Starship giant transposons dominate plastic genomic regions in a fungal plant pathogen and drive virulence evolution

Starships form a recently discovered superfamily of giant transposons in Pezizomycotina fungi, implicated in mediating horizontal transfer of diverse cargo genes between fungal genomes. Their elusive nature has long obscured their significance, and their impact on genome evolution remains poorly understood. Here, we reveal a surprising abundance and diversity of Starships in the phytopathogenic fungus Verticillium dahliae. Remarkably, Starships dominate the plastic genomic compartments involved in host colonization, are enriched in virulence-associated genes, and exhibit genetic and epigenetic characteristics associated with adaptive genome evolution. We further uncover extensive horizontal transfer of Starships between Verticillium species and, strikingly, from distantly related Fusarium fungi. Finally, we demonstrate how Starship activity facilitated the de novo formation of a novel virulence gene. Our findings illuminate the profound influence of Starship dynamics on fungal genome evolution and the development of virulence.星舰（Starships）是近期在子囊菌亚门（Pezizomycotina）真菌中发现的一类巨型转座子超家族，被认为可介导真菌基因组间多种负载基因的水平转移。其隐秘的存在特性长期以来掩盖了其生物学意义，目前学界对其在基因组进化中发挥的影响仍知之甚少。本研究揭示了植物病原真菌大丽轮枝菌（Verticillium dahliae）中星舰惊人的丰度与多样性。值得注意的是，星舰主导了参与宿主定殖的可塑性基因组区段，显著富集于致病相关基因，且展现出与适应性基因组进化相关的遗传与表观遗传特征。我们进一步揭示了星舰在轮枝菌属（Verticillium）物种间的广泛水平转移，尤为惊人的是，还发现了星舰从亲缘关系较远的镰孢菌属（Fusarium）真菌中的跨属水平转移。最后，我们证实星舰的活性可促成全新致病基因的从头（de novo）形成。本研究结果阐明了星舰动态对真菌基因组进化与致病力发育的深远影响。