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Abstract
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.
Highlights
The role of the alternative respiratory pathway in the protection of plants against biotic stress was examined in transgenic tobacco (Nicotiana attenuata) plants silenced in the expression of ALTERNATIVE OXIDASE (AOX) gene
Two AOX genes, NaAOX1 and NaAOX2, from N. attenuata of nearly identical nucleotide sequence, have been previously deposited in public National Center for Biotechnology Information databases (AY422688, AY422689). Both genes show a high level of identity to members of the Arabidopsis AOX1 gene family: NaAOX1 and NaAOX2 proteins are 70.7% and 70.3% identical to AtAOX1a from Arabidopsis (Supplemental Fig. S1A)
The high degree of identity between NaAOX1 and NaAOX2 genes at the nucleotide level did not allow for efficient monitoring and gene-specific silencing of individual NaAOX isoforms by quantitative reverse transcription PCR and RNA interference (RNAi), respectively
Summary
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. The induction of AOX in leafy mustard (Brassica juncea) during infection with turnip mosaic virus was suppressed in the presence of ethylene biosynthesis inhibitor aminoethoxyvinylglycine, suggesting that ethylene and AOX are likely involved in leafy mustard’s systemic resistance to virus infection (Zhu et al, 2011) Bacterial pathogens and their elicitors strongly elicit AOX transcript accumulations and protein levels, both in leaves and cell suspensions (Krause and Durner, 2004; Mizuno et al, 2005; Kiba et al, 2008). In Paracoccidioides brasiliensis, a human thermal dimorphic pathogenic fungus, PbAOX played an important role in fungal defense response against oxidative stress imposed by immune cells and virulence of the pathogen (Ruiz et al, 2011)
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