi (Gehring & Whitham, 1991; van der Heijden et al., 2015; Pérez‐Izquierdo et al., 2017, 2019) it is plausible that genetically fire‐driven changes in trees, such as degree of serotiny, may co‐affect these mutualistic communities. Nevertheless, fires recurrently affect large areas of Mediterranean ecosystems, yet the cumulative effects of recurrent wildfires on ECM fungal communities are less well known than those of single wildfires (Buscardo et al., 2015).…”