On the evolution of Pyrenophora tritici-repentis
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Date
2025
Authors
Gourlie, Ryan A. R.
University of Lethbridge. Faculty of Arts and Science
Journal Title
Journal ISSN
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Publisher
Lethbridge, Alta. : University of Lethbridge, Dept. of Biological Sciences
Abstract
Pyrenophora tritici-repentis (Ptr) is a globally distributed and economically important plant pathogen causing tan spot, a destructive foliar disease of wheat. The relatively recent emergence of Ptr provides a unique opportunity to better understand how necrotrophic pathogens evolve in modern agricultural systems. In this thesis, a variety of genomic and bioinformatic techniques were employed to examine the genomes of a large set of geographically diverse isolates with representatives from all of the established virulence races. These races contain different combinations of Ptrs three primary necrotrophic effectors: ToxA, ToxB, and ToxC. Comparison of total gene content between isolates found that Ptr possesses an open-pangenome, with a high accessory gene content (57%), and significant differences between pathogenic and non-pathogenic races. Putative effectors were found to be primarily accessory in nature, while carbohydrate-active enzymes associated with plant cell wall degradation were conserved. Gene distances and evolutionary rates suggest that the genomic architecture of Ptr is that of a ‘one-compartment’ genome despite having a high proportion of transposable elements (~18 to 25% of the genome). Significant chromosomal rearrangements were observed between isolates including the translocation of ToxA and the presence of ToxB within an accessory region. The translocation of ToxA, along with a 143 kbp region, was facilitated by the Starship transposon Horizon. Within Horizon, was nested the ToxhAT transposon which was responsible for the horizontal transfer of ToxA into Ptr. The accessory region which contains ToxB contained several Starship cargo genes but lacked other defining Starship characteristics, namely the requisite tyrosine recombinase. This region may be an accessory chromosomal arm, an ancient derelict Starship, or the beginning of genome compartmentalization. Detailed examination and extensive manual alignments between ToxB containing isolates revealed the presence of a Helitron-like transposable element, ToxB-HLE, which is replicating the ToxB gene in some isolates. Furthermore, two independent Copia retrotransposon insertions were found to be responsible for the disruption of ToxB thereby creating two of the known inactive toxb haplotypes. Finally, a genome wide association study revealed single-nucleotide polymorphisms significantly associated with the ToxC phenotype (-log(p) = 5.5). The nature of ToxC is unknown, and this analysis provides a number of candidate genes which may be involved in ToxC biosynthesis, secretion, or regulation. This body of work represents one of the most extensive examinations of the Ptr genome and its necrotrophic effectors preformed to-date and has shown that the pathogen exhibits high genome plasticity through not only through rearrangements but gene gains and losses as well. It also shows that transposons play a significant role in the evolution and adaptability of this global plant pathogen by mobilizing, replicating, and disrupting virulence genes.
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Keywords
Plant pathology , Fungal genomics , Transposons , Evolution , Necrotrophic effectors , Bioinformatics , Comparative genomics