Vacuolar Processing Enzymes are Components of Basal Defenses Against Phloem-Feeding Insect Herbivores

The vacuole is a major organelle involved in programmed cell death (PCD) in plants and the vacuolar processing enzymes (VPE) have been implicated in PCD-mediated defenses. Our earlier studies have shown that certain VPE isoforms are highly induced in aphid-resistant introgression lines derived from S. tuberosum x S. bulbocastanum but not in their sibling lines that are susceptible to aphids.  To clarify the question regarding any direct involvement of VPEs to plant defenses against a sucking herbivore (Myzus persicae), we examined a subset of T-DNA insertion mutants in Arabidopsis. Two VPE isoforms (β-VPE, δ-VPE) were found to be induced within 48 hours after aphid feeding in wild-type Arabidopsis, while their T-DNA insertion mutants exhibited a knock-down and knock-out expression, respectively. Basal resistance to aphids were compromised in both β-VPE and δ-VPE mutants relative to the wild-type, manifested by an earlier onset of leaf curling and tissue necrosis, rapid aphid reproduction, and other physiological measures of tissue injury. The β-VPE and δ-VPE networks are comprised of genes involved in sucrose metabolism and transport (AtSUC5, AtSUS3, invertases), efflux and detoxification-related proteins (carboxypeptidases), and known modulators of gene-for-gene-type disease resistance linked to sucrose metabolism (AtSweet13, AtSweet15). Our results suggest that VPEs are important components of basal resistance to phloem-feeders, perhaps by mediating mechanisms directly involved in detoxification, while also ensuring nutrient/metabolite availability to the host tissues to counteract a potentially depleting condition caused by insect feeding. These mechanisms might be important for slowing down the progression of perturbations caused by herbivory.