Comparative genomics of Cadophora luteo-olivacea reveals a divergent lineage, conserved functional repertoires, and strain-level phenotypic variation

ABSTRACT Cadophora luteo-olivacea has been reported from different hosts and environments and is associated with grapevine trunk diseases, yet the extent to which isolates differ in genome composition, functional potential, and pathogenicity remains poorly understood. Here, we performed a comparative genomic analysis of 12 C. luteo-olivacea isolates recovered from grapevine, almond, apple, Crocus bulbs, soil, air, wastewater, and deep-sea sediment. Genome assemblies were highly complete (BUSCO >99%) and ranged from 46.94 to 50.70 Mbp. Pairwise average nucleotide identity (ANI) revealed a cohesive 11-strain group and one markedly divergent strain, CBS 266.93. Phylogenomic analysis based on 2,645 single-copy orthologs further showed that CBS 266.93 lies outside the main C. luteo-olivacea clade, with Cadophora malorum representing its closest sampled relative, indicating that its taxonomic placement warrants further investigation. Across the remaining strains, broad functional conservation was observed, including similar KOG profiles, extensive carbohydrate-active enzyme repertoires (798-849 genes per genome), and abundant biosynthetic gene clusters (26-35 per genome). Transposable element content varied substantially among strains (0.67-4.45% of genome), but this variation did not parallel overall functional profiles. All isolates induced lesions on grapevine leaves in vitro , although lesion severity differed significantly among strains, indicating quantitative variation in lesion-forming ability under controlled conditions. Exploratory small RNA profiling of inoculated grapevine leaves revealed isolate-associated differences in host miRNA family profiles, particularly involving miR398, miR827, and miR156. Together, these results show substantial genomic and functional similarity among most sampled isolates, alongside lineage- and strain-level phenotypic and host-associated variation.