Abstract
BackgroundPlants, fungi, and bacteria form complex, mutually-beneficial communities within the soil environment. In return for photosynthetically derived sugars in the form of exudates from plant roots, the microbial symbionts in these rhizosphere communities provide their host plants access to otherwise inaccessible nutrients in soils and help defend the plant against biotic and abiotic stresses. One role that bacteria may play in these communities is that of Mycorrhizal Helper Bacteria (MHB). MHB are bacteria that facilitate the interactions between plant roots and symbiotic mycorrhizal fungi and, while the effects of MHB on the formation of plant-fungal symbiosis and on plant health have been well documented, the specific molecular mechanisms by which MHB drive gene regulation in plant roots leading to these benefits remain largely uncharacterized.ResultsHere, we investigate the effects of the bacterium Pseudomonas fluorescens SBW25 (SBW25) on aspen root transcriptome using a tripartite laboratory community comprised of Populus tremuloides (aspen) seedlings and the ectomycorrhizal fungus Laccaria bicolor (Laccaria). We show that SBW25 has MHB activity and promotes mycorrhization of aspen roots by Laccaria. Using transcriptomic analysis of aspen roots under multiple community compositions, we identify clusters of co-regulated genes associated with mycorrhization, the presence of SBW25, and MHB-associated functions, and we generate a combinatorial logic network that links causal relationships in observed patterns of gene expression in aspen seedling roots in a single Boolean circuit diagram. The predicted regulatory circuit is used to infer regulatory mechanisms associated with MHB activity.ConclusionsIn our laboratory conditions, SBW25 increases the ability of Laccaria to form ectomycorrhizal interactions with aspen seedling roots through the suppression of aspen root antifungal defense responses. Analysis of transcriptomic data identifies that potential molecular mechanisms in aspen roots that respond to MHB activity are proteins with homology to pollen recognition sensors. Pollen recognition sensors integrate multiple environmental signals to down-regulate pollenization-associated gene clusters, making proteins with homology to this system an excellent fit for a predicted mechanism that integrates information from the rhizosphere to down-regulate antifungal defense response genes in the root. These results provide a deeper understanding of aspen gene regulation in response to MHB and suggest additional, hypothesis-driven biological experiments to validate putative molecular mechanisms of MHB activity in the aspen-Laccaria ectomycorrhizal symbiosis.
Highlights
Plants, fungi, and bacteria form complex, mutually-beneficial communities within the soil environment
Phenotypic measurements of aspen in tripartite community Aspen seedlings were cultured in sand pots supplemented under four experimental conditions: aspen seedlings alone, aspen seedlings inoculated with Laccaria, aspen seedlings inoculated with SBW25, and aspen
To identify if Laccaria or SBW25 was present in the rhizosphere community from transcriptomic data, we determined whether a statistically significant enrichment for fungal or bacterial reads could be detected in transcriptomes where SBW25 or Laccaria are present relative to those experimental conditions where SBW25 or Laccaria are absent
Summary
Fungi, and bacteria form complex, mutually-beneficial communities within the soil environment. Plants form complex, mutually-beneficial communities with fungi and bacteria that live within the rhizosphere, which is the narrow band of soil directly infused by plant root exudates. The plant receives a wide variety of ecological services from its root-associated organisms, including access to sources of nutrients that would otherwise be unavailable to the plant and protection from biotic and abiotic stresses [2,3,4,5].These interactions occur through the exchange of small molecules, such as nutrients, signaling compounds, and small secreted proteins between the community partners [6,7,8]. MHB facilitate plant-fungal interactions through the production of effectors and/or hormones that drive patterns of gene regulation in both plant roots and mycorrhizal fungi hyphae that enhance their subsequent mycorrhizal interactions [10, 18]
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