The mitotic exit mediated by small GTPase Tem1 is essential for the pathogenicity of Fusarium graminearum.

The mitotic exit is a key step in cell cycle, but the mechanism of mitotic exit network in the wheat head blight fungus Fusarium graminearum remains unclear. F. graminearum infects wheat spikelets and colonizes the entire head by growing through the rachis node at the bottom of each spikelet. In this study, we found that a small GTPase FgTem1 plays an important role in F. graminearum pathogenicity and functions in regulating the formation of infection structures and invasive hyphal growth on wheat spikelets and wheat coleoptiles, but plays only little roles in vegetative growth and conidiation of the phytopathogen. FgTem1 localizes to both the inner nuclear periphery and the spindle pole bodies, and negatively regulates mitotic exit in F. graminearum. Furthermore, the regulatory mechanisms of FgTem1 have been further investigated by high-throughput co-immunoprecipitation and genetic strategies. The septins FgCdc10 and FgCdc11 were demonstrated to interact with the dominant negative form of FgTem1, and FgCdc11 was found to regulate the localization of FgTem1. The cell cycle arrest protein FgBub2-FgBfa1 complex was shown to act as the GTPase-activating protein (GAP) for FgTem1. We further demonstrated that a direct interaction exists between FgBub2 and FgBfa1 which crucially promotes conidiation, pathogenicity and DON production, and negatively regulates septum formation and nuclear division in F. graminearum. Deletions of FgBUB2 and FgBFA1 genes caused fewer perithecia and immature asci formations, and dramatically down-regulated trichothecene biosynthesis (TRI) gene expressions. Double deletion of FgBUB2/FgBFA1 genes showed that FgBUB2 and FgBFA1 have little functional redundancy in F. graminearum. In summary, we systemically demonstrated that FgTem1 and its GAP FgBub2-FgBfa1 complex are required for fungal development and pathogenicity in F. graminearum. Author summary: Cell cycle is controlled by numerous mechanisms ensuring correct cell division. One fundamental question in the cell cycle is the mitotic exit and entry into the next cycle, but the mechanism of mitotic exit network in the wheat head blight fungus Fusarium graminearum remains unclear. In this study, we identified a small GTPase FgTem1 to be involved in mitotic exit in this fungus and demonstrated that this protein is required for the fungal pathogenicity and functions in regulating the infection structures formation and invasive hyphal growth on wheat spikelets and wheat coleoptiles. Furthermore, the regulatory mechanisms of FgTem1 have been further investigated. To the best of our knowledge, this work is the most comprehensive genetic dissection of Tem1 in filamentous fungal pathogens. Our results unveil a key link between mitotic exit network and the pathogenicity of the phytopathogen. These findings provide a novel molecular basis for the design and development of chemicals that prevent phytopathogen infection. [ABSTRACT FROM AUTHOR]