Horizontal transfers between fungalFusariumspecies contributed to successive outbreaks of coffee wilt disease

Abstract

Outbreaks of fungal disease have devastated plants and animals throughout history. Over the past century, the repeated emergence of coffee wilt disease caused by the fungal pathogenFusarium xylarioidesseverely impacted coffee production across sub-Saharan Africa. To improve the disease management of such pathogens, it is crucial to understand their genetic structure and evolutionary potential. We compared the genomes of 13 historic strains spanning six decades and multiple disease outbreaks to investigate population structure and host specialisation. We foundF. xylarioidescomprises at least four distinct lineages: one host-specific toCoffea arabica, one toC. canephoravar.robusta, and two historic lineages isolated from variousCoffeaspecies. Mapping variation onto a new long-read reference genome showed that host-specificity appears to be acquired through horizontal transfer of effector genes from members of theF. oxysporumspecies complex. This species complex is known to cause wilt disease in over 100 plant species. Multiple transfers into theF. xylarioidespopulations matched to different parts of theF. oxysporummobile pathogenicity chromosome and were enriched in effector genes and transposons. Effector genes in this region and other horizontally transferred carbohydrate-active enzymes important in the breakdown of plant cell walls were shown by transcriptomics to be highly expressed during infection ofC. arabicaby the fungal arabica strains. Widespread sharing of specific transposons betweenF. xylarioidesandF. oxysporum, and the presence of largeStarshipelements, indicate that transposons were involved in horizontal transfers. Our results support the hypothesis that horizontal gene transfers contributed to the repeated emergence of this fungal disease.

HarbouringStarships: The accumulation of large Horizontal Gene Transfers in Domesticated and Pathogenic Fungi

“…Notably, these cargo genes have already been linked to, sometimes retroactively, resistance to formaldehyde (Urquhart, Gluck-Thaler, et al, 2023), heavy metals (Urquhart et al, 2022;, adaptation to food production (Cheeseman et al, 2014;Lo et al, 2023;Ropars et al, 2015) and plant pathogenicity (A. Bucknell et al, 2024;Gourlie et al, 2022;Peck et al, 2023), suggesting that Starships and their associated cargo may facilitate rapid adaptation to challenging environments (A. H. Bucknell & McDonald, 2023). This may be particularly relevant to both newly emerging (Seyedmousavi et al, 2018) and treatment resistant pathogens (Rivelli Zea & Toyotome, 2022) within the Aspergillus genus.…”