Lipid peroxidation (LPO) is induced by a variety of abiotic and biotic stresses. Although LPO is involved in diverse signaling processes, little is known about the oxidation mechanisms and major
lipid targets. A systematic lipidomics analysis of LPO in the interaction of Arabidopsis (Arabidopsis thaliana) with Pseudomonas syringae revealed that LPO is predominantly confined to plastid
lipids comprising
galactolipid and triacylglyceride species and precedes programmed cell death.
Singlet oxygen was identified as the major cause of
lipid oxidation under basal conditions, while a
13-lipoxygenase (LOX2) and
free radical-catalyzed
lipid oxidation substantially contribute to the increase upon pathogen
infection. Analysis of lox2 mutants revealed that LOX2 is essential for enzymatic membrane peroxidation but not for the pathogen-induced free
jasmonate production. Despite massive oxidative modification of plastid
lipids, levels of nonoxidized
lipids dramatically increased after
infection. Pathogen
infection also induced an accumulation of fragmented
lipids. Analysis of mutants defective in 9-lipoxygenases and LOX2 showed that
galactolipid fragmentation is independent of LOXs. We provide strong in vivo evidence for a
free radical-catalyzed
galactolipid fragmentation mechanism responsible for the formation of the essential
biotin precursor
pimelic acid as well as of
azelaic acid, which was previously postulated to prime the immune response of Arabidopsis. Our results suggest that
azelaic acid is a general marker for LPO rather than a general immune signal. The proposed fragmentation mechanism rationalizes the pathogen-induced radical amplification and formation of electrophile signals such as phytoprostanes,
malondialdehyde, and
hexenal in plastids.