Differential Immune Priming Effects of Banana Extracellular Self-DNA Derived from Bananas with Varying Disease Severities Against Fusarium oxysporum f. sp. cubense Tropical Race 4

Banana Fusarium wilt, caused by Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4), poses a significant threat to global banana production; however, effective and sustainable control strategies remain limited. Extracellular self-DNA (esDNA), which functions as a damage-associated molecular pattern (DAMP), has recently been identified as a crucial regulator of plant innate immunity. Nonetheless, it is unclear whether the immune regulatory function of esDNA varies with disease progression. In this study, we examined the effects of esDNA derived from banana leaves exhibiting different disease severities on plant resistance to Fusarium wilt. Hydroponic experiments revealed that esDNA displayed a distinct disease-stage-dependent regulatory pattern. EsDNA from mildly diseased tissues significantly suppressed Foc TR4 colonization, supported plant growth, and mitigated oxidative damage, whereas esDNA from severely dise ased tissues lost protective effects and even intensified cellular stress. Physiological analyses indicated that beneficial esDNA effectively reduced H2O2 and malondialdehyde accumulation while enhancing antioxidant enzyme activities and phenylpropanoid metabolism. Transcriptome profiling further demonstrated that esDNA extensively altered pathogen-induced gene expression, with enrichment of pathways involved in metabolic and redox homeostasis. These transcriptional changes correlate with the observed reduction in oxidative damage and improved plant growth, suggesting that restoration of homeostasis may contribute to esDNA-mediated resistance. Our findings collectively demonstrate that esDNA serves as a dynamic DAMP signal, exhibiting effects that depend on the disease stage. This study offers new insights into the role of plant self-DNA in mediating immunity and presents a promising strategy for developing environmentally sustainable control measures against banana Fusarium wilt.