Weaponizing nutrition: plants use a double strategy to fight herbivory, converting nutritionally essential fatty acids into defensive oxylipin signals

Jasmonates, key plant immune hormones, derive almost exclusively from omega-3 polyunsaturated fatty acids (n3-PUFAs), yet the evolutionary rationale for this substrate specificity remains unresolved. This study employed the liverwort Marchantia polymorpha to investigate the functional roles of omega-3 fatty acid desaturases (n3-FADs) in n3-PUFA metabolism, jasmonate biosynthesis and plant defense. CRISPR-Cas9-mediated loss-of-function mutants were generated for MpFAD3 (endoplasmic reticulum-localized) and MpFAD7 (chloroplast-localized), including a double mutant (Mpfad3fad7). Phenotypic characterization encompassed fatty acid and jasmonate profiling, transcriptomic analysis, pathogen inoculation (Fusarium oxysporum), herbivory assays (Spodoptera exigua) and dietary PUFA supplementation experiments. We found that MpFAD3 and MpFAD7 control distinct jasmonate subsets, with Mpfad3fad7 representing the first fully jasmonate-deficient Marchantia line. Contrary to expectations, jasmonate-deficient fad mutants did not support enhanced larval performance, whereas dietary n3-PUFA supplementation significantly promoted caterpillar growth and pupation success. Our results indicate that plants deploy a dual anti-herbivore defense strategy by converting nutritionally essential n3-PUFAs into defense signals, simultaneously depleting insect nutrients and activating immune responses. The presence of both n3-PUFAs and oxylipins in algae lacking jasmonate pathways supports n3-PUFA depletion as an ancestral defense mechanism predating jasmonate-dependent immunity.