Self-eating while being eaten: Elucidating the relationship between aphid feeding and the plant autophagy machinery in Arabidopsis leaves

Abstract

AbstractAutophagy, an intracellular process that facilitates the degradation of cytoplasmic materials, plays a dominant role in plant fitness and immunity. While autophagy was shown to be involved in plant response to fungi, bacteria, and viruses, its role in response to insect herbivory is as yet unknown. In this study, we demonstrate a role of autophagy in plant defense against herbivory usingArabidopsis thalianaand the green peach aphid,Myzus persicae. Following six hours of aphid infestation of wildtype plants, we observed high expression of the autophagy-related genesATG8aandATG8f, as well asNBR1(Next to BRCA1 gene 1), a selective autophagy receptor. Moreover, the number of autophagosomes detected by the overexpression of GFP-fused ATG8f in Arabidopsis increased upon aphid infestation. Following this,atg5.1andatg7.2mutants were used to study the effect of autophagy on aphid reproduction and feeding behavior. While aphid reproduction on both mutants was lower than on wildtype, feeding behavior was only affected byatg7.2mutants. Moreover, upon aphid feeding, thePhytoalexin-deficient 4(PAD4) defense gene was upregulated in wildtype plants but not affected in the mutants. By contrast, the hydrogen peroxide content was much higher in the mutants relative to wildtype, which might have disturbed aphid reproduction and interfered with their feeding. Additionally, an analysis of the phloem sap metabolite profile revealed thatatg7.2mutant plants have lower levels of amino acids and sugars. These findings, together with the high hydrogen peroxide levels, suggest that aphids might exploit the plant autophagy mechanism for their survival.