Expression of α-DIOXYGENASE 1 in Tomato and Arabidopsis Contributes to Plant Defenses Against Aphids

Plant alpha-dioxygenases (alpha-DOX) are fatty acid-hydroperoxidases that contribute to the synthesis of oxylipins, a diverse group of compounds primarily generated through oxidation of linoleic (LA) and linolenic acid (LNA). Oxylipins are implicated in plant signaling against biotic and abiotic stresses. We report here that the potato aphid (Macrosiphum euphorbiae) induces Sl alpha-DOX1 but not Sl alpha-DOX2 expression in tomato (Solanum lycopersicum). Sl alpha-DOX1 upregulation by aphids does not require either jasmonic acid (JA) or salicylic acid (SA) accumulation, since tomato mutants deficient in JA (spr2, acx1) or SA accumulation (NahG) still show Sl alpha-DOX1 induction. Virus-induced gene silencing of Sl alpha-DOX1 enhanced aphid population growth in wild-type (WT) plants, revealing that Sl alpha-DOX1 contributes to basal resistance to aphids. Moreover, an even higher percent increase in aphid numbers occurred when Sl alpha-DOX1 was silenced in spr2, a mutant line characterized by elevated LA levels, decreased LNA, and enhanced aphid resistance as compared with WT. These results suggest that aphid reproduction is influenced by oxylipins synthesized from LA by Sl alpha-DOX1. In agreement with our experiments in tomato, two independent alpha-dox1 T-DNA insertion mutant lines in Arabidopsis thaliana also showed increased susceptibility to the green peach aphid (Myzus persicae), indicating that the role alpha-DOX is conserved in other plant-aphid interactions.