Molecular Mechanisms Involved in the Multicellular Growth of Ustilaginomycetes.

Multicellularity is defined as the developmental process by which unicellular organisms became pluricellular during the evolution of complex organisms on Earth. This process requires the convergence of genetic, ecological, and environmental factors. In fungi, mycelial and pseudomycelium growth, snowflake phenotype (where daughter cells remain attached to their stem cells after mitosis), and fruiting bodies have been described as models of multicellular structures. Ustilaginomycetes are Basidiomycota fungi, many of which are pathogens of economically important plant species. These fungi usually grow unicellularly as yeasts (sporidia), but also as simple multicellular forms, such as pseudomycelium, multicellular clusters, or mycelium during plant infection and under different environmental conditions: Nitrogen starvation, nutrient starvation, acid culture media, or with fatty acids as a carbon source. Even under specific conditions, Ustilago maydis can form basidiocarps or fruiting bodies that are complex multicellular structures. These fungi conserve an important set of genes and molecular mechanisms involved in their multicellular growth. In this review, we will discuss in-depth the signaling pathways, epigenetic regulation, required polyamines, cell wall synthesis/degradation, polarized cell growth, and other cellular-genetic processes involved in the different types of Ustilaginomycetes multicellular growth. Finally, considering their short life cycle, easy handling in the laboratory and great morphological plasticity, Ustilaginomycetes can be considered as model organisms for studying fungal multicellularity.

Regulation of genes involved in cell wall synthesis and structure during Ustilago maydis dimorphism.

The cell wall is the structure that provides the shape to fungal cells and protects them from the difference in osmotic pressure existing between the cytosol and the external medium. Accordingly, changes in structure and composition of the fungal wall must occur during cell differentiation, including the dimorphic transition of fungi. We analyzed, by use of microarrays, the transcriptional regulation of the 639 genes identified to be involved in cell wall synthesis and structure plus the secretome of the Basidiomycota species Ustilago maydis during its dimorphic transition induced by a change in pH. Of these, 189 were differentially expressed during the process, and using as control two monomorphic mutants, one yeast like and the other mycelium constitutive, 66 genes specific of dimorphism were identified. Most of these genes were up-regulated in the mycelial phase. These included CHS genes, genes involved in ß-1,6-glucan synthesis, N-glycosylation, and proteins containing a residue of glycosylphosphatidylinositol, and a number of genes from the secretome. The possible significance of these data on cell wall plasticity is discussed.

Transcriptional regulation of the genes encoding chitin and ß-1,3-glucan synthases from Ustilago maydis.

Transcriptional regulation of genes encoding chitin synthases (CHS) and ß-1,3-glucan synthase (GLS) from Ustilago maydis was studied. Transcript levels were measured during the growth curve of yeast and mycelial forms, in response to ionic and osmotic stress, and during infection of maize plants. Expression of the single GLS gene was constitutive. In contrast, CHS genes expression showed differences depending on environmental conditions. Transcript levels were slightly higher in the mycelial forms, the highest levels occurring at the log phase. Ionic and osmotic stress induced alterations in the expression of CHS genes, but not following a defined pattern, some genes were induced and others repressed by the tested compounds. Changes in transcripts were more apparent during the pathogenic process. At early infection stages, only CHS6 gene showed significant transcript levels, whereas at the period of tumor formation CHS7 and CHS8 genes were also were induced.