Trans-2-decenal inhibits Alternaria alternata through disruption of redox homeostasis and membrane integrity.

Abstract

BACKGROUND Alternaria alternata is a globally distributed plant pathogen infecting >400 plant species. Trans-2-decenal is a notable plant-derived secondary metabolite with strong volatility and antifungal properties, although its specific activity and mode-of-action against A. alternata remain unclear. RESULTS Toxicity assays showed that trans-2-decenal inhibited A. alternata with a median inhibitory concentration (IC50) of 12.23 mg L-1. Treated with trans-2-decenal resulted in hyphal abnormalities, reduced spore production and suppressed spore germination. Mechanistically, it disrupted fungal cell membrane integrity, as confirmed by propidium iodide staining and increased leakage of DNA and soluble proteins in conductivity assays. Further investigations revealed that trans-2-decenal disrupted redox homeostasis by inducing reactive oxygen species (ROS) accumulation. DCFH-DA fluorescence staining showed elevated ROS levels, whereas antioxidant enzyme assays revealed dose-dependent changes, including decreased superoxide anion (O2.-) and catalase (CAT) activity, and significantly increased hydrogen peroxide (H2O2), superoxide dismutase (SOD) and malondialdehyde (MDA) levels, collectively indicating oxidative stress and damage. Transcriptome analysis identified 2319 differentially expressed genes (DEGs), with gene ontology (GO) enrichment highlighting inhibition of pathways associated with oxidative stress response, transmembrane transport and ribosome biogenesis. Molecular docking further suggested interactions between trans-2-decenal and key antioxidant enzyme and membrane transporter of A. alternata. In vivo assays showed that 32 mg L-1 trans-2-decenal fumigation achieved protective and curative efficacies of 97.14% and 96.54%, respectively, against yam leaf spot disease. CONCLUSION Trans-2-decenal inhibited A. alternata through a multitarget synergistic mechanism, providing theoretical support for its development as a plant-derived biofumigant and a promising tool for the green management of A. alternata-induced diseases. © 2025 Society of Chemical Industry.