Environmental Signals Controlling Sexual Development of the Corn Smut Fungus Ustilago maydis through the Transcriptional Regulator Prf1

Abstract

Environmental signals induce and coordinate discrete morphological transitions during sexual development of Ustilago maydis. In this fungus, mating of two compatible haploid sporidia is a prerequisite for plant infection. Cell fusion is governed by the action of pheromones and receptors, whereas the subsequent pathogenicity program is controlled by the combinatorial interaction of homeodomain proteins. The U. maydis pheromone response factor (Prf1) is a central regulator of both processes. We have analyzed the regulation of the prf1 gene and demonstrate that pheromone and cAMP signaling regulate prf1 post-transcriptionally. Transcriptional activation of prf1 was observed in the presence of carbon sources, such as glucose and fructose, allowing us to define the cis-acting element in the prf1 promoter that mediates these effects. The same element provides for negative control of prf1 gene transcription at high cAMP levels. A protein that specifically binds to this element was purified and analyzed for its role in prf1 gene regulation. On the basis of these results, we present a model in which prf1 integrates different environmental signals to control development in U. maydis.

Investigating Host Induced Meiosis in a Fungal Plant Pathogen

“…Four different environmental signals affect Prf1: the carbon source, pheromones, the b heterodimer and the cAMP pathway. These signals act to control Prf1 transcriptionally and post-transcriptionally (Hartmann et al, 1999). This is similar to the function of Ste11 in S. pombe, which controls pheromone gene expression in response to environmental signals, allowing for conjugation, the initiation of the sexual cycle and the commencement of meiosis.…”

“…High cAMP levels repress Prf1 transcription though the UAS. It is important to note that this is a separate mechanism from the post-transcriptional activation of Prf1 by PKA, and this seemingly contradictory activity of the cAMP pathway results in increase in a gene expression at moderate cAMP levels, but repression through transcriptional control at higher levels (Hartmann et al, 1999). This emphasizes the fine scale control imparted by cAMP levels.…”

“…Interestingly, it is a transcription factor that is involved in the sexual development of U. maydis in response to environmental signals, much like Ste11. Prf1 is involved in regulating a and b mating type gene expression, resulting in high levels of pheromones and receptors during mating, and controlling b gene expression during pathogenesis (Hartmann et al, 1999). Four different environmental signals affect Prf1: the carbon source, pheromones, the b heterodimer and the cAMP pathway.…”

“…The Prf1 UAS appears to regulate transcription of Prf1 in response to cAMP and carbon source signals. Glucose or sucrose stimulates Prf1 transcription via the UAS (Hartmann et al, 1999). High cAMP levels repress Prf1 transcription though the UAS.…”

Ustilago maydis – a valuable model system for the study of fungal dimorphism and virulence

“…The Prf1 protein carries several sequence motifs specific for PKAand MAPK-dependent phosphorylation and the presence of these sites is essential for Prf1 function (Hartmann et al, 1999). In addition, expression of the prf1 gene itself is subject to nutritional stimulation and to positive feedback control after pheromone stimulation (Hartmann et al, 1999). One has to assume that basal activity of Prf1 requires phosphorylation by lowlevel constitutive activity of the MAPK Kpp2\Ubc3.…”