Killer meiotic driver prevents chromosome loss and enhances fitness in a fungal pathogen

Fungal pathogens often carry dispensable chromosomes (DCs) that confer a selective advantage in adverse environments or during host infection but can be spontaneously lost under non-selective conditions. How DCs are maintained in evolving populations remains poorly understood. Here we show that a meiotic driver known as Spore Killer (spok), located on a giant Starship transposon, limits spontaneous loss of a conserved DC in the cross-kingdom pathogen Fusarium oxysporum. Transfer of a functional spok gene, but not of a killing-deficient mutant allele, to a mitotically unstable DC significantly reduced its loss rate, while spok deletion from a stably maintained DC increased loss frequency. Competition experiments between isogenic strains carrying a functional or a killing-deficient spok allele revealed a dramatic fitness gain conferred by Spok killing activity, which required transmission by hyphal fusion. Thus, spoks and their Starship carriers benefit fungal hosts by preventing DC loss and preserving long-term metabolic and pathogenic plasticity.