The Armillaria response to Gastrodia elata is partially mediated by strigolactone-induced changes in reactive oxygen species

Armillaria root diseases, caused by Armillaria spp., pose a significant threat to woody plants worldwide and result in substantial economic losses. However, certain species in the genus Armillaria can establish a unique symbiotic relationship with Gastrodia elata, which is the only known example of a plant benefiting from Armillaria. Although various plant signals that play a role in this interaction have been identified, the mechanism remains largely unknown from the Armillaria's perspective. In this study, we performed whole-genome sequencing of an Armillaria gallica strain named NRC001 isolated from G. elata. Comparative genomic analysis showed it is low-pathogenic Armillaria spp., which possesses 169 expanded gene families compared to high-pathogenic Armillaria spp. Among these expanded families, transcriptomic analysis revealed a significant increase in expression levels of four reactive oxygen species (ROS)-related gene families in A. gallica on G. elata compared to A. gallica on wood. Thus, a systematic survey of ROS-related gene families was carried out, and a total of 218 genes belonging to 44 ROS-related gene families in A. gallica were identified. Physiological experiments and transcriptome analysis showed that strigolactones (SLs) released by G. elata have a mediation impact on ROS, particularly enhancing the ROS scavenging activities by increasing the expression level and activity of several enzymes, such as catalase and glutathione reductase. Among the ROS-related genes, the aquaporin (AQP) is crucial as it is responsible for transporting hydrogen peroxide (H2O2) across the cell membrane. Five orthologs of AQP genes in A. gallica were identified and overexpressed in yeast. Only AgAQPA from the so-called 'other aquaglyceroporin' subfamily was demonstrated to be capable of mediating H2O2 transport in A. gallica. To our best knowledge, this is the first 'other aquaglyceroporins' gene in fungi to be identified as having transporter capacity. This study not only provides new insights into the mechanisms by which SL signaling regulates interactions between Armillaria and G. elata, but also sheds light on the function of fungal AQPs.