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

Abstract

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.

Characterization of Heterobasidion occidentale transcriptomes reveals candidate genes and DNA polymorphisms for virulence variations

“…Following a Blast search of available genome sequences of four H. annosum genotypes and four H. irregulare genotypes, CYP5348Z1 was not detected in these two Heterobasidion species. Other CYP5032 members were found in the genomes of a few other fungal species and Hoc‐contig91 was clustered with those predicted from genomes of H. annosum (Sillo et al ., ) and Gloeophyllum trabeum (Floudas et al ., ) (Fig. S4).…”

“…The phylogenomic relationship among Heterobasidion species and isolates/genotypes was determined by phylogenomic analysis using REALPHY (Bertels et al ., ). Raw reads of two H. occidentale isolates, and six genotypes of H. irregulare and H. annosum (Sillo et al ., ), were included for read mapping to a reference that was the coding sequences of the H. irregulare ‐TC32‐1 proteome (Olson et al ., ). As integrated in REALPHY, Bowtie2 (Langmead et al ., ) was used for read mapping; and PhyML (Guindon et al ., ) was used for construction of a phylogenetic tree using the maximum‐likelihood method by bootstrapping with 1000 repeats.…”

“…With the development of next-generation sequencing (NGS), genomes of H. irregulare and H. annosum were sequenced Sillo et al, 2015;Choi et al, 2017). Investigation of the molecular mechanisms underlying fungal penetration and proliferation in the hostile microenvironment of tree tissues implied that enzymatic degradation and efficient efflux mechanisms contribute to pathogenicity, enabling H. irregulare to overcome host chemical defence .…”

“…Investigation of the molecular mechanisms underlying fungal penetration and proliferation in the hostile microenvironment of tree tissues implied that enzymatic degradation and efficient efflux mechanisms contribute to pathogenicity, enabling H. irregulare to overcome host chemical defence . Comparative genomic study of H. irregulare and H. annosum genotypes revealed that pathogenicity-related genes were more conserved between species than genes involved in saprobic growth and sporulation (Sillo et al, 2015). As these genome sequences became available, several recent studies reported on more detailed characterization of ABC transporters, CAZyes, cytochrome P450 proteins (CYPome) and candidate effectors in H. irregulare (Yakovlev et al, 2012;Chen et al, 2015;Kuo et al, 2015;Lund en et al, 2015;Baral et al, 2016;Mgbeahuruike et al, 2017;Raffaello and Asiegbu, 2017).…”

A nonnative and a native fungal plant pathogen similarly stimulate ectomycorrhizal development but are perceived differently by a fungal symbiont

“…Dutch elm disease, chestnut blight, ash dieback, and the mortality of stone pine trees are just a few examples of tree diseases caused by invasive fungal pathogens (Anderson et al ., ; Gonthier et al ., ; Liebhold et al ., ; Gross et al ., ). Although the invasion of fungal plant pathogens may be driven by ecological factors affecting transmission potential (Garbelotto et al ., ; Giordano et al ., ; Sillo et al ., ), disease outbreaks caused by introduced pathogens have often been attributed to a disproportional pathogenicity of the pathogens on naïve hosts (Oliva et al ., ), consistent with the lack of coevolution hypothesis (Parker & Gilbert, ).…”