Comparative Genomics of a Plant-Pathogenic Fungus,Pyrenophora tritici-repentis, Reveals Transduplication and the Impact of Repeat Elements on Pathogenicity and Population Divergence

Abstract

Pyrenophora tritici-repentis is a necrotrophic fungus causal to the disease tan spot of wheat, whose contribution to crop loss has increased significantly during the last few decades. Pathogenicity by this fungus is attributed to the production of host-selective toxins (HST), which are recognized by their host in a genotype-specific manner. To better understand the mechanisms that have led to the increase in disease incidence related to this pathogen, we sequenced the genomes of three P. tritici-repentis isolates. A pathogenic isolate that produces two known HSTs was used to assemble a reference nuclear genome of approximately 40 Mb composed of 11 chromosomes that encode 12,141 predicted genes. Comparison of the reference genome with those of a pathogenic isolate that produces a third HST, and a nonpathogenic isolate, showed the nonpathogen genome to be more diverged than those of the two pathogens. Examination of gene-coding regions has provided candidate pathogen-specific proteins and revealed gene families that may play a role in a necrotrophic lifestyle. Analysis of transposable elements suggests that their presence in the genome of pathogenic isolates contributes to the creation of novel genes, effector diversification, possible horizontal gene transfer events, identified copy number variation, and the first example of transduplication by DNA transposable elements in fungi. Overall, comparative analysis of these genomes provides evidence that pathogenicity in this species arose through an influx of transposable elements, which created a genetically flexible landscape that can easily respond to environmental changes.

Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts

“…The Bgh isolates differing in avirulence gene combinations that were resequenced in this study permitted us to examine polymorphisms between CSEP orthologs. The massive proliferation of repetitive elements in the genome of the Bgh isolate DH14, accounting for ∼64% of the fungal genome (15,27), suggests that CSEP arsenals could have been impacted by the activity of these elements as recently demonstrated by resequencing of three isolates of Pyrenophora tritici-repentis, a necrotrophic fungus responsible for tan spot disease of wheat (42). Consistent with this, the flanking regions of most of the Bgh isolatespecific CSEPs show similarity to repeat sequences.…”

A Novel Type Pathway-Specific Regulator and Dynamic Genome Environments of a Solanapyrone Biosynthesis Gene Cluster in the Fungus Ascochyta rabiei

“…TEs can be broadly categorized into two major groups, retrotransposons and DNA transposons (31). Although the majority of TEs in the genomes of the fungal class Dothideomycetes are retrotransposons, members of the Tc1/Mariner superfamily of DNA transposons are frequently found in certain members of the fungal class (32)(33)(34). The Tc1/Mariner-type TEs are highly variable in size but are generally delimited by terminal inverted repeats and encode a single transposase (35).…”

Conservation of the genes for HC-toxin biosynthesis in Alternaria jesenskae

“…A predicted alpha subunit gene, called TOXH , is clustered with the other genes of TOX2 in C. carbonum but has not yet been functionally characterized (unpublished results from this lab; GenBank accession KC866372). The apicidin cluster of F. incarnatum and the hypothetical HC-toxin clusters of P. tritici-repentis and S. turcica (see Discussion) contain an alpha subunit gene, but, inexplicably, the clusters in neither of these two fungi, nor in F. incarnatum , which makes apicidin, contain a ortholog of TOXC [14,21,22]. …”

“…[39-41]. However, this scenario struggles to explain why secondary metabolite genes appear to have a different evolutionary trajectory than genes for primary metabolism, i.e., to what extent there are positively selected genetic mechanisms that promote diversity in secondary metabolite capacity at the expense of stability, such as transposable elements, sub-telomeric instability, and chromosomal translocations [10,22]. …”