AtLOX2 plays a role in contrasting the growth of Xylella fastidiosa subsp. fastidiosa Temecula1 in the model Arabidopsis thaliana

Lipids are essential for the versatile lifestyle of the xylem-limited pathogen Xylella fastidiosa, which can transition between planktonic, twitching, and biofilm states. Recently we demonstrated that oxylipins (oxidized unsaturated fatty acids) are hallmarks of X. fastidiosa (Xf) subsp. pauca infection in olive trees and specifically in Ogliarola salentina, one of the most susceptible varieties. Furthermore, we demonstrated that 9- and 13-oxylipins, respectively formed by the action of 9- and 13-lipoxygenases (9- e 13-LOXs) on linolenic acid, act similarly to some bacterial oxylipins (e.g., 10-HpOME deriving from the oleic acid) by promoting biofilm formation instead of planktonic growth of Xf. This study aims to decipher if and how plant 13-LOXs can modulate pathogen virulence in the model plant Arabidopsis thaliana, previously proposed as a potential host for Xf. The first issue was to evaluate the ability of X. fastidiosa subsp. fastidiosa Temecula 1 to colonize wild-type plants respect to lox2 mutant. This mutant is silenced for AtLOX2, a 13-LOX gene involved in the synthesis of jasmonates. The ability of Xf to move from the inoculation point and colonize the distal part of the leaf was evaluated by real-time PCR. The profile of free fatty acids, oxylipins, and the defense hormone levels, as the salicylic and jasmonic acid, of non-infected and infected plants were monitored at different time intervals. The results obtained indicate that the bacterium can colonize the plant foliar tissues with a trend that profoundly differs between the two genotypes (Col-0 vs lox2). In fact, the reduction of 13-oxylipins allows the pathogen to move and colonize of the host to a greater extent. No critical alteration of jasmonic acid level was observed, whereas a crucial decrease in salicylic acid could be related to plant immunity suppression, favoring the pathogen progression. Overall, the data presented demonstrated the implication of plant 13-oxylipins in pathogen invasion abilities and plant defense responses.