Coupling the endophytic microbiome with the host transcriptome in olive roots

The connection between olive genetic responses to environmental and agro-climatic conditions and the composition, structure and functioning of host-associated, belowground microbiota has never been studied under the holobiont conceptual framework. Two groups of cultivars growing under the same environmental, pedological and agronomic conditions, and showing highest (AH) and lowest (AL) Actinophytocola relative abundances, were earlier identified. We aimed now to: i) compare the root transcriptome profiles of these two groups harboring significantly different relative abundances in the above-mentioned bacterial genus; ii) examine their rhizosphere and root-endosphere microbiota co-occurrence networks; and iii) connect the root host transcriptome pattern to the composition of the root microbial communities by correlation and co-occurrence network analyses. Significant differences in olive gene expression were found between the two groups. Co-occurrence networks of the root endosphere microbiota were clearly different as well. Pearson’s correlation analysis enabled a first portray of the interaction occurring between the root host transcriptome and the endophytic community. To further identify keystone operational taxonomic units (OTUs) and genes, subsequent co-occurrence network analysis showed significant interactions between 32 differentially expressed genes (DEGs) and 19 OTUs. Overall, negative correlation was detected between all upregulated genes in the AH group and all OTUs except of Actinophytocola. While two groups of olive cultivars grown under the same conditions showed significantly different microbial profiles, the most remarkable finding was to unveil a strong correlation between these profiles and the differential gene expression pattern of each group. In conclusion, this study shows a holistic view of the plant-microbiome communication.