Abstract
BackgroundNearly 50% of crop yields are lost to pests and disease, with plants and pathogens locked in an amplified co-evolutionary process of disease outbreaks. Coffee wilt disease, caused by Fusarium xylarioides, decimated coffee production in west and central Africa following its initial outbreak in the 1920s. After successful management, it later re-emerged and by the 2000s comprised two separate epidemics on arabica coffee in Ethiopia and robusta coffee in east and central Africa.ResultsHere, we use genome sequencing of six historical culture collection strains spanning 52 years to identify the evolutionary processes behind these repeated outbreaks. Phylogenomic reconstruction using 13,782 single copy orthologs shows that the robusta population arose from the initial outbreak, whilst the arabica population is a divergent sister clade to the other strains. A screen for putative effector genes involved in pathogenesis shows that the populations have diverged in gene content and sequence mainly by vertical processes within lineages. However, 15 putative effector genes show evidence of horizontal acquisition, with close homology to genes from F. oxysporum. Most occupy small regions of homology within wider scaffolds, whereas a cluster of four genes occupy a 20Kb scaffold with strong homology to a region on a mobile pathogenicity chromosome in F. oxysporum that houses known effector genes. Lacking a match to the whole mobile chromosome, we nonetheless found close associations with DNA transposons, especially the miniature impala type previously proposed to facilitate horizontal transfer of pathogenicity genes in F. oxysporum. These findings support a working hypothesis that the arabica and robusta populations partly acquired distinct effector genes via transposition-mediated horizontal transfer from F. oxysporum, which shares coffee as a host and lives on other plants intercropped with coffee.ConclusionOur results show how historical genomics can help reveal mechanisms that allow fungal pathogens to keep pace with our efforts to resist them. Our list of putative effector genes identifies possible future targets for fungal control. In turn, knowledge of horizontal transfer mechanisms and putative donor taxa might help to design future intercropping strategies that minimize the risk of transfer of effector genes between closely-related Fusarium taxa.
Highlights
50% of crop yields are lost to pests and disease, with plants and pathogens locked in an amplified co-evolutionary process of disease outbreaks
Representative whole-genome alignments revealed the presence of the 11 syntenic core chromosomes shared by F. verticillioides, F. oxysporum and more distantly-related Fusarium taxa [9] in F. xylarioides (Figures S2 and S3), and the additional genomic material compared with F. verticillioides (Figure S3)
We classified these unaligned scaffolds based on their presence and absence across other Fusarium fujikuroi Complex (FFC) species: those which are absent from F. verticillioides but which are present in F. udum and the historic Coffea659 strain are labelled “FXU” (F. xylarioides and -udum specific); those which are absent from F. verticillioides and F. udum and are shared with Coffea659 are labelled “FXS” (F. xylarioides-specific); and those which are not shared with Coffea659 and are unique to each F. xylarioides strain are labelled “LS”
Summary
50% of crop yields are lost to pests and disease, with plants and pathogens locked in an amplified co-evolutionary process of disease outbreaks. Largescale planting of crops generates strong selection for new pathogens to emerge, which leads to further rounds of plant breeding to develop new resistant genotypes. This leads to “boom and bust cycles” that intensify the natural co-evolutionary dynamics of hosts and pathogens. An emerging pathogen can evolve new mechanisms to suppress and overwhelm basal plant defences. These could arise by mutation (including gene duplication or loss), recombination and selection operating within a single population, or from hybridization and/or horizontal gene transfer between species to generate new pathogenicity variants [5, 6]. Fusarium oxysporum’s well-studied host-specific formae speciales (f. sp.) cause disease on over 120 plant species, including Panama disease of bananas, F. oxysporum f. sp. cubense [7]
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