Integrated Pangenomic and Systems Biology Analyses Reveal the Genomic Basis of Virulence and Adaptation in Bipolaris sorokiniana

Bipolaris sorokiniana is a hemibiotrophic fungal pathogen responsible for foliar and root diseases of cereals, causing annual yield losses of 10-50%. The recurrent breakdown of host resistance and the emergence of fungicide-resistant pathogen populations underscore the urgent need to understand the genomic mechanisms underpinning pathogen adaptation and virulence. Here, we present the first comprehensive species-wide pangenomic and systems-level analyses of B. sorokiniana based on 19 genomes of globally distributed strains. Orthology-based analyses revealed an open pangenome comprising 16,981 orthogroups, partitioned into a conserved core genome (60.8%) and a highly dynamic accessory genome (39.2%), consisting of soft-core (8.5%), shell (19.7%), and cloud (11.0%) compartments. The core genes were predominantly associated with essential cellular and metabolic functions, while the accessory fractions were enriched in regulatory, stress-responsive, and adaptive processes. Secondary metabolite profiling identified 39-54 biosynthetic gene clusters per genome and revealed a largely conserved metabolic repertoire. Gene family evolution analyses revealed an excess of gene loss over expansion, indicating ongoing genome streamlining and lineage-specific adaptation. The core interactome comprised four densely connected functional communities governing genome maintenance, ribosome biogenesis, cellular bioenergetics, and protein translation. Collectively, this study elevates B. sorokiniana research from single-genome analyses to a population-scale analysis, providing vital insights into the evolutionary architecture of pathogenicity, adaptation, and genome diversification. These findings provide a valuable genomic resource for disease surveillance and functional characterization of virulence determinants, as well as the development of durable resistance strategies and next-generation antifungals for sustainable disease management in cereals.