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Evolution of the ToxB gene in Pyrenophora tritici-repentis and related species

    Authors and Affiliations
    • Dr. Mohamed Hafez, Lethbridge, Canada; [email protected]
    • Mr. Ryan Gourlie, Lethbridge, Canada; [email protected]
    • Dr. Megan McDonald, University of Birmingham, Birmingham, United Kingdom of Great Britain and Northern Ireland; [email protected]
    • Ms. Melissa Telfer, Lethbridge, Canada; [email protected]
    • Dr. Marcelo Carmona, Buenos Aires, Argentina; [email protected]
    • Mr. Francisco Sautua, Buenos Aires, Argentina; [email protected]
    • Dr. Caroline Moffat, Curtin University, 1649, Centre for Crop and Disease Management, Molecular and Life Sciences, Curtin University, Kent St, Bentley, Western Australia, Australia, 6102, Curtin University; [email protected]
    • Dr. Paula Moolhuijzen, Curtin University Bentley Campus, 1649, Science and Engineering, Kent st, Bentley, Perth, Western Australia, Australia, 6845; [email protected]
    • Dr. Pao Theen See, Curtin University, 1649, Centre for Crop and Disease Management, School of Molecular and Life Sciences, Perth, Western Australia, Australia; [email protected]
    • Dr. Reem Aboukhaddour, Agriculture and Agri-Food Canada, 6337, 4503 1 ave South, Lethbridge, Alberta, Canada, T1J4B1; [email protected]

      Published Online:

      Pyrenophora tritici-repentis is a destructive pathogen of wheat with global impact. It possesses a highly plastic open pangenome shaped by the gain and loss of effector genes. This study investigated the allelic variations in the chlorosis-encoding gene, ToxB, across 422 isolates representing all identified pathotypes and worldwide origins. To gain better insights into ToxB evolution, we examined its presence and variability in other Pyrenophora spp. A ToxB haplotype network was constructed, revealing the evolutionary relationships of this gene (20 haplotypes) across four Pyrenophora species. Notably, toxb, the homolog of ToxB, was detected for the first time in the barley pathogen Pyrenophora teres. The ToxB/toxb genes display evidence of selection that is characterized by loss of function, duplication, and diverse mutations. Among ToxB/toxb open reading frame, 72 mutations were identified, including 14 synonymous, 55 nonsynonymous, and 3 indel mutations. Remarkably, a ~5.6 Kb Copia-like retrotransposon, named Copia-1_Ptr, was found inserted in the toxb gene of a race 3 isolate. This insert disrupted the ToxB gene’s function, a first case of effector gene disruption by a transposable element in Ptr. Additionally, a microsatellite with 25-nucleotide repeats (0 to 10) in the upstream region of ToxB suggested a potential mechanism influencing ToxB expression and regulation. Exploring ToxB-like protein distribution in other Ascomycetes revealed their presence in 19 additional species, including the Leotiomycetes class for the first time. The presence/absence pattern of ToxB-like proteins defied species relatedness compared to a phylogenetic tree, suggesting a past horizontal gene transfer event.