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Polyphyletic origin and horizontal exchange drive the emergence of a novel resistance-breaking Fusarium oxysporum f. sp. lactucae race

  1. 1Niab

Abstract

Fusarium oxysporum f. sp. lactucae (Fola), the cause of lettuce fusarium wilt, poses an increasing threat to global production due to the rapid emergence of resistance breaking isolates. However, the evolutionary origins and mechanisms underpinning this diversification remain poorly understood. We characterised 103 Fola isolates using molecular profiling, selecting ten key isolates for long-read whole-genome sequencing and performed in planta virulence assays for selected isolates. This included the first assemblies for Fola2 and Fola3, recent resistance-breaking variants and a highly divergent isolate from France designated as a putative novel race, FolaX. Phylogenomic analysis revealed that Fola is polyphyletic, with lettuce pathogenicity acquired independently across divergent F. oxysporum clades. Despite this, all lineages share a conserved "PanFola" effector set with near-identical sequences, indicating extensive horizontal gene transfer. Resistance-breaking Fola variants within established races were linked to copy number variations and targeted deletions, such as the loss of the SIX8/PSE1 locus in Fola4+. Conversely, FolaX possessed a divergent core genome and a chimeric accessory genome derived from multiple Fola lineages via segmental chromosome transfer and transposon-mediated reshuffling. Our findings highlight the remarkable evolutionary plasticity of Fola and the need for breeding strategies that address the dynamic nature of effector repertoires.

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BibTeX
@misc{price2026polyphyletic,
  title = {{Polyphyletic origin and horizontal exchange drive the emergence of a novel resistance-breaking Fusarium oxysporum f. sp. lactucae race}},
  author = {R. J. Price and E. van Brabant and H. Bates and H. Mestdagh and S. Jenkins and E. Vines and M. Hofte and J. Clarkson},
  howpublished = {bioRxiv},
  year = {2026},
  month = sep,
  doi = {10.64898/2026.09.30.755575},
  url = {https://www.biorxiv.org/content/10.64898/2026.09.30.755575v1},
  note = {CC BY},
}
RIS
TY  - UNPB
TI  - Polyphyletic origin and horizontal exchange drive the emergence of a novel resistance-breaking Fusarium oxysporum f. sp. lactucae race
AU  - R. J. Price
AU  - E. van Brabant
AU  - H. Bates
AU  - H. Mestdagh
AU  - S. Jenkins
AU  - E. Vines
AU  - M. Hofte
AU  - J. Clarkson
PY  - 2026
DA  - 2026/09/30
PB  - bioRxiv
DO  - 10.64898/2026.09.30.755575
UR  - https://www.biorxiv.org/content/10.64898/2026.09.30.755575v1
AB  - Fusarium oxysporum f. sp. lactucae (Fola), the cause of lettuce fusarium wilt, poses an increasing threat to global production due to the rapid emergence of resistance breaking isolates. However, the evolutionary origins and mechanisms underpinning this diversification remain poorly understood. We characterised 103 Fola isolates using molecular profiling, selecting ten key isolates for long-read whole-genome sequencing and performed in planta virulence assays for selected isolates. This included the first assemblies for Fola2 and Fola3, recent resistance-breaking variants and a highly divergent isolate from France designated as a putative novel race, FolaX. Phylogenomic analysis revealed that Fola is polyphyletic, with lettuce pathogenicity acquired independently across divergent F. oxysporum clades. Despite this, all lineages share a conserved "PanFola" effector set with near-identical sequences, indicating extensive horizontal gene transfer. Resistance-breaking Fola variants within established races were linked to copy number variations and targeted deletions, such as the loss of the SIX8/PSE1 locus in Fola4+. Conversely, FolaX possessed a divergent core genome and a chimeric accessory genome derived from multiple Fola lineages via segmental chromosome transfer and transposon-mediated reshuffling. Our findings highlight the remarkable evolutionary plasticity of Fola and the need for breeding strategies that address the dynamic nature of effector repertoires.
ER  -