Chromosome-level comparative genomics and host-specific fungal transcriptomics uncover adaptive virulence strategies...

Sporisorium scitamineum is the causal agent of sugarcane smut, affecting global sugarcane production. Despite advances in smut genomics, the relationships between fungal genetic diversity, host adaptation, and virulence remain elusive.

We applied chromosome-level genome sequencing (Oxford Nanopore and Illumina technologies) of two haploid strains (MAT-1 x MAT-2) per isolate and high-depth transcriptomic profiling (Illumina) during early infection (48 hpi) of a more virulent isolate (SSC04) in resistant (SP80-3280) and susceptible (IAC66-6) sugarcane genotypes.

Despite the overall genomic similarity (99.9%), we identified nine highly polymorphic genomic islands (HPIs). The most variant HPI harbors the mating-type loci, where dense sequence variation, intrachromosomal rearrangements, and inversions, potentially linked to transposable element remnants, were observed. Additionally, the genome-wide analysis revealed non-synonymous single-nucleotide variants (SNVs) in 160 genes, including those involved in vesicular trafficking and candidate-secreted effectors. Transcriptomic profiling of the more virulent isolated revealed host-dependent transcriptional reprogramming in response to immune and metabolic cues, driving distinct infection strategies: in resistant plants, the fungus upregulated genes associated with detoxification, nitrogen starvation responses, and cell wall-degrading enzymes, while in susceptible hosts, it induced genes related to hyphal growth, lipid catabolism, and the unfolded protein response. The repertoire of expressed candidate effector genes also varied according to host and isolate genotypes.

These findings uncover genomic signatures and context-dependent transcriptional regulation shaping the adaptive landscape of S. scitamineum virulence, identifying targets for pathogen monitoring and breeding for resistance.