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Ustilago maydis, corn smut

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Taxonomic lineage

cellular organisms - Eukaryota - Fungi/Metazoa group - Fungi - Dikarya - Basidiomycota - Ustilaginomycotina - Ustilaginomycetes - Ustilaginales - Ustilaginaceae - Ustilago - Ustilago maydis

Brief facts

• Ustilago maydis (corn smut) is dimorphic filamentous fungus that together with mushrooms and many other fungi belongs to phylum Basidiomycota. Dimorphic means that the fungus exists in two forms: saprotrophic yeast-like form that lives on dead organic material and is non-pathogenic and parasitic filamentous form that derives nutrients from its host. Filamentous means that unlike yeasts, which cells do not have polarity and proliferate by simple budding U. maydis expands its mycelium by polar tip hyphal growth.
• Order Ustilaginales contains many important plant pathogens such as Ustilago hordei, Ustilago nuda, Ustilago nigra (oat pathogens), Tilletia indica, Tilletia caries, and Tilletia controversa (wheat pathogens). Of all Ustilaginales, U. maydis is best known and has rather narrow specificity - it can parazitize only on corn (Zea mays) and on its ancestor teozinte (Zea mexicana).
• U. maydis causes stunting, chlorosis, and above all, induces formation of galls, or tumors, on infested corn palnt, primarily on ears.
• Corn invaded by U. maydis is considered a delicacy in Mexico. Traditional Mexican dishes such as Quesadillas de huitlacoche or Sopa de huitlacoche have been recently introduced into the high-end restaurants with success. The cooking of U. maydis infested corn is believed to exist since pre-Columbus era.
• U. maydis is used extensively in biological research and is considered a very valuable model system not only in molecular plant pathology but also in studies of eukaryotic cell's signaling pathways, molecular transport, cell division mechanisms, and many other areas.

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Developmental stages

Life cycle of U. maydis has been subject of intensive research. It has many fascinating aspects, which cannot be described in this short review. Some of them will be gradually added.

• Non-parasitic phase Diploid teliospores released into environment from corn tumors by parasitic form of the fungus.
  • Germination Teliospores germinate inder favorable conditions forming protomycelium.
  • Meiosis Meiosis occurs giving rise to two haploid lines of the fungus.
  • Saprobic growth Haploid cells (sporidia) start to colonize soil and dead organic matter proliferating by polar budding in yeast-like manner.
  • Pheromone exchange Sporidia sense each other by exchanging pheromones; switch from budding to hyphal growth occurs.
  • Conjugation tubes
    formation Cell start to make narrow filaments, which are referred as mating hyphae or conjugation tubes.
  • Dikaryon formation The conjugation tubes grow toward each other and upon fusion form dikaryon.
• Parasitic phase The dikaryon is pathogenic if it resulted from fusion of two compatible haploid hyphae.
  • Invasion Infective dikaryon invades the plant through natural openings such as stromata and floral organs.
  • Tumor formation Fungus hyphae grow inside the plant intra- and intercellularly causing formation of tumors.
  • Sporulation Hyphae acquire a round shape, and a thick cell wall is formed; as the spores mature they becomes pigmented; karyogamy takes place with the formation of diploid stage of the fungus; resultant teliospores dispersed into environment and saprobic stage of the fungus begins.

 

 

References

• Wahl R, Wippel K, Goos S, Kämper J, Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol. 2010 Feb 9;8(2):e1000303.

  

  U. maydis–induced tumor formation in maize and predicted structure of Srt1.
  
  (A) Ear tumors of a maize plant infected with U. maydis that caused tumor induction.
  (B) Uninfected (middle) and U. maydis–infected, tumorous (left) maize kernels, plus a tumor section (right) showing layers of black fungal teliospores.
  (C) Putative topology of Srt1.

• Freitag J, Lanver D, Böhmer C, Schink KO, Bölker M, Sandrock B. Septation of infectious hyphae is critical for appressoria formation and virulence in the smut fungus Ustilago maydis. PLoS Pathog. 2011 May;7(5):e1002044.

  

  Filamentous growth of U. maydis on the plant surface.
  The dikaryotic filament of U. maydis grows by inserting retraction septa at the distal end of the filament. For details see main text. Arrows indicate growth direction; asterisk marks a new assembled retraction septum and the cytoplasm-filled tip compartment is drawn in grey.

• Nadal M, García-Pedrajas MD, Gold SE. Dimorphism in fungal plant pathogens. FEMS Microbiol Lett. 2008 Jul;284(2):127-34. Epub 2008 May 12.
• Steinberg G, Perez-Martin J. Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol. 2008 Feb;18(2):61-7.
• Klosterman SJ, Perlin MH, Garcia-Pedrajas M, Covert SF, Gold SE. Genetics of morphogenesis and pathogenic development of Ustilago maydis. Adv Genet. 2007;57:1-47.
• Feldbrügge M, Kämper J, Steinberg G, Kahmann R. Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol. 2004 Dec;7(6):666-72.
• Anderson AL, Leffler K. Castles and cuitlacoche: the first international Ustilago conference. Fungal Genet Biol. 2003 Apr;38(3):265-71.
• Gage MJ, Bruenn J, Fischer M, Sanders D, Smith TJ. KP4 fungal toxin inhibits growth in Ustilago maydis by blocking calcium uptake. Mol Microbiol. 2001 Aug;41(4):775-85.
• Bölker M. Ustilago maydis--a valuable model system for the study of fungal dimorphism and virulence. Microbiology. 2001 Jun;147(Pt 6):1395-401.
• Banuett F. Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu Rev Genet. 1995;29:179-208.
• Banuett F. Ustilago maydis, the delightful blight. Trends Genet. 1992 May
• Major topic "Ustilago": free full text articles in PubMed