Insights into genomic evolution from the chromosomal and mitochondrial genomes of Ustilaginoidea virens

Ustilaginoidea virens, the causal agent of rice false smut, is an economically important filamentous fungal pathogen. A high-quality reference genome of U. virens promotes understanding of molecular mechanisms underlying its virulence and pathogenicity. Here, we report the first chromosome-level assembly of U. virens genome consisting of seven chromosomes ranging from 2.4 to 7.5 Mb. The assembly has dramatic improvements over previous assemblies, including considerably longer contigs, higher proportion of repetitive elements and more functionally annotated genes. Phylogenetic analyses revealed an extremely low intraspecific sequence divergence in U. virens. By contrast, intraspecific genome comparisons uncovered dynamic genomic alterations including massive structural variations and widespread lineage-specific regions (LSRs) among U. virens strains, which were mainly generated by recent burst of retrotransposons. Genomic plasticity created by structural variations and LSRs might drive rapid evolution of U. virens. High-quality mitochondrial genomes of eight U. virens strains exhibit size variations from 94 to 102 kb. Consistently, U. virens contains conserved lengths of exons and highly dynamic mobile introns, which contribute to intraspecific size variations due to gain/loss of homing endonuclease genes. This study highlights unique characteristics in nuclear and mitochondrial genomic divergence and provides new insights into genomic and mitochondrial evolution of U. virens.