Current Genetics

, Volume 47, Issue 5, pp 316–333 | Cite as

Differential gene expression in filamentous cells of Ustilago maydis

  • Mohan R. Babu
  • Kristen Choffe
  • Barry J. Saville
Research Article


When fungi interact with plants as pathogens or as symbionts, there are often changes in fungal cell morphology and nuclear state. This study establishes the use of cDNA microarrays to detect gene expression changes in Ustilago maydis cells that differ in structure and nuclear content. Categorizing differentially expressed genes on the basis of function indicated that U. maydis cell types vary most in the expression of genes related to metabolism. We also observed that more genes are up-regulated in the filamentous dikaryon than in the filamentous diploid, relative to non-pathogenic budding cells. Our comparison of pathogenic development indicated that the dikaryon is more virulent than the diploid. Other identified expression patterns suggest a cell-specific difference in nutrient acquisition, cell metabolism and signal transduction. The relevance of gene expression change to cell type biology is discussed.


Fungal pathogen Gene expression Virulence Dikaryon Diploid 

Supplementary material

294_2005_574_ESM_supp.pdf (124 kb)
(PDF 125 KB)


  1. Agrios GN (1997) Plant pathology, 4th edn. Academic, New YorkGoogle Scholar
  2. Aign V, Hoheisel JD (2003) Analysis of nutrient-dependent transcript variations in Neurospora crassa. Fungal Genet Biol 40:225–233Google Scholar
  3. Akopyants NS, Matlib RS, Bukanova EN, Smeds MR, Brownstein BH, Stormo GD, Beverley SM (2004) Expression profiling using random genomic DNA microarrays identifies differentially expressed genes associated with three major developmental stages of the protozoan parasite Leishmania major. Mol Biochem Parasitol 136:71–86Google Scholar
  4. Austin R, Provart N, Sacadura NT, Nugent KG, Babu M, Saville BJ (2004) A comparative genomic analysis of ESTs from Ustilago maydis. Funct Integr Genomics 4:207–218Google Scholar
  5. Banuett F (1995) Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu Rev Genet 29:179–208CrossRefPubMedGoogle Scholar
  6. Banuett F, Herskowitz I (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA 86:5878–5882Google Scholar
  7. Banuett F, Herskowitz I (1996) Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122:2965–2976Google Scholar
  8. Basse CW, Steinberg G (2004) Ustilago maydis, model system for analysis of the molecular basis of fungal pathogenicity. Mol Plant Pathol 5:83–92Google Scholar
  9. Basse CW, Stumpferl S, Kahmann R (2000) Characterization of a Ustilago maydis gene specifically induced during the biotrophic phase: evidence for negative as well as positive regulation. Mol Cell Biol 20:321–329Google Scholar
  10. Belhumeur P, Lee A, Tam R, DiPaolo T, Fortin N, Clark MW (1993) GSP1 and GSP2, genetic suppressors of the prp20-1 mutant in Saccharomyces cerevisiae: GTP-binding proteins involved in the maintenance of nuclear organization. Mol Cell Biol 13:2152–2161Google Scholar
  11. Bortfeld M, Auffarth K, Kahmann R, Basse CW (2004) The Ustilago maydis a2 mating-type locus genes iga2 and rga2 compromise pathogenicity in the absence of the mitochondrial p32 family protein Mrb1. Plant Cell 16:2233–2248Google Scholar
  12. Boyd ML, Carris LM (1997) Enhancement of teliospore germination in wheat- and wild grass-infecting species of Tilletia on activated charcoal medium. Phytopathology 88:260–264Google Scholar
  13. Brachmann A, Weinzierl G, Kämper J, Kahmann R (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42:1047–1063CrossRefPubMedGoogle Scholar
  14. Cano-Canchola C, Acevedo L, Ponce-Noyola P, Flores-Martinez A, Flores-Carreon A, Leal-Morales CA (2000) Induction of lytic enzymes by the interaction of Ustilago maydis with Zea mays tissues. Fungal Genet Biol 29:145–151Google Scholar
  15. Chambergo FS, Bonaccorsi ED, Ferriera AJ, Ramos AS, Ferriera JJ Jr, Abrahao-Neto J, Farah JP, El-Dorry H (2002) Elucidation of the metabolic fate of glucose in filamentous fungus Trichoderma reesei using expressed sequence tag (EST) analysis and cDNA microarrays. J Biol Chem 277:13983–13988Google Scholar
  16. Chigira Y, Abe K, Gomi K, Nakajima T (2002) ChsZ, a gene for a novel class of chitin synthase from Aspergillus oryzae. Curr Genet 41:261–267Google Scholar
  17. Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, Wolfsberg TG, Gabriellan AE, Landsman D, Lockhart DJ, Davis RW (1998) A genomic-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 2:65–73CrossRefPubMedGoogle Scholar
  18. Christensen JJ (1931) Studies on the genetics of Ustilago zeae. Phytopathology 4:124–188Google Scholar
  19. Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I (1998) The transcriptional program of sporulation in budding yeast. Science 282:699–705CrossRefPubMedGoogle Scholar
  20. Clark IA, Alleva LM, Mills AC, Cowden WB (2004) Pathogenesis of malaria and clinically similar conditions. Clin Microbiol Rev 2004 17:509–539Google Scholar
  21. Day PR, Anagnostakis SL (1971) Corn smut sikaryon in culture. Nat New Biol 231:19–20Google Scholar
  22. DeRisi J, Penland L, Brown PO, Bittner ML, Meltzer PS, Ray M, Chen Y, Su YA, Trent JM (1996) Use of cDNA microarray to analyse gene expression patterns in human cancer. Nat Genet 14:457–460Google Scholar
  23. DeRisi JL, Iyer VR, Brown PO (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278:680–686PubMedGoogle Scholar
  24. Dutta S, Gerhold DL, Rice M, Germann M, Kmiec EB (1997) The cloning and overexpression of a cruciform binding protein from Ustilago maydis. Biochim Biophys Acta 1352:258–266Google Scholar
  25. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868CrossRefGoogle Scholar
  26. Gagiano M, Bauer FF, Pretorius IS (2002) The sensing of nutritional status and the relationship to filamentous growth in Saccharomyces cerevisiae. FEMS Yeast Res 2:433–470Google Scholar
  27. Gold SE, Brogdon SM, Mayroga ME, Kronstad JW (1997) The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 9:1585–1594Google Scholar
  28. Herrmann S, Oelmuller R, Buscot F (2004) Manipulation of the onset of ectomycorrhiza formation by indole-3-acetic acid, activated charcoal or relative humidity in the association between oak microcuttings and Piloderma croceum: influence on plant development and photosynthesis. J Plant Physiol 161:509–517Google Scholar
  29. Heyer LJ, Kruglyak S, Yooseph S (1999) Exploring expression data: identification and analysis of co-expressed genes. Genome Res 9:1106–1115Google Scholar
  30. Holliday R (1961) Induced mitotic crossing-over in Ustilago maydis. Genet Res 2:231–248Google Scholar
  31. Holliday R (1974) Ustilago maydis. In: King RC (ed) Handbook of genetics, vol 1. Plenum, New York, pp 575–595Google Scholar
  32. Huber SMFE, Lottspeich F, Kämper J (2002) A gene that encodes a product with similarity to dioxygenases is highly expressed in teliospores of Ustilago maydis. Mol Genet Genomics 267:757–771CrossRefPubMedGoogle Scholar
  33. Kadowaki T, Goldfarb D, Spitz LM, Tartakoff AM, Ohno M (1993) Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO J 12:2929–2937Google Scholar
  34. Kojic M, Kostrub CF, Buchman AR, Holloman WK (2002) BRCA2 homolog required for proficiency in DNA repair, recombination, and genome stability in Ustilago maydis. Mol Cell 10:683–691CrossRefPubMedGoogle Scholar
  35. Kronstad JW, Leong SA (1989) Isolation of two alleles of the b locus of Ustilago maydis. Proc Natl Acad Sci USA 86:978–982Google Scholar
  36. Kronstad JW, Leong SA (1990) The b mating- type locus of Ustilago maydis contains variable and constant regions. Genes Dev 4:1384–1395PubMedGoogle Scholar
  37. Madhani HD, Fink GR (1998) The control of filamentous differentiation and virulence in fungi. Trends Cell Biol 8:348–353Google Scholar
  38. Martínez-Espinoza AD, Garcia-Pedrajas MD, Gold SE (2002) The ustilaginales as plant pests and model systems. Fungal Genet Biol 35:1–20CrossRefPubMedGoogle Scholar
  39. Mews HW, Albermann K, Bahr M, Frishman D, Gleissner A, Hani J, Heumann K, Kliene K, Maierl A, Oliver SG, Pfeiffer F, Zollner A. (1997) Overview of the yeast genome. Nature 387 [Suppl]:7–8Google Scholar
  40. Neal SJ, Gibson M, Anthony KC, Westwood JT (2003) Construction of a cDNA-based microarray for Drosophila melanogaster: a comparison of gene transcription profiles from SL2 and Kc167 cells. Genome 46:879–892Google Scholar
  41. Nugent KG, Choffe K, Saville BJ (2004) Gene expression during Ustilago maydis diploid filamentous growth: EST library creation and analyses. Fungal Genet Biol 41:349–360CrossRefPubMedGoogle Scholar
  42. O’Donnell KL, McLaughlin DJ (1984) Ultrastructure of meiosis in Ustilago maydis. Mycologia 76:468–485Google Scholar
  43. Quadbeck-Seeger C, Wanner G, Huber S, Kahmann R, Kämper J (2000) A protein with similarity to the human retinoblastoma binding protein 2 acts specifically as a repressor for genes regulated by the b mating-type locus in Ustilago maydis. Mol Microbiol 38:154–166Google Scholar
  44. van de Rhee MD, Mendes O, Werten MWT, Huizing HJ, Mooibroek H (1996) Highly efficient homologous integration via tandem exo-b-1,3,-glucanase genes in common mushroom, Agaricus bisporus. Curr Genet 30:166–173Google Scholar
  45. Romeis T, Brachmann A, Kahmann R, Kämper J (2000) Identification of a target gene for bE-bW homeodomain protein complex in Ustilago maydis. Mol Microbiol 37:54–66CrossRefPubMedGoogle Scholar
  46. Ross DT, Scherf U, Eisen MB, Perou CM, Rees C, Spellman P, Iyer V, Jeffrey SS, Van de Rijn M, Waltham M, Pergamenschikov A, Lee JCF, Lashkari D, Shalon D, Myers TG, Weinstein JN, Botstein D, Brown PO (2000) Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 24:227–235Google Scholar
  47. Sacadura NT, Saville BJ (2003) Gene expression and EST analyses of Ustilago maydis germinating teliospores. Fungal Genet Biol 40:47–64CrossRefPubMedGoogle Scholar
  48. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp 7.27–7.30Google Scholar
  49. Saville BJ, Leong SA (1992) The molecular biology of pathogenesis in Ustilago maydis. In: Setlow JK (ed) Genetic engineering: principles and methods, vol 14. Plenum, New YorkGoogle Scholar
  50. Schauwecker F, Wanner G, Kahmann R (1995) Filament-specific expression of a cellulose gene in the dimorphic fungus Ustilago maydis. Biol Chem Hoppe-Seyler 376:617–625Google Scholar
  51. Sims AH, Robson GD, Hoyle DC, Oliver SG, Turner G, Prade RA, Russell HH, Dunn-Coleman NS, Gent ME (2004) Use of expressed sequence tag analysis and cDNA microarrays of the filamentous fungus Aspergillus nidulans. Fungal Genet Biol 41:199–212Google Scholar
  52. Snetselaar KM, Mims CW (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84:193–203Google Scholar
  53. Snetselaar KM, Mims CW (1994) Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol Res 98:347–355Google Scholar
  54. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B (1998) Comprehensive identification of cell cycle regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9:3273–3297PubMedGoogle Scholar
  55. Takano Y, Choi W, Mitchell TK, Okuno T, Dean RA (2003) Large scale parallel analysis of gene expression during infection-related morphogenesis of Magnaporthe grisea. Mol Plant Pathol 4:337–346Google Scholar
  56. Taniguchi M, Miura K, Iwao H, Yamanaka S (2001) Quantitative assessment of DNA microarrays—comparison with northern blot analyses. Genomics 71:34–39CrossRefGoogle Scholar
  57. Wen X, Furham S, Michaels GS, Carr DB, Smith S, Barker JL, Somogyi R (1998) Large-scale temporal gene expression mapping of central nervous system development. Proc Natl Acad Sci USA 95:334–339Google Scholar
  58. Yao B, Rakhade SN, Li Q, Ahmed S, Krauss R, Draghici S, Loeb JA (2004) Accuracy of cDNA microarray methods to detect small gene expression changes induced by neuregulin on breast epithelial cells. BMC Bioinformatics 5:1–16Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Mohan R. Babu
    • 1
  • Kristen Choffe
    • 1
  • Barry J. Saville
    • 1
  1. 1.Department of BotanyUniversity of Toronto at MississaugaMississaugaCanada

Personalised recommendations