Chemical cues from beetle larvae trigger proliferation and virulence of a plant pathogen

Pest insects and microbial pathogens threaten agricultural crop productivity and global forest biomes, and insect-microbe interactions can increase the severity of plant decline. Whilst bacterial chemicals have been shown to influence insect behaviour, the impact of insect-derived chemistries on phytopathogens is barely understood. Here, we investigated beetle larvae-bacteria interactions in acute oak decline (AOD), a decline disease of oak characterised by inner bark necrosis caused by a polymicrobial consortium including Brenneria goodwinii and larval galleries of Agrilus biguttatus. To test the hypothesis that larval chemicals influence the activity of B. goodwinii, we extracted A. biguttatus larvae and tested the effect of extracts on the growth and gene expression of B. goodwinii in vitro. We demonstrate that larval chemicals elicit increased bacterial growth rate and final cell density, as well as differential expression of almost 800 genes, including the Type III Secretion System and its effectors, major virulence factors in other plant pathogens. Contrastingly, gallery woody-tissue extracts induced no such effects. Our work highlights the importance of multi-kingdom interactions in plant disease and demonstrate a novel mode-of-action for insect-derived chemical elicitors in facilitating the virulence of phytopathogens, which may be important in understanding plant diseases globally.