Abstract
The soil-borne fungus Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4) causes banana Fusarium wilt, a serious threat to global banana production. Biocontrol represents a promising alternative to conventional chemical control for managing this disease. Our previous studies identified Streptomyces luomodiensis SCA4-21 as a novel species with antifungal properties. Here, we show that the extract from strain SCA4-21 significantly inhibits Foc TR4 mycelial growth and spore germination, severely disrupting hyphal and spore ultrastructure. The extract also exhibited broad-spectrum activity against eight other phytopathogenic fungi. We identified 32 volatile organic compounds produced by strain SCA4-21, including five with known antifungal properties. In pot experiments, strain SCA4-21 inoculation not only significantly suppressed Foc TR4 infection in banana seedlings, with a biocontrol efficacy of 59.3%, but also markedly promoted plant growth. The inoculation significantly enriched beneficial bacterial genera (Streptomyces, Bacillus, Sphingomonas, Massilia, and Pseudomonas) and fungal genera (Mortierella, Gibellulopsis, and Xenomyrothecium), while reducing the pathogenic bacterium Pantoea and lowering Fusarium abundance to levels statistically indistinguishable from the control. Microbial function prediction based on 16S rRNA gene sequencing data revealed enhanced metabolic pathways, including carbohydrate metabolism, amino acid metabolism, and metabolism of terpenoids and polyketides. We propose that strain SCA4-21 combats banana Fusarium wilt through a synergistic mechanism involving antifungal compound production and recruitment of beneficial microbiota. These findings highlight strain SCA4-21 as a promising biocontrol agent for sustainable banana production. IMPORTANCE: Banana (Musa spp.) is one of the most popular fruit crops and the fourth largest food crop in developing countries within tropical and subtropical regions. However, the emergence and rapid spread of strain Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4) seriously hinder the development of the banana industry. Currently, there is no effective control measure available. Biological control holds potential due to its safety and effectiveness. Here, we found that the extract of Streptomyces luomodiensis SCA4-21 exhibited significant inhibitory effects on the hyphal growth and spore germination of Foc TR4, as well as severe destructive effects on its cell morphology and ultrastructure, and broad-spectrum antifungal activity. We also discovered that the inoculation of strain SCA4-21 significantly inhibited the infection of Foc TR4 in banana seedling corms, reduced the incidence index of banana Fusarium wilt, promoted the growth of banana seedlings, and enhanced beneficial microbes and metabolic pathways, suggesting that strain SCA4-21 is a promising biocontrol agent.