Sanctuary: A starship transposon facilitating the movement of the virulence factor ToxA in fungal wheat pathogens

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Bucknell, A., Wilson, H. M., Gonçalves Dos Santos, K. C., Simpfendorfer, S., Milgate, A., Germain, H., Solomon, P. S., Bentham, A. et McDonald, M. C. (2025). Sanctuary: A starship transposon facilitating the movement of the virulence factor ToxA in fungal wheat pathogens. mBio, 16 (10). Article e01371-25. ISSN 2161-2129 2150-7511 DOI 10.1128/mbio.01371-25

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Résumé

ABSTRACT

There is increasing evidence that mobile genetic elements can drive the emergence of pathogenic fungal species by moving virulence genes horizontally. The 14 kbp ToxhAT transposon was shown to move the necrotrophic effector, ToxA, horizontally between wheat pathogens, namely Parastagonospora nodorum, Pyrenophora tritici-repentis, and Bipolaris sorokiniana. All three species utilize the ToxA protein to infect wheat. Previous work found ToxhAT in distinct chromosomal positions in two B. sorokiniana isolates, indicating that the transposon remains active in this species. Here, we confirm the movement of ToxhAT using long-read sequencing of eight new and one previously published B. sorokiniana isolates. One event of independent transposition of ToxhAT was observed, and target site duplications of “TA” were identified, confirming that this is an active transposon in this species that likely falls into the Tc1/Mariner transposon family. We propose renaming this non-autonomous transposon to ToxTA. Whole genome analysis revealed that ToxTA is a passenger embedded in a much larger, conserved 170–196 kbp mobile genetic element. This element, termed Sanctuary, belongs to the newly described Starship transposon superfamily. This classification is based on the presence of direct repeats, empty insertion sites, a putative tyrosine recombinase gene, and other features of Starship transposons. We also show that ToxTA has been independently acquired by two different Starships, Sanctuary and Horizon, which share little to no sequence identity, outside of ToxTA. This classification makes Horizon and Sanctuary part of a growing number of Starships involved in the horizontal gene transfer of adaptive genetic material between fungal species.

IMPORTANCE
The work presented here expands our understanding of a novel group of mobile genetic elements called Starships that facilitate the horizontal exchange of numerous genes between fungal pathogens. Our analysis shows that Sanctuary and ToxTA are both active transposons within the Bipolaris sorokiniana genome. We also show that the smaller ToxTA transposon has been independently acquired by two different Starships, namely Sanctuary in B. sorokiniana and Horizon in Pyrenophora tritici-repentis and Parastagonospora nodorum. Outside of ToxTA, these two Starships share no sequence identity. The acquisition of ToxTA by two different mobile elements in three different fungal wheat pathogens demonstrates how horizontal transposon transfer is driving the evolution of virulence in these important wheat pathogens.

Type de document: Article
Mots-clés libres: Starships ToxA Horizontal gene transfer Bipolaris Transposons Long-read sequencing
Date de dépôt: 12 mars 2026 14:49
Dernière modification: 13 mars 2026 22:14
Version du document déposé: Version officielle de l'éditeur
URI: https://depot-e.uqtr.ca/id/eprint/12648

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