Chemical cues from Agrilus biguttatus beetle larvae trigger proliferation and putative virulence gene expression of the tree pathogen Brenneria goodwinii

Aims: Agricultural crop productivity and global forest biomes are coming under increasing threat from insect pests and microbial pathogens. This impact is worsened by inter-kingdom insect–microbe interactions that can increase transmission and disease severity in affected plants. While bacterial chemical cues have been shown to directly influence insect behaviour, the impact of insect-derived compounds on phytopathogens is poorly understood. Here, we investigated the chemical basis for interactions between beetle larvae and bacteria in acute oak decline (AOD), a disease characterized by inner bark necrosis of Quercus robur and Q. petraea involving a polymicrobial consortium, including Brenneria goodwinii and larval galleries of Agrilus biguttatus. Methods and results: We found that A. biguttatus larval extractable metabolites increase bacterial growth rate and final cell density during in vitro culture, and stimulate the differential expression of ∼600 genes, including the type III secretion system and its effectors, which are major virulence factors in plant pathogens. Chemical compounds from closely related insect species did not have this effect. Conclusions: These findings highlight the importance of inter-kingdom interactions in plant disease and suggest a role for insect-derived chemical elicitors in facilitating the virulence of phytopathogens.