Profiles of secoiridoids and alkaloids in tissue of susceptible and resistant green ash progeny reveal patterns of induced responses to emerald ash borer inFraxinus pennsylvanica

Abstract

The emerald ash borer (Agrilus planipennis, EAB) invasion in North America threatens most North American Fraxinus species, including green ash (F. pennsylvanica), the mostly widely distributed species. A small number of green ash (lingering ash, 0.1-1%) survive years of heavy EAB attack and kill more EAB larvae when challenged in greenhouse studies than susceptible controls. We combined untargeted metabolomics with intensive phenotyping of segregating F1 progeny from susceptible or lingering ash parents to detect chemotypes associated with defensive responses to EAB. We examined three contrasting groups: low larval kill (0-25% of larvae killed), high larval kill (55-95% of larvae killed) and uninfested. Contrasting the chemotypes of these groups revealed evidence of an induced response to EAB. Infested trees deployed significantly higher levels of select secoiridoids than uninfested trees. Within the infested group, the low larval kill (LLK) individuals deployed significantly higher levels of select secoiridoids than the high larval kill (HLK) individuals. The HLK individuals deployed significantly higher concentrations of three metabolites annotated as aromatic alkaloids compared to the LLK and uninfested individuals. We propose a two-part model for the North American Fraxinus response to EAB wherein every individual has the capacity to detect and respond to EAB, but only certain trees mount an effective defense, killing enough EAB larvae to prevent or minimize lethal damage to the vascular system. Integration of intensive phenotyping of structured populations with metabolomics reveals the multi-faceted nature of the defenses deployed in naive host populations against invasive species.