Programmed cell cycle arrest is required for infection of corn plants by the fungus Ustilago maydis

Abstract

Ustilago maydis is a plant pathogen that requires a specific structure called infective filament to penetrate the plant tissue. Although able to grow, this filament is cell cycle arrested on the plant surface. This cell cycle arrest is released once the filament penetrates the plant tissue. The reasons and mechanisms for this cell cycle arrest are unknown. Here, we have tried to address these questions. We reached three conclusions from our studies. First, the observed cell cycle arrest is the result of the cooperation of at least two distinct mechanisms: one involving the activation of the DNA damage response (DDR) cascade; and the other relying on the transcriptional downregulation of Hsl1, a kinase that modulates the G2/M transition. Second, a sustained cell cycle arrest during the infective filament step is necessary for the virulence in U. maydis, as a strain unable to arrest the cell cycle was severely impaired in its ability to infect corn plants. Third, production of the appressorium, a structure required for plant penetration, is incompatible with an active cell cycle. The inability to infect plants by strains defective in cell cycle arrest seems to be caused by their failure to induce the appressorium formation process. In summary, our findings uncover genetic circuits to arrest the cell cycle during the growth of this fungus on the plant surface, thus allowing the penetration into plant tissue.

Colletotrichum orbiculare Regulates Cell Cycle G1/S Progression via a Two-Component GAP and a GTPase to Establish Plant Infection

“…In M. oryzae, S phase is necessary to initiate appressorium differentiation, while M phase and autophagy in conidia are essential for the development of functional appressoria that form the penetration peg (Veneault-Fourrey et al, 2006;Saunders et al, 2010a). By contrast, in U. maydis, cell cycle arrest in G2 phase is required for the induction of appressorium formation, and the arrest is held until the infective dikaryotic hyphae penetrate host plants (Castanheira et al, 2014). Thus, M. oryzae and U. maydis have distinctive mechanisms of appressorium development that are coordinated with proper cell cycle progression.…”

The Biotrophic Development of Ustilago maydis Studied by RNA-Seq Analysis

“…The dikaryon is cell cycle arrested (Castanheira et al, 2014) and is able to invade the plant via a specialized infection structure, the appressorium. Appressoria allow direct invasion of epidermal plant cells in a process which is likely aided by plant cell wall degrading enzymes and plant cell wall loosening.…”

Penetration Peg Formation and Invasive Hyphae Development Require Stage-Specific Activation of MoGTI1 in Magnaporthe oryzae

“…Mitotic entry is considered to be sufficient to initiate appressorium maturation but exit from mitosis is required only for plant infection (Saunders et al 2010). In U. maydis, cell cycle regulation has been shown to be tightly regulated during plant infection (Castanheira et al 2014). Recently, we found that the wheat scab fungus F. graminearum has two CDC2 kinase genes.…”