Comparative Genomics of Sibling Fungal Pathogenic Taxa Identifies Adaptive Evolution without Divergence in Pathogenicity Genes or Genomic Structure

It has been estimated that the sister plant pathogenic fungal species Heterobasidion irregulare and Heterobasidion annosum may have been allopatrically isolated for 34–41 Myr. They are now sympatric due to the introduction of the first species from North America into Italy, where they freely hybridize. We used a comparative genomic approach to 1) confirm that the two species are distinct at the genomic level; 2) determine which gene groups have diverged the most and the least between species; 3) show that their overall genomic structures are similar, as predicted by the viability of hybrids, and identify genomic regions that instead are incongruent; and 4) test the previously formulated hypothesis that genes involved in pathogenicity may be less divergent between the two species than genes involved in saprobic decay and sporulation. Results based on the sequencing of three genomes per species identified a high level of interspecific similarity, but clearly confirmed the status of the two as distinct taxa. Genes involved in pathogenicity were more conserved between species than genes involved in saprobic growth and sporulation, corroborating at the genomic level that invasiveness may be determined by the two latter traits, as documented by field and inoculation studies. Additionally, the majority of genes under positive selection and the majority of genes bearing interspecific structural variations were involved either in transcriptional or in mitochondrial functions. This study provides genomic-level evidence that invasiveness of pathogenic microbes can be attained without the high levels of pathogenicity presumed to exist for pathogens challenging naïve hosts

Mitonuclear interactions may contribute to fitness of fungal hybrids

Abstract Hybridization between species is being recognized as a major force in the rapid adaptive evolution of fungal plant pathogens. The first stages of interspecific hybridization necessarily involve nuclear-mitochondrial chimeras. In their 2001 publication, Olson and Stenlid reported that mitochondria control the virulence of first generation hybrids between the North American fungal pathogen Heterobasidion irregulare and its congeneric H. occidentale. By assessing saprobic ability and gene expression of H. irregulare × H. annosum sensu stricto hybrids and of their parental genotypes, we demonstrate that mitochondria also influence saprobic growth of hybrids. Moreover, gene expression data suggest that fungal fitness is modulated by an intimate interplay between nuclear genes and mitochondrial type, and is dependent on the specific mitonuclear combination