Comparative transcriptomics uncovers plant and fungal genetic determinants of mycorrhizal compatibility

Ectomycorrhizal symbiosis supports tree growth and is crucial for nutrient cycling and temperate and boreal ecosystems functioning. The establishment of functional ECM first requires the association of compatible partners. However, host and fungal genetic determinants governing mycorrhizal compatibility are unknown. To identify such factors in poplar and its fungal associates, we mined existing and de-novo tree and fungal transcriptional datasets. We identified core plant regulons enabling ECM symbiosis at early and mature stages of the interaction. These regulons can be divided into general fungal-sensing and ECM-specific components. We highlight the importance of fungal modulation of plant JA-related defences and the regulation of secretory pathways for ECM compatibility, including upregulation of key fungal small secreted proteins, the downregulation of plant secreted peroxidases and the downregulation of plant cell-wall remodelling proteins concomitantly with the upregulation of fungal glycosyl hydrolases acting on pectin. Not only gene-regulation, but also its temporal scale and dynamics seems to play a crucial role for mycorrhizal compatibility. The expression profile of the host Common Symbiosis Pathway was also studied, revealing constitutive levels of expression of a part of the pathway and moderate upregulation in compatible ECM interactions. Overall, these results underscore the importance of novel biological functions during the establishment of ECM symbiosis, help us gain insights into the molecular events determining mycorrhiza compatibility and serve as a data-rich transcriptomic resource to open new research questions in the field. Significance statementEctomycorrhizal symbiosis is essential for forest ecosystems, but the genetic determinants of host and fungal compatibility remain underexplored. Employing comparative transcriptomics, we identified plant general and ECM-specific gene regulons, outlining the expression profile of Common Symbiosis Pathway genes in multiple ECM interactions and highlighting fungal and plant genes associated to interkingdom crosstalk and cell wall remodelling. These findings help us gain insights into the molecular events determining mycorrhiza compatibility.