ToxA is present in the U.S. Bipolaris sorokiniana population and is a significant virulence factor on wheat harboring Tsn1

Authors: Friesen, Timothy; Holmes, Danielle; Bowden, Robert; Faris, Justin

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/16/2018
Publication Date: 12/1/2018
Citation: Friesen, T.L., Holmes, D.J., Bowden, R.L., Faris, J.D. 2018. ToxA is present in the U.S. Bipolaris sorokiniana population and is a significant virulence factor on wheat harboring Tsn1. Plant Disease. 102(12):2446-2452. Plant Dis. 102:2446-2452.
DOI: https://doi.org/10.1094/PDIS-03-18-0521-RE

Interpretive Summary: ToxA is a protein that has been shown to be used by at least three wheat pathogens to cause plant cell death, negatively affecting wheat yield and quality throughout the world. The ToxA gene was recently identified for the first time in the spot blotch fungus Bipolaris sorokiniana in Australia. Here we show that the ToxA gene is also present in the B. sorokiniana population in the winter wheat region of southcentral Texas. Leaves from ‘Duster’ wheat showing high levels of disease were collected in Castroville, TX. More than 85% of the isolates collected harbored the BsToxA gene and secreted ToxA in culture. Disease evaluations of one of these ToxA-producing isolates showed that sensitivity to ToxA accounted for 24.4% of the disease in a winter wheat population, showing that the pathogen causing spot blotch on wheat is using ToxA as a virulence factor to infect wheat. Sensitivity to ToxA is prevalent in popular hard winter wheat cultivars in the central and southcentral winter wheat regions of the US including Kansas, Oklahoma and Texas, showing the potential of a selective advantage for B. sorokiniana isolates that harbor the ToxA gene.

Technical Abstract: ToxA, a necrotrophic effector originally identified from the tan spot fungus Pyrenophora tritici-repentis in 1987, was subsequently identified from Parastagonospora nodorum in 2006. More recently, the ToxA gene was identified in the spot blotch fungus Bipolaris sorokiniana in Australia. Here we show that the ToxA gene is also present in the B. sorokiniana population in the winter wheat region of southcentral Texas. Leaves from ‘Duster’ wheat showing strong necrotic lesions were collected in Castroville, TX. Fifteen single-spore isolates were collected from separate lesions and thirteen of them harbored the BsToxA gene and secreted ToxA in culture based on sensitivity of BG261, the differential line containing the dominant ToxA sensitivity gene, Tsn1. Four harboring BsToxA and one deficient in BsToxA were used to infiltrate two wheat lines harboring Tsn1 as well as their corresponding tsn1 mutant lines. Culture filtrates of the isolate lacking BsToxA did not induce necrosis on any of the lines. Culture filtrates of the four BsToxA-containing isolates induced necrosis on the wild type (Tsn1) lines but not on the corresponding tsn1 mutant lines. Sensitivity to these culture filtrates also mapped to the previously identified location for Tsn1 in the winter wheat mapping population Arina × Forno. Inoculation of one of these ToxA-producing isolates on the same population showed that the Tsn1 locus accounted for 24.4% of the disease variation. All thirteen isolates harbored the same BsToxA nucleotide sequence, which was identical to one of the two haplotypes previously identified in Australia. Sensitivity to ToxA is prevalent in popular hard winter wheat cultivars in the central and southcentral winter wheat regions of the US, showing the potential of a selective advantage for B. sorokiniana isolates that harbor the ToxA gene.