Summary:
Ustilago maydis is a phytopathogenic basidiomycete infecting corn plants. Pathogenic development is initiated via a pheromone/receptor-based system encoded by the a-mating type locus. Upon pheromone stimulation, two compatible haploid sporidia form conjugation hyphae that are cell cycle arrested in the G2 phase. Upon fusion of the conjugation tubes, a dikaryotic hyphae is formed in which the G2 cell cycle arrested is maintained until plant penetration. The processes subsequent to the a-mediated fusion are triggered by the b-mating type locus which encodes a pair of homeodomain proteins, termed bE and bW that can form a heterodimeric complex functioning as a transcriptional regulator.
hdp1 encodes an a- and b-dependently induced homeodomain transcription factor. Deletion of hdp1 impairs filament formation and G2 cell cycle arrest. Upon fusion of compatible Δhdp1 cells, the resulting filaments are reduced in length, and an increased number of hyphae with more than two nuclei is observed. Similarly, deletion of hdp1 leads to a higher frequency of nuclei with single chromosomal content (1C) in pheromone induced conjugation hyphae, implying that hdp1 is involved in the a-mediated G2 cell cycle arrest. In addition, induced hdp1 expression is sufficient to trigger G2 cell cycle arrest and filament formation.
Both Prf1, the main transcriptional regulator within the a-mediated signaling cascade, and Rop1, a factor required for prf1 expression in the saprophytic stage, are induced by Hdp1. Although not required for the pheromone dependent induction of both genes, hdp1 modulates their expression, by that integrating a positive feedback loop from the b-regulatory cascade to the pheromone signaling pathway.
Microarray analysis revealed that two genes associated with cell cycle control are regulated by Hdp1. pcl12, encoding a Pho85-type cyclin, is induced, while clb1 encoding a B-type cyclin, is repressed upon hdp1 induction. Deletion of pcl12 abolishes filament formation in axenic culture. The gene appears to be essential for the Hdp1-induced filamentation and G2 cell cycle arrest; however, its effect on cell cycle arrest is most likely also influenced by environmental cues. clb1, on the other hand, does not play a major role in Hdp1-mediated cell cycle arrest. The current model suggests that Hdp1 is used for fine-tuning the a- and b- mediated cell cycle regulation and integrating additional environmental cues.