The influence of light and leaf antioxidant status on plant responses to aphids

Cross-tolerance to environmental stresses results from the synergistic co-activation of defence pathways that cross biotic-abiotic stress boundaries. However, the signalling mechanisms that underpin such responses remain poorly characterised. The effects of an abiotic stress (high light; HL) on the responses of Arabidopsis thaliana and tobacco (Nicotiana tabacum) plants to a biotic stress (infestation by the green peach aphid, Myzus persicae) were therefore analysed. Particular focus was placed on the role of cellular redox state as a regulator of cross-tolerance phenomena and the identification of signalling pathways that underpin aphid resistance. Aphid fecundity was measured in a range of A. thaliana mutants that have defects in non-enzymatic antioxidants (ascorbate and glutathione), enzymatic antioxidants (catalase) or downstream kinase/phosphatase signalling cascades, and in transgenic tobacco lines that have either increased or decreased levels of ascorbate oxidase. A pre-treatment with HL increased the resistance of transgenic tobacco plants with low ascorbate oxidase to aphid infestation. In contrast, the A. thaliana ascorbate oxidase knockout mutants did not show the HL-dependent decrease in aphid infestation. Aphid fecundity was decreased on A. thaliana mutants that have altered antioxidant (ascorbate, glutathione, catalase) status, or that lack the gamma (γ) subunit of protein phosphatase (PP2A). A pre-treatment with HL increased the resistance of A. thaliana plants to aphid infestation in all of the genotypes, except for the cat2 mutants that lack the photorespiratory form of leaf catalase and glutathione defective mutants. Taken together these findings demonstrate that redox processes and oxidative signalling are important modulators of aphid resistance and the light-aphid interaction. Moreover, the analysis of aphid fecundity on these A. thaliana mutants, which also have different levels of leaf camalexin, suggests that the levels of this secondary metabolite alone do not influence aphid infestation. A transcriptome and metabolome profiling analysis of the responses of the different tobacco lines highlights the central role of cell wall modifications/signalling as key components in plant responses to aphid infestation.