Research Article: Within-species phylogenetic relatedness of a common mycorrhizal fungus affects evenness in plant communities through effects on dominant species

Date Published: November 21, 2018

Publisher: Public Library of Science

Author(s): Romain Savary, Lucas Villard, Ian R. Sanders, Harald Auge.


Arbuscular mycorrhizal fungi (AMF) have been shown to influence plant community structure and diversity. Studies based on single plant–single AMF isolate experiments show that within AMF species variation leads to large differential growth responses of different plant species. Because of these differential effects, genetic differences among isolates of an AMF species could potentially have strong effects on the structure of plant communities. We tested the hypothesis that within species variation in the AMF Rhizophagus irregularis significantly affects plant community structure and plant co-existence. We took advantage of a recent genetic characterization of several isolates using double-digest restriction-site associated DNA sequencing (ddRADseq). This allowed us to test not only for the impact of within AMF species variation on plant community structure but also for the role of the R. irregularis phylogeny on plant community metrics. Nine isolates of R. irregularis, belonging to three different genetic groups (Gp1, Gp3 and Gp4), were used as either single inoculum or as mixed diversity inoculum. Plants in a mesocosm representing common species that naturally co-exist in European grasslands were inoculated with the different AMF treatments. We found that within-species differences in R. irregularis did not strongly influence the performance of individual plants or the structure of the overall plant community. However, the evenness of the plant community was affected by the phylogeny of the fungal isolates, where more closely-related AMF isolates were more likely to affect plant community evenness in a similar way compared to more genetically distant isolates. This study underlines the effect of within AMF species variability on plant community structure. While differential effects of the AMF isolates were not strong, a single AMF species had enough functional variability to change the equilibrium of a plant community in a way that is associated with the evolutionary history of the fungus.

Partial Text

Soil microorganisms that influence plant-plant interactions play a central role in terrestrial ecosystems [1]. This is particularly true for arbuscular mycorrhizal fungi (AMF; subphylum Glomeromycotina), which are considered the commonest of plant root symbionts, due to their unique capacity to form endosymbioses and to exchange nutrients with 74% of land plants [2]. During the last decades, various beneficial effects of these fungi on different plant species were reported such as an increase in plant growth and plant nutrient acquisition, [3], greater resistance to pathogens [4] and herbivores [5], and increasing tolerance to drought, high salinity and pollutants [6–8]. In addition to direct effects on plant physiology, AMF have also been shown to alter competitive interactions between plants [3]. Consequently, this impacts common metrics of plant community structure, such as community richness, community evenness (i.e the relative abundance of community members) and it affects also the community productivity. For example, removing AMF from nutrient-poor tallgrass prairies, where the dominant plant is highly mycotrophic, had a tendency to favor facultative mycotrophic plants, thus increasing total community evenness and richness without increasing total productivity [9]. Conversely, in grasslands, dominated by grass species that derive little benefit from the association, AMF have been observed to favour the productivity of subordinate forbs [3], thus increasing community evenness and richness [10]. Other studies also demonstrated that AMF could promote or limit community productivity depending on the AMF taxon involved, regardless of plant community species richness [11].

Up to now, the interaction between AMF and plant species within a community was mostly investigated by manipulating AMF at the species level, rarely taking into account the phylogenetic relatedness of AMF isolates. To our knowledge, this study is the first to consider genetic differences among isolates of an AMF species as a source of potential functional trait variability that could differentially impact plant-plant interactions within a community. We show that despite the strong AMF intraspecific effect on single plant responses observed elsewhere [15–16, 18], the effect of R. irregularis isolates on each plant species and on the global community were weak. Though weak, the level of R. irregularis isolate relatedness did influence the response of some plant species in the community. Furthermore, we observed a phylogenetic conservatism on plant community metrics of responsiveness and on community evenness.

To our knowledge, these are the first results to show that within species diversity of these fungi and in particular phylogenetic relatedness can impact mycorrhizal responsiveness of dominant plants in a community and, consequently, biomass partitioning among a community of plants. These results extend the findings of Powell et al. (2009) [14] in that phylogenetic conservatism of AMF functional traits on plant communities can exist within an AMF species and not only between major AMF clades. If confirmed, this feature is interesting because it suggests that the outcomes of plant-fungal and community-fungal interactions are genetically based and could be conserved over evolutionary time. Further studies should focus on AMF traits that are known to be of major importance to plant growth such as level of nutrient acquisition and transfer to the host and consider them in a phylogenetic context at AMF intra-specific level.




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