Biz1, a Zinc Finger Protein Required for Plant Invasion byUstilago maydis, Regulates the Levels of a Mitotic Cyclin

Plant invasion by pathogenic fungi involves regulated growth and highly organized fungal morphological changes. For instance, when the smut fungus Ustilago maydis infects maize (Zea mays), its dikaryotic infective filament is cell cycle arrested, and appressoria are differentiated prior to plant penetration. Once the filament enters the plant, the cell cycle block is released and fungal cells begin proliferation, suggesting a tight interaction between plant invasion and the cell cycle and morphogenesis control systems. We describe a novel factor, Biz1 (b-dependent zinc finger protein), which has two Cys(2)His(2) zinc finger domains and nuclear localization, suggesting a transcriptional regulatory function. The deletion of biz1 shows no detectable phenotypic alterations during axenic growth. However, mutant cells show a severe reduction in appressoria formation and plant penetration, and those hyphae that invade the plant arrest their pathogenic development directly after plant penetration. biz1 is induced via the b-mating-type locus, the key control instance for pathogenic development. The gene is expressed at high levels throughout pathogenic development, which induces a G2 cell cycle arrest that is a direct consequence of the downregulation of the mitotic cyclin Clb1. Our data support a model in which Biz1 is involved in cell cycle arrest preceding plant penetration as well as in the induction of appressoria.