Organic acids induce plant defense responses and suppress root-knot nematodes in tomato via molecular mechanisms and molecular docking insights

Abstract

Abstract Root-knot nematodes ( Meloidogyne spp. ) are among the most destructive pathogens affecting tomato production worldwide, leading to severe yield losses and compromised plant health. This study evaluated the efficacy of six organic acids—benzoic, salicylic, citric, lactic, malic, and acetic acids—applied at three concentrations each, in managing Meloidogyne incognita infection in tomato cultivar “023.”Among all treatments, salicylic acid (SA) exhibited the strongest nematicidal activity, achieving 100% juvenile mortality within 72 hours and the highest inhibition of egg hatchability, even at the lowest concentration (0.01%). Benzoic and malic acid followed, showing strong nematocidal effects with moderate suppression of egg hatching, while citric and lactic acids displayed intermediate efficacy. Acetic acid was the least effective. Under greenhouse conditions, Salicylic acid alleviated nematode-induced growth loss through a significant reduction in root galling, egg masses, larvae, and egg counts, resulting in marked improvements in shoot and root biomass compared to the infected untreated control and other treatments. Citric and benzoic acids moderately improved plant growth, especially in root development, whereas lactic and acetic acids had minimal effects. At the molecular level, salicylic acid markedly upregulated the expression of peroxidase (POD) and polyphenol oxidase (PPO) genes, peaking at day 4 and remaining elevated through day 8. Citric, benzoic, and malic acids caused moderate induction, while lactic and acetic acids induced weak or transient expression. The expression pattern suggests dynamic and transient defense activation in response to organic acid treatments. Computational insights obtained through molecular docking simulations predicted that salicylic and benzoic acids may interfere with essential biological processes in Meloidogyne incognita . Both compounds exhibited the highest binding affinities toward several key pathogenicity-related proteins, including NAD(P)H oxidase, putative aspartyl protease, cytochrome c oxidase subunit 1, prefoldin-2, venom allergen-like protein Mi-vap-2, and protein disulfide-isomerase, complementing their in vivo nematicidal effects. Overall, salicylic acid at 0.01% emerged as the most potent and eco-friendly alternative for managing root-knot nematodes in tomato plants, combining strong nematicidal activity, enhanced plant defense responses, and molecular-level evidence of protein inhibition.