Discovery of a New Starship Transposon Driving the Horizontal Transfer of the <i>ToxA</i> Virulence Gene in <i>Alternaria ventricosa</i>

The virulence gene <i>ToxA</i> has been proposed to be horizontally transferred between three fungal wheat pathogens (<i>Parastagonospora nodorum</i>, <i>Pyrenophora tritici-repentis</i>, and <i>Bipolaris sorokiniana</i>) as part of a conserved ~14 kb...

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Main Authors: Fei Liu, Ratchadawan Cheewangkoon, Rui-Lin Zhao
Format: Article
Language:English
Published: MDPI AG 2025-02-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/13/2/376
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Summary:The virulence gene <i>ToxA</i> has been proposed to be horizontally transferred between three fungal wheat pathogens (<i>Parastagonospora nodorum</i>, <i>Pyrenophora tritici-repentis</i>, and <i>Bipolaris sorokiniana</i>) as part of a conserved ~14 kb <i>ToxhAT</i> transposon. Here, our analysis of 2137 fungal species-representative assemblies revealed that the <i>ToxA</i> gene is an isolate of <i>Alternaria ventricosa</i> and shows a remarkable 99.5% similarity to those found in <i>B. sorokiniana</i> and <i>P. tritici-repentis.</i> Analysis of the regions flanking <i>ToxA</i> within <i>A. ventricosa</i> revealed that it was embedded within a 14 kb genomic element nearly identical to the corresponding <i>ToxhAT</i> regions in <i>B. sorokiniana</i>, <i>P. nodorum</i>, and <i>P. tritici-repentis</i>. Comparative analysis further showed that <i>ToxhAT</i> in <i>A. ventricosa</i> resides within a larger mobile genetic element, which we identified as a member of the Starship transposon superfamily, named <i>Frontier</i>. Our analysis demonstrated that <i>ToxhAT</i> has been independently captured by three distinct Starships—<i>Frontier</i>, <i>Sanctuary</i>, and <i>Horizon</i>—which, despite having minimal sequence similarity outside of <i>ToxhAT</i>, facilitate its mobilization. These findings place <i>Frontier</i>, <i>Sanctuary</i>, and <i>Horizon</i> within a growing class of Starships implicated in the horizontal transfer of adaptive genes among fungal species. Moreover, we identified three distinct HGT events involving <i>ToxA</i> across these four fungal species, reinforcing the hypothesis of a single evolutionary origin for the <i>ToxhAT</i> transposon. These findings underscore the pivotal role of transposon-mediated HGT in the adaptive evolution of eukaryotic pathogens, offering new insights into how transposons facilitate genetic exchange and shape host–pathogen interactions in fungi.
ISSN:2076-2607