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.

Fungi provide relevant ecosystem services contributing to primary productivity and the cycling of nutrients in forests. These fungal inputs can be decisive for the resilience of Mediterranean forests under global change scenarios, making necessary an in-deep knowledge about how fungal communities operate in these ecosystems. By using high-throughput sequencing and enzymatic approaches, we studied the fungal communities associated with three genotypic variants of Pinus pinaster trees, in 45-year-old common garden plantations. We aimed to determine the impact of biotic (i.e., tree genotype) and abiotic (i.e., season, site) factors on the fungal community structure, and to explore whether structural shifts triggered functional responses affecting relevant ecosystem processes. Tree genotype and spatial-temporal factors were pivotal structuring fungal communities, mainly by influencing their assemblage and selecting certain fungi. Diversity variations of total fungal community and of that of specific fungal guilds, together with edaphic properties and tree's productivity, explained relevant ecosystem services such as processes involved in carbon turnover and phosphorous mobilization. A mechanistic model integrating relations of these variables and ecosystem functional outcomes is provided. Our results highlight the importance of structural shifts in fungal communities because they may have functional consequences for key ecosystem processes in Mediterranean forests.

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Fire is a major disturbance linked to the evolutionary history and climate of Mediterranean ecosystems, where the vegetation has evolved fire‐adaptive traits (e.g., serotiny in pines). In Mediterranean forests, mutualistic feedbacks between trees and ectomycorrhizal (ECM) fungi, essential for ecosystem dynamics, might be shaped by recurrent fires. We tested how the structure and function of ECM fungal communities of Pinus pinaster and Pinus halepensis vary among populations subjected to high and low fire recurrence in Mediterranean ecosystems, and analysed the relative contribution of environmental (climate, soil properties) and tree‐mediated (serotiny) factors. For both pines, local and regional ECM fungal diversity were lower in areas of high than low fire recurrence, although certain fungal species were favoured in the former. A general decline of ECM root‐tip enzymatic activity for P. pinaster was associated with high fire recurrence, but not for P. halepensis. Fire recurrence and fire‐related factors such as climate, soil properties or tree phenotype explained these results. In addition to the main influence of climate, the tree fire‐adaptive trait serotiny recovered a great portion of the variation in structure and function of ECM fungal communities associated with fire recurrence. Edaphic conditions (especially pH, tightly linked to bedrock type) were an important driver shaping ECM fungal communities, but mainly at the local scale and probably independently of the fire recurrence. Our results show that ECM fungal community shifts are associated with fire recurrence in fire‐prone dry Mediterranean forests, and reveal complex feedbacks among trees, mutualistic fungi and the surrounding environment in these ecosystems.

In molecular ecology, the development of efficient molecular markers for fungi remains an important research domain. Nuclear ribosomal internal transcribed spacer (ITS) region was proposed as universal DNA barcode marker for fungi, but this marker was criticized for Indel-induced alignment problems and its potential lack of phylogenetic resolution. Our main aim was to develop a new phylogenetic gene and a putative functional marker, from single-copy gene, to describe fungal diversity. Thus, we developed a series of primers to amplify a polymorphic region of the Glycoside Hydrolase GH63 gene, encoding exo-acting α-glucosidases, in basidiomycetes. These primers were validated on 125 different fungal genomic DNAs, and GH63 amplification yield was compared with that of already published functional markers targeting genes coding for laccases, N-acetylhexosaminidases, cellobiohydrolases and class II peroxidases. Specific amplicons were recovered for 95% of the fungal species tested, and GH63 amplification success was strikingly higher than rates obtained with other functional genes. We downloaded the GH63 sequences from 483 fungal genomes publicly available at the JGI mycocosm database. GH63 was present in 461 fungal genomes belonging to all phyla, except Microsporidia and Neocallimastigomycota divisions. Moreover, the phylogenetic trees built with both GH63 and Rpb1 protein sequences revealed that GH63 is also a promising phylogenetic marker. Finally, a very high proportion of GH63 proteins was predicted to be secreted. This molecular tool could be a new phylogenetic marker of fungal species as well as potential indicator of functional diversity of basidiomycetes fungal communities in term of secretory capacities.