Kinome expansion in the Fusarium oxysporum species complex driven by accessary chromosomes

Abstract

The Fusarium oxysporum species complex (FOSC) is a group of soil-borne pathogens causing severe disease in over one hundred plant hosts, while individual strains exhibit strong host specificity. Both chromosome transfer and comparative genomics experiments have demonstrated that lineage-specific (LS) chromosomes contribute to the host specific pathogenicity. However, little is known about the functional importance of genes encoded in these LS chromosomes. Focusing on signaling transduction, this study compared kinomes of 12 F. oxysporum isolates, including both plant and human pathogens and one non-pathogenic biocontrol strain, with seven additional publicly available ascomycete genomes. Overall, F. oxysporum kinomes are the largest, facilitated in part by the acquisitions of the LS chromosomes. The comparative study identified 99 kinases that are present in almost all examined fungal genomes, forming the core signaling network of ascomycete fungi. Compared to the conserved ascomycete kinome, the expansion of the F. oxysporum kinome occurs in several kinases families such as Histidine kinases that are involved in environmental signal sensing and TOR kinase that mediates cellular responses. Comparative kinome analysis suggests a convergent evolution that shapes individual F. oxysporum isolates with an enhanced and unique capacity for environmental perception and associated downstream responses.\n\nIMPORTANCEIsolates of F. oxysporum are adapted to survive a wide range of host and non-host conditions. In addition, F. oxysporum was recently recognized as the top emerging opportunistic fungal pathogen infecting immunocompromised humans. The sensory and response networks of these fungi undoubtedly play a fundamental role in establishing the adaptability of this group. We have examined the kinomes of 12 F. oxysporum isolates and highlighted kinase families that distinguish F. oxysporum from other fungi, as well as different isolates from one another. The amplification of kinases involved in environmental signal relay and regulating downstream cellular responses clearly sets Fusarium apart from other Ascomycetes. Though the function of many of these kinases is still unclear, their specific proliferation highlights them as a result of the evolutionary forces which have shaped this species complex, and clearly marks them as targets for exploitation in order to combat disease.