The machinery for cell polarity, cell morphogenesis, and the cytoskeleton in the Basidiomycete fungus Ustilago maydis-a survey of the genome sequence

Abstract

Ustilago maydis, a Basidiomycete fungus that infects maize, exhibits two basic morphologies, a yeast-like and a filamentous form. The yeast-like cell is elongated, divides by budding, and the bud grows by tip extension. The filamentous form divides at the apical cell and grows by tip extension. The repertoire of morphologies is increased during interaction with its host, suggesting that plant signals play an important role in generation of additional morphologies. We have used Saccharomyces cerevisiae and Schizosaccharomyces pombe genes known to play a role in cell polarity and morphogenesis, and in the cytoskeleton as probes to survey the U. maydis genome. We have found that most of the yeast machinery is conserved in U. maydis, albeit the degree of similarity varies from strong to weak. The U. maydis genome contains the machinery for recognition and interpretation of the budding yeast axial and bipolar landmarks; however, genes coding for some of the landmark proteins are absent. Genes coding for cell polarity establishment, exocytosis, actin and microtubule organization, microtubule plus-end associated proteins, kinesins, and myosins are also present. Genes not present in S. cerevisiae and S. pombe include a homolog of mammalian Rac, a hybrid myosin-chitin synthase, and several kinesins that exhibit more similarity to their mammalian counterparts. We also used the U. maydis genes identified in this analysis to search other fungal and other eukaryotic genomes to identify the closest homologs. In most cases, not surprisingly, the closest homolog is among filamentous fungi, not the yeasts, and in some cases it is among mammals.

Figure 1. Different morphologies in the life cycle of U. maydis

U. maydis exhibits two basic morphologies, a yeast-like and a filamentous form. Interaction with the plant increases the repertoire of morphologies observed suggesting that plant signals play a role in reorganization of the machinery for cell polarity, cell morphogenesis, and the cytoskeleton. Panel A. Different stages of budding of haploid yeast-like cells. Panel B. Dikaryotic filaments in culture. No branching is observed. Panels C, D, E, and F. Dikaryotic filaments growing in the plant. Panel C shows a branch (arrowhead). Panel D shows a clamp-like structure (arrowhead) (see Scherer et al., 2006). Panels E and F show multiple branches (arrowheads in Panel F). The cell wall of the plant cell is indicated an arrow. Panel G. Cylindrical cells released upon hyphal fragmentation within the tumors during teliospore formation. Panel H. The cylindrical cells undergo morphological changes during teliospore formation. The cells in Panels G and H are normally embedded in a mucilaginous matrix, which may provide osmotic support during the cell wall remodelling events occurring during these morphological transitions (Banuett and Herskowtiz, 1996). Inset (I). Mature teliospores with echinulate cell wall. The teliospores give rise to haploid yeast-like cells upon meiosis. The scale bar in Panel A is 5 µm, and in Panels B, C, D, E, F, and H, 50 µm.