Increase in lipoic acid content delays maturation in tomato fruits in cross-talk with ethylene biosynthesis

Lipoic acid (LA) is a potent antioxidant and is also bound as an essential enzymatic cofactor to mitochondrial and plastidial protein complexes, indispensable for all living organisms. In plants, LA biosynthesis requires S-adenosyl-L-methionine (SAM or Ado-Met), which is also the precursor for ethylene production. Tomato (Solanum lycopersicum) fruit maturation is a climacteric process characterized by an autocatalytic rise in ethylene synthesis, increased respiration, and elevated production of reactive oxygen species (ROS), requiring the activation of antioxidant systems. Despite the shared dependence of LA and ethylene biosynthesis on SAM, the interaction between these pathways during fruit maturation remains poorly understood. To address this, fruits from tomato plants subjected to three complementary conditions were analyzed: application of exogenous LA (200 or 500 nM), fruit-specific overexpression of the key enzyme required for LA synthesis, mitochondrial lipoyl synthase (PG:SlLIP1m) to enhance endogenous LA, and inhibition of ethylene biosynthesis using aminoethoxyvinylglycine (AVG). Increased LA levels, achieved either exogenously or genetically, delayed the breaker-to-red transition and significantly increased fruit weight, accompanied by higher bound and free LA pools, greater ethylene levels and enhanced antioxidant capacity at late developmental stages. AVG treatments also delayed maturation and increased LA content, but failed to enhance fruit weight and resulted in reduced antioxidant capacity. LA- and ethylene-enriched fruits displayed altered ethylene dynamics and expression of PG2 and NAP2, whereas AVG treatment reduced expression of both ethylene marker genes, consistent with ethylene inhibition. Collectively, these findings support a more complex interaction between LA and ethylene in regulating tomato fruit maturation through redox and metabolic homeostasis, rather than simple competition for SAM, providing a potential strategy to modulate maturation timing and improve fruit biomass.