Volatile-mediated microbiome enrichment by Streptomyces albidoflavus G1 enhances suppression of apple ring rot pathogen Botryosphaeria dothidea

Apple ring rot, caused by the fungal pathogen Botryosphaeria dothidea , is a devastating disease that causes substantial production and postharvest losses worldwide. Microbial volatile organic compounds (VOCs) are promising biocontrol agents against postharvest fungal diseases. However, how VOCs produced by Streptomyces albidoflavus suppress B. dothidea and whether they are associated with changes in the apple microbiota and the host transcriptional response remains largely unexplored. This study integrated volatilome profiling, microbiome analysis, VOC-bacterial interaction assays, and apple transcriptome profiling to investigate how G1-VOCs suppress apple ring rot. G1 showed strong VOC-mediated inhibitory activity against B. dothidea in bipartite plate and detached fruit assays. GC–MS analysis identified differentially abundant volatiles associated with sesquiterpenoid, triterpenoid, and phenylalanine metabolism, and selected VOC standards impaired fungal growth, membrane integrity, and biofilm formation under the tested assay conditions. 16S rRNA gene amplicon analysis revealed that G1-VOC exposure under pathogen challenge was associated with a simplified, Pseudomonas -dominated bacterial community in internal lesion-margin tissues, accompanied by increased Pseudomonas -specific 16S rRNA gene copies. The cultivable isolate Pseudomonas paracarnis aNRL1, recovered from G1-VOC-treated lesion-margin tissues, matched the enriched Pseudomonas -assigned ASV_2, strongly inhibited B. dothidea in vitro , and reduced lesion development on apple fruit. Selected G1-associated volatiles exerted compound-specific effects on aNRL1 growth, biofilm formation and motility. Apple transcriptome analysis further revealed pathogen-dependent remodeling of brassinosteroid signaling, together with increased expression of genes related to mitogen-activated protein kinase (MAPK), lipid metabolism, and cuticle/wax biosynthesis. Together, these findings support a multilayered model in which G1-derived VOCs directly impair B. dothidea physiology while coinciding with Pseudomonas -dominated restructuring of the internal lesion-margin bacterial community and host barrier- and defense-associated transcriptional remodeling, with P. paracarnis aNRL1 providing a cultivable functional link to the enriched Pseudomonas signal. Video Abstract