Whole-genome analysis uncovers four novel Streptomyces species linked to sweet potato soil rot in China.

UNLABELLED: Sweet potato soil rot, caused by pathogenic Streptomyces, is an emerging threat to sweet potato production in China. However, the diversity and pathogenic mechanisms of the associated species remain poorly understood. In this study, symptomatic storage roots exhibiting typical pox-like lesions were collected from major production regions in Henan and Guangdong provinces. A total of 225 actinomycete strains were isolated using optimized methods, and six highly pathogenic strains were identified through tuber slice, hydroponic, and pot inoculation assays. Morphological, physiological, whole-genome sequencing, and phylogenetic analyses revealed considerable diversity among these pathogenic isolates. Average nucleotide identity (ANI) analysis showed that strain (ST10) was closely related to Streptomyces albogriseolus, whereas the remaining strains displayed substantial genomic divergence, indicating diverse taxonomic affiliations. Comparative genomic analysis identified a conserved core genome together with extensive strain-specific gene content, reflecting both functional conservation and adaptive evolution. Phylogenomic analysis placed several isolates close to S. ipomoeae, and others within distinct pathogenic lineages. Notably, none of the six strains possessed the canonical thaxtomin biosynthetic gene cluster, suggesting that pathogenicity is mediated by alternative virulence mechanisms. Instead, conserved gene clusters associated with siderophores and stress-related metabolites were identified, indicating potential roles in host colonization and ecological adaptation. These findings expand our understanding of the genomic diversity and potential pathogenic mechanisms of sweet potato-associated Streptomyces and provide a valuable foundation for disease management and resistance breeding.

IMPORTANCE: Herein, we established an optimized isolation method yielding 225 actinomycete strains and a rapid pipeline for pathogenic identification of sweet potato-associated Streptomyces. Six isolates were confirmed as causal agents of sweet potato soil rot, including four novel species. Complete genome sequences of five strains provide a fundamental resource for elucidating pathogenesis mechanisms and advancing taxonomic and evolutionary studies of the genus. The absence of canonical thaxtomin biosynthetic genes across all pathogenic strains, combined with the presence of conserved siderophore and stress-related metabolite clusters, demonstrates that these pathogens utilize alternative virulence mechanisms distinct from well-characterized Streptomyces plant pathogens. Comparative genomics reveals a conserved core genome alongside strain-specific gene content, reflecting functional conservation and adaptive evolution. These genomic resources and experimental validations establish a foundational framework for understanding pathogen diversity, enabling accurate diagnosis of emerging strains and directly informing resistance breeding programs by identifying genetic targets for screening sweet potato germplasm.