Alternative oxidase in resistance to biotic stresses: Nicotiana attenuata AOX contributes to resistance to a pathogen and a piercing-sucking insect but not Manduca sexta Larvae

The role of the alternative respiratory pathway in the protection of plants against biotic stress was examined in transgenic tobacco (Nicotiana attenuata) plants (irAOX) silenced in the expression of ALTERNATIVE OXIDASE (AOX) gene. Wild-type and irAOX plants were independently challenged with (1) chewing herbivores (Manduca sexta), (2) piercing-sucking insects (Empoasca spp.), and (3) bacterial pathogens (Pseudomonas syringae pv tomato DC3000), showing that all these treatments can strongly elicit accumulation of AOX gene transcripts in wild-type plants. When N. attenuata chemical defenses and resistance were examined, irAOX plants showed wild-type levels of defense-related phytohormones, secondary metabolites, and resistance to M. sexta. In contrast, piercing-sucking leafhoppers (Empoasca spp.) caused more leaf damage and induced significantly higher salicylic acid levels in irAOX compared with wild-type plants in the field and/or glasshouse. Subsequently, irAOX plants accumulated lower levels of defense metabolites, 17-hydroxygeranyllinalool diterpene glycosides, caffeoylputrescine, and nicotine compared with wild-type plants under prolonged attack of Empoasca spp. in the glasshouse. Finally, an accelerated cell death phenotype was observed in irAOX plants infected with P. syringae, which correlated with higher levels of salicylic acid and hydrogen peroxide levels in pathogen-infected irAOX compared with wild-type leaves. Overall, the AOX-associated changes in phytohormone and/or redox levels appear to support the resistance of N. attenuata plants against cell piercing-sucking insects and modulate the progression of cell death in pathogen-infected tissues but are not effective against rapidly feeding specialist herbivore M. sexta.