Metamorphosis of the Basidiomycota Ustilago maydis: Transformation of yeast-like cells into basidiocarps

• Published in: Fungal genetics and biology 2012-10, Vol.49 (10), p.765-771
• Main Authors: Cabrera-Ponce, José L., León-Ramírez, Claudia G., Verver-Vargas, Aurora, Palma-Tirado, Lourdes, Ruiz-Herrera, José
• Format: Article
• Language: English
• Subjects: Auxins; Basidiocarps; Basidiospores; Cell culture; Corn smut; Cytokinins; Cytokinins - pharmacology; Diploidy; DNA, Fungal - genetics; Embryogenic calli; Fruiting Bodies, Fungal - cytology; Fruiting Bodies, Fungal - genetics; Fruiting Bodies, Fungal - growth & development; Gibberellins - pharmacology; Haploidy; Holobasidia; Hyphae - cytology; Hyphae - drug effects; Hyphae - genetics; Hyphae - growth & development; Indoleacetic Acids - pharmacology; Life cycle; Meiosis; Metamorphosis; Metamorphosis, Biological; Plant Diseases - microbiology; Plant Growth Regulators - pharmacology; Recombination; Recombination, Genetic; Spores, Fungal - cytology; Spores, Fungal - drug effects; Spores, Fungal - genetics; Spores, Fungal - growth & development; Teliospores; Transformation; Tumors; Ustilago - cytology; Ustilago - drug effects; Ustilago - genetics; Ustilago - growth & development; Ustilago maydis; Virulence; Yeasts - cytology; Yeasts - drug effects; Yeasts - genetics; Yeasts - growth & development; Zea mays; Zea mays - cytology; Zea mays - embryology; Zea mays - microbiology
• ISSN: 1087-1845; 1096-0937
• DOI: 10.1016/j.fgb.2012.07.005

► We demonstrate for the first time that a species of Ustilaginomycotina is able to form basidiocarps. ► For the first time the sexual cycle of a species of Ustilaginomycotina is obtained in vitro. ► The conditions to obtain reproducibly these processes are described. Ustilago maydis (DC) Cda., a phytopathogenic Basidiomycota, is the causal agent of corn smut. During its life cycle U. maydis alternates between a yeast-like, haploid nonpathogenic stage, and a filamentous, dikaryotic pathogenic form that invades the plant and induces tumor formation. As all the members of the Subphylum Ustilaginomycotina, U. maydis is unable to form basidiocarps, instead it produces teliospores within the tumors that germinate forming a septate basidium (phragmobasidium). We have now established conditions allowing a completely different developmental program of U. maydis when grown on solid medium containing auxins in dual cultures with maize embryogenic calli. Under these conditions U. maydis forms large hemi-spheroidal structures with all the morphological and structural characteristics of gastroid-type basidiocarps. These basidiocarps are made of three distinct hyphal layers, the most internal of which (hymenium) contains non-septate basidia (holobasidia) from which four basidiospores develop. In basidiocarps meiosis and genetic recombination occur, and meiotic products (basidiospores) segregate in a Mendelian fashion. These results are evidence of sexual cycle completion of an Ustilaginomycotina in vitro, and the demonstration that, besides its quasi-obligate biotrophic pathogenic mode of life, U. maydis possesses the genetic program to form basidiocarps as occurs in saprophytic Basidiomycota species.