Oak displays common local but specific distant gene regulation responses to different mycorrhizal fungi.

Background: Associations of tree roots with diverse symbiotic mycorrhizal fungi have distinct effects on whole plant functioning. An untested explanation might be that such effect variability is associated with distinct impacts of different fungi on gene expression in local and distant plant organs. Using a large scale transcriptome sequencing approach, we compared the impact of three ectomycorrhizal (EMF) and one orchid mycorrhizal fungi (OMF) on gene regulation in colonized roots (local), non-colonized roots (short distance) and leaves (long distance) of the Quercus robur clone DF159 with reference to the recently published oak genome. Since different mycorrhizal fungi form symbiosis in a different time span and variable extents of apposition structure development, we sampled inoculated but non-mycorrhizal plants, for which however markedly symbiotic effects have been reported. Local root colonization by the fungi was assessed by fungal transcript analysis.
Results: The EMF induced marked and species specific effects on plant development in the analysed association stage, but the OMF did not. At local level, a common set of plant differentially expressed genes (DEG) was identified with similar patterns of responses to the three EMF, but not to the OMF. Most of these core DEG were down-regulated and correspond to already described but also new functions related to establishment of EMF symbiosis. Analysis of the fungal transcripts of two EMF in highly colonized roots also revealed onset of a symbiosis establishment. In contrast, in the OMF, the DEG were mainly related to plant defence. Already at short distances, high specificities in transcriptomic responses to the four fungi were detected, which were further enhanced at long distance in leaves, where almost no common DEG were found between the treatments. Notably, no correlation between phylogeny of the EMF and gene expression patterns was observed.
Conclusions: Use of clonal oaks allowed us to identify a core transcriptional program in roots colonized by three different EMF, supporting the existence of a common EMF symbiotic pathway. Conversely, the specific responses in non-colonized organs were more closely related to the specific impacts of the different of EMF on plant performance.