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

Background Apple ring rot, caused by the fungal pathogen Botryosphaeria dothidea , is a devastating disease affecting apple production. It causes extensive damage to fruit and branches, leading to significant economic losses within the apple industry in China and across the globe. While the volatile organic compound G1-VOC has demonstrated remarkable efficacy in suppressing B. dothidea and reducing fruit decay, its internal biocontrol mechanism and the host transcriptional response remain largely unexplored. Results This study integrated microbiome analysis, VOC-bacterial interaction studies, and transcriptome profiling to investigate the mechanism by which G1-VOCs regulates apple endophytes to suppress apple ring rot. Initially, G1 was identified for its VOC-mediated biocontrol activity. GC-MS analysis showed compounds from sesquiterpenoid, triterpenoid, and phenylalanine metabolism pathways act as primary inhibitors, disrupting fungal glycolysis, membrane integrity, and biofilm formation. 16S rRNA analysis revealed G1-VOCs prevent bacterial diversity imbalances caused by Staphylococcus during infection while maintaining microbial stability by regulating Pseudomonas abundance and recruiting the antagonistic strain Pseudomonas sp. aNRL1. Interactions between G1-VOCs and aNRL1 suggested the volatiles modulate bacterial growth kinetics, biofilm formation and motility to favour antagonistic strain. Finally, transcriptome analysis demonstrated G1 treatment reactivates the Brassinosteroid signaling pathway and upregulates genes associated with the MAPK cascade, lipid metabolism, and cuticle/wax biosynthesis during pathogen challenge. Conclusion G1-VOCs regulate microbial composition in apple endophytic tissues by enriching antagonistic strain and reprogram the apple transcriptome by upregulating defence and signalling pathways to counteract B. dothidea.