Pathocycles: Ustilago maydis as a model to study the relationships between cell cycle and virulence in pathogenic fungi

Abstract

Activation of virulence in pathogenic fungi often involves diVerentiation processes that need the reset of the cell cycle and induction of a new morphogenetic program. Therefore, the fungal capability to modify its cell cycle constitutes an important determinant in carrying out a successful infection. The dimorphic fungus Ustilago maydis is the causative agent of corn smut disease and has lately become a highly attractive model in addressing fundamental questions about development in pathogenic fungi. The diVerent morphological and genetic changes of U. maydis cells during the pathogenic process advocate an accurate control of the cell cycle in these transitions. This is why this model pathogen deserves attention as a powerful tool in analyzing the relationships between cell cycle, morphogenesis, and pathogenicity. The aim of this review is to summarize recent advances in the unveiling of cell cycle regulation in U. maydis. We also discuss the connection between cell cycle and virulence and how cell cycle control is an important downstream target in the fungus-plant interaction.

The distinct wiring between cell cycle regulation and the widely conserved Morphogenesis-Related (MOR) pathway in the fungus Ustilago maydis determines the morphological outcome

“…In U. maydis, cell size in daughter cells is dependent on the length of G2 phase: the longer the G2 phase, the larger the daughter cell and vice versa (Pérez-Martín et al, 2006). Therefore a delay in G2 phase is compatible with the enlarged cell compartments we observed in ukc1-defective cells.…”

“…organisms (including U. maydis) as an integrator of signals related to cell size (Daga and Jimenez, 1999;Jorgensen and Tyers, 2004;Pérez-Martín et al, 2006;Rupes, 2002). The results shown in the previous paragraph strongly suggest the idea that cell cycle regulation could also act as an integrator of signals related to the ability to sustain or not polar growth in U. maydis.…”

“…The intricacies between cell cycle regulation and morphogenesis in fungi as well as the apparent non-conservation of the MOR pathway targets led us to think that some of the differences observed in MOR pathway regulation in fungi could be related to species-specific connections between this pathway and cell cycle regulation. We also base this assumption on our previous experiments addressing the connections between the cell cycle and MAPK-based signaling pathways in the phytopathogenic fungus Ustilago maydis (Pérez-Martín et al, 2006). This fungus has been used as a model system in fungal development for many years (Steinberg and Pérez-Martín, 2008).…”

Carbon source-induced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins

“…The observed carbon source-induced modifications of the morphology of M. perniciosa mycelia together with changes in secretome composition could be correlated to the pathogenesis of this fungus, as observed for other microorganisms (Hegedus and Rimmer, 2005;Perez-Martin et al, 2006;Kamoun, 2007;Klosterman et al, 2007). Specifically, for hemibiotrophic and necrotrophic fungi, the induction of host cell death, a characteristic of pathogenesis, is related to the secretion of pathogenesis proteins into the inter-or intra-cellular space (Kamoun, 2007).…”

Ortholog of BRCA2-interacting protein BCCIP controls morphogenetic responses during DNA replication stress in Ustilago maydis

“…That is, bud formation takes place at the onset of G2 phase [34]. The accumulation of unbudded cells in bcp1 mutants therefore suggests either a delay in G1 or S phase.…”