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

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.