| Summary: | <i>Streptomyces alfalfa</i> strain 11F has inhibitory effects on many phytopathogenic fungi and improves the establishment and biomass yield of switchgrass. However, the antagonistic effects of strain 11F on <i>Fusarium</i> wilt of watermelon and its secondary metabolites that contribute to its biocontrol activity are poorly understood. We evaluated the antagonistic and growth-promoting effects of strain 11F and conducted a transcriptome analysis to identify the metabolites contributing to antifungal activity. Strain 11F had marked inhibitory effects on six fungal pathogens. The incidence of <i>Fusarium</i> wilt of watermelon seedlings was decreased by 46.02%, while watermelon seedling growth was promoted, as indicated by plant height (8.7%), fresh weight (23.1%), and dry weight (60.0%). Clean RNA-sequencing data were annotated with 7553 functional genes. The 2582 differentially expressed genes (DEGs) detected in the Control vs. Case 2 comparison were divided into 42 subcategories of the biological process, cellular component, and molecular function Gene Ontology categories. Seven hundred and forty functional genes (55.47% of the DEGs) were assigned to Kyoto Encyclopedia of Genes and Genomes metabolic pathways, reflecting the complexity of the strain 11F metabolic regulatory system. The expression level of the gene <i>phzF</i>, which encodes an enzyme essential for phenazine-1-carboxylic acid (PCA) synthesis, was downregulated 3.7-fold between the 24 h and 48 h fermentation time points, suggesting that strain 11F can produce phenazine compounds. A phenazine compound from 11F was isolated and identified as phenazine-1-carboxamide (PCN), which contributed to the antagonistic activity against <i>Fusarium oxysporum</i> f. sp. <i>niveum</i>. PCA was speculated to be the synthetic precursor of PCN. The downregulation in <i>phzF</i> expression might be associated with the decrease in PCA accumulation and the increase in PCN synthesis in strain 11F from 24 to 48 h. <i>Streptomyces alfalfae</i> 11F protects watermelon seedlings from <i>Fusarium</i> wilt of watermelon and promotes seedling growth. The transcriptome analysis of strain 11F provides insights into the synthesis of PCN, which has antifungal activity against <i>F. oxysporum</i> f. sp. <i>niveum</i> of watermelon.
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