Lipoxygenase‐derived 9‐hydro(pero)xides of linoleoylethanolamide interact with ABA signaling to arrest root development during Arabidopsis seedling establishment

Summary Ethanolamide‐conjugated fatty acid derivatives, also known as N ‐acylethanolamines ( NAE s), occur at low levels (μg per g) in desiccated seeds, and endogenous amounts decline rapidly with seedling growth. Linoleoylethanolamide ( NAE 18:2) is the most abundant of these NAE s in seeds of almost all plants, including Arabidopsis thaliana . In Arabidopsis, NAE 18:2 may be oxidized by lipoxygenase ( LOX ) or hydrolyzed by fatty acid amide hydrolase ( FAAH ) during normal seedling establishment, and this contributes to the normal progression of NAE depletion that is coincident with the depletion of abscisic acid ( ABA ). Here we provide biochemical, genetic and pharmacological evidence that a specific 9‐ LOX metabolite of NAE 18:2 [9‐hydro(pero)xy linoleoylethanolamide (9‐ NAE ‐H(P) OD )] has a potent negative influence on seedling root elongation, and acts synergistically with ABA to modulate the transition from embryo to seedling growth. Genetic analyses using mutants in ABA synthesis ( aba1 and aba2 ), perception ( pyr1 , pyl1 , pyl2 , pyl4 , pyl5 and pyl8 ) or transcriptional activation ( abi3 ‐ 1 ) indicated that arrest of root growth by 9‐ NAE ‐H(P) OD requires an intact ABA signaling pathway, and probably operates to increase ABA synthesis as part of a positive feedback loop to modulate seedling establishment in response to adverse environmental conditions. These results identify a specific, bioactive ethanolamide oxylipin metabolite of NAE 18:2, different from those of ethanolamide‐conjugated linolenic acid ( NAE 18:3), as well as a molecular explanation for its inhibitory action, emphasizing the oxidative metabolism of NAE s as an important feature of seedling development.