TheUstilago maydisClp1 Protein Orchestrates Pheromone andb-Dependent Signaling Pathways to Coordinate the Cell Cycle and Pathogenic Development

Abstract

Regulation of the cell cycle and morphogenetic switching during pathogenic and sexual development in Ustilago maydis is orchestrated by a concerted action of the a and b mating-type loci. Activation of either mating-type locus triggers the G2 cell cycle arrest that is a prerequisite for the formation of the infectious dikaryon; this cell cycle arrest is released only after penetration of the host plant. Here, we show that bW, one of the two homeodomain transcription factors encoded by the b mating-type locus, and the zinc-finger transcription factor Rbf1, a master regulator for pathogenic development, interact with Clp1 (clampless 1), a protein required for the distribution of nuclei during cell division of the dikaryon. In addition, we identify Cib1, a previously undiscovered bZIP transcription factor required for pathogenic development, as a Clp1-interacting protein. Clp1 interaction with bW blocks b-dependent functions, such as the b-dependent G2 cell cycle arrest and dimorphic switching. The interaction of Clp1 with Rbf1 results in the repression of the a-dependent pheromone pathway, conjugation tube formation, and the a-induced G2 cell cycle arrest. The concerted interaction of Clp1 with Rbf1 and bW coordinates a-and b-dependent cell cycle control and ensures cell cycle release and progression at the onset of biotrophic development.

Crosstalk between the Unfolded Protein Response and Pathways That Regulate Pathogenic Development inUstilago maydis

“…The biotrophic stage is initiated by fusion of two haploid cells via a pheromone-based recognition system encoded by the a mating-type locus (Bölker et al, 1992). The resulting filamentous dikaryon is characterized by a G2 cell cycle block and is thus unable to proliferate (Scherer et al, 2006;Mielnichuk et al, 2009;Heimel et al, 2010a). Before plant penetration, the cell cycle-arrested filaments elongate by polar tip growth.…”

Fungal Morphogenesis

“…For example, U. maydis forms a dikaryon after two mating-compatible yeast cells fuse. The dikaryon switches to hyphal growth only after signals from the host plant release the fungus from cell-cycle arrest (Garcia-Muse et al 2004;Heimel et al 2010). Coprinopsis basidia are committed to meiosis and sporulation, and they will continue that development pathway even when excised from their parental fruit body (Chiu and Moore 1988b).…”

Investigating Host Induced Meiosis in a Fungal Plant Pathogen

“…It is noteworthy that Heimel et al (2010) recently showed that UmCib1, a transcription factor required for pathogenic development, is predominantly unspliced during saprophytic growth, but undergoes splicing during biotrophic growth. Therefore, it is highly likely that other biological roles for alternate splicing in U. maydis remain to be discovered.…”