Gene loss dynamics and T3PKS conservation shape the evolution and pathogenicity of Rosellinia necatrix

ABSTRACT Fungal pathogens exhibit remarkable genome plasticity, driven by polyploidy, genome duplication, transposable elements, and niche adaptation. Gene losses often occur in dispensable regions, including in the remarkably dynamic secondary metabolite gene clusters (SMGCs). Within the diverse family Xylariaceae, comprising endophytes, saprotrophs, and phytopathogens, the broad-spectrum pathogen Rosellinia necatrix is of major concern, causing white root rot in numerous crops worldwide. Its strategy involves the root infection of weakened plants, tissue colonization, and saprotrophic survival in soil; yet, the genetic basis of this versatility remains poorly understood. Herein, we applied comparative genomics across Xylariaceae to investigate the molecular determinants of R. necatrix pathogenicity. We uncovered widespread gene losses in R. necatrix , particularly in SMGCs, candidate effectors, and transporter families (MFS and ABC transporters), suggesting a streamlining of its metabolic repertoire during adaptation to diverse hosts. We also identified two highly conserved type III polyketide synthases (T3PKS) across the family, predicted to encode chalcone synthases. Structural modeling and docking analyses support their role in chalcone-related biosynthesis, pointing to an unexpected link between fungal metabolism and plant-associated compounds. Variation in SMGC and carbohydrate-active enzyme (CAZy) repertoires across Xylariaceae further suggests a hemibiotrophic potential for R. necatrix , reconciling its capacity for both latent colonization and aggressive necrosis. Our findings establish niche specificity as a key driver of genome reduction in R. necatrix and reveal conserved metabolic innovations across Xylariaceae. By integrating gene loss dynamics with secondary metabolism, this work provides new insights into fungal adaptation and pathogenicity, with implications for disease management in perennial and annual crops.