1932

Abstract

My path in science began with a fascination for microbiology and phages and later involved a switch of subjects to the fungus and how it causes disease in maize. I will not provide a review of my work but rather focus on decisive findings, serendipitous, lucky moments when major advances made the –maize system what it is now—a well-established model for biotrophic fungi. I also want to share with you the joy of finding the needle in a haystack at the very end of my scientific career, a fungal structure likely used for effector delivery, and how we were able to translate this into a potential application in agriculture.

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2022-09-08
2024-04-19
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Literature Cited

  1. 1.
    Banuett F, Herskowitz I. 1989. Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. PNAS 86:5878–82
    [Google Scholar]
  2. 2.
    Bölker M, Böhnert HU, Braun KH, Görl J, Kahmann R. 1995. Tagging pathogenicity genes in Ustilago maydis by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 248:547–52
    [Google Scholar]
  3. 3.
    Bölker M, Genin S, Lehmler C, Kahmann R. 1995. Genetic regulation of mating and dimorphism in Ustilago maydis. Can. J. Bot. 73:320–25
    [Google Scholar]
  4. 4.
    Bölker M, Kahmann R. 1989. The Escherichia coli regulatory protein OxyR discriminates between methylated and unmethylated states of the phage Mu mom promoter. EMBO J 8:2403–10
    [Google Scholar]
  5. 5.
    Bölker M, Urban M, Kahmann R. 1992. The a mating type locus of U. maydis specifies cell signaling components. Cell 68:441–50
    [Google Scholar]
  6. 6.
    Brachmann A, Schirawski J, Müller P, Kahmann R. 2003. An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J 22:2199–210
    [Google Scholar]
  7. 7.
    Brachmann A, Weinzierl G, Kämper J, Kahmann R. 2001. Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol. Microbiol. 42:1047–63
    [Google Scholar]
  8. 8.
    Day P, Anagnostakis S, Puhalla J. 1971. Pathogenicity resulting from mutation at the b locus of Ustilago maydis. PNAS 68:533–35
    [Google Scholar]
  9. 9.
    Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V et al. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395–98
    [Google Scholar]
  10. 10.
    Doehlemann G, Van Der Linde K, Aßmann D, Schwammbach D, Hof A et al. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLOS Pathog 5:e1000290
    [Google Scholar]
  11. 11.
    Dutheil JY, Mannhaupt G, Schweizer G, Sieber CKM, Münsterkötter M et al. 2016. A tale of genome compartmentalization: the evolution of virulence clusters in smut fungi. Genome Biol. Evol. 8:681–704
    [Google Scholar]
  12. 12.
    Eichhorn H, Lessing F, Winterberg B, Schirawski J, Kämper J et al. 2006. A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18:3332–45
    [Google Scholar]
  13. 13.
    Fild LJ, Bruenn JA, Chang T-H, Pinhasi O, Koltin Y. 1983. Two Ustilago maydis viral dsRNAs of different size code for the same product. Nucleic Acids Res 11:2765–78
    [Google Scholar]
  14. 14.
    Froeliger EH, Leong SA. 1991. The a mating-type alleles of Ustilago maydis are idiomorphs. Gene 100:113–22
    [Google Scholar]
  15. 15.
    Fukada F, Rössel N, Münch K, Glatter T, Kahmann R. 2021. A small Ustilago maydis effector acts as a novel adhesin for hyphal aggregation in plant tumors. New Phytol 231:416–31
    [Google Scholar]
  16. 16.
    Gillissen B, Bergemann J, Sandmann C, Schroeer B, Bölker M, Kahmann R. 1992. A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68:647–57
    [Google Scholar]
  17. 17.
    Glass NL, Kuldau GA. 1992. Mating type and vegetative incompatibility in filamentous ascomycetes. Annu. Rev. Phytopathol. 30:201–24
    [Google Scholar]
  18. 18.
    Han X, Altegoer F, Steinchen W, Binnebesel L, Schuhmacher J et al. 2019. A kiwellin disarms the metabolic activity of a secreted fungal virulence factor. Nature 565:650–53
    [Google Scholar]
  19. 19.
    Hartmann HA, Krüger J, Lottspeich F, Kahmann R. 1999. Environmental signals controlling sexual development of the corn smut fungus Ustilago maydis through the transcriptional regulator Prf1. Plant Cell 11:1293–305
    [Google Scholar]
  20. 20.
    Hayes W. 1968. The Genetics of Bacteria and Their Viruses New York: John Wiley Sons
  21. 21.
    Heimel K, Scherer M, Vranes M, Wahl R, Pothiratana C et al. 2010. The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLOS Pathog 6:e1001035
    [Google Scholar]
  22. 22.
    Herskowitz I. 1989. A regulatory hierarchy for cell specialization in yeast. Nature 342:749–57
    [Google Scholar]
  23. 23.
    Holliday R. 1961. The genetics of Ustilago maydis. Genet. Res. 2:204–30
    [Google Scholar]
  24. 24.
    Holliday R. 1964. A mechanism for gene conversion in fungi. Genet. Res. 5:282–304
    [Google Scholar]
  25. 25.
    Hsueh Y-P, Heitman J. 2008. Orchestration of sexual reproduction and virulence by the fungal mating-type locus. Curr. Opin. Microbiol. 11:517–24
    [Google Scholar]
  26. 26.
    Kahmann R, Kamp D. 1979. Nucleotide sequences of the attachment sites of bacteriophage Mu DNA. Nature 280:247–50
    [Google Scholar]
  27. 27.
    Kahmann R, Kamp D. 1987. Sequence of the right end of Mu. Phage Mu N Symonds, A Toussaint, P van de Putte, MM Howe 297–308 New York: Cold Spring Harb.
    [Google Scholar]
  28. 28.
    Kahmann R, Ludwig N, Sievers S, Lampe P, Reissmann S et al. 2021. Novel antifungal compounds Eur. Patent Appl. EP21154940.7
  29. 29.
    Kahmann R, Prell H. 1971. Complementation between P22 Amber mutants and phage L. Mol. Gen. Genet. 113:363–66
    [Google Scholar]
  30. 30.
    Kahmann R, Rudt F, Koch C, Mertens G. 1985. G inversion in bacteriophage Mu DNA is stimulated by a site within the invertase gene and a host factor. Cell 41:771–80
    [Google Scholar]
  31. 31.
    Kamp D, Kahmann R, Zipser D, Broker TR, Chow LT. 1978. Inversion of the G DNA segment of phage Mu controls phage infectivity. Nature 271:577–80
    [Google Scholar]
  32. 32.
    Kämper J, Friedrich MW, Kahmann R. 2020. Creating novel specificities in a fungal nonself recognition system by single step homologous recombination events. New Phytol 228:1001–10
    [Google Scholar]
  33. 33.
    Kämper J, Kahmann R, Bölker M, Ma L-J, Brefort T et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101
    [Google Scholar]
  34. 34.
    Kämper J, Reichmann M, Romeis T, Bölker M, Kahmann R. 1995. Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:73–83
    [Google Scholar]
  35. 35.
    Kinscherf TG, Leong SA. 1988. Molecular analysis of the karyotype of Ustilago maydis. Chromosoma 96:427–33
    [Google Scholar]
  36. 36.
    Klippel A, Cloppenborg K, Kahmann R. 1988. Isolation and characterization of unusual gin mutants. EMBO J 7:3983–89
    [Google Scholar]
  37. 37.
    Klippel A, Kanaar R, Kahmann R, Cozzarelli NR. 1993. Analysis of strand exchange and DNA binding of enhancer-independent Gin recombinase mutants. EMBO J 12:1047–57
    [Google Scholar]
  38. 38.
    Koch C, Vandekerckhove J, Kahmann R. 1988. Escherichia coli host factor for site-specific DNA inversion: cloning and characterization of the fis gene. PNAS 85:4237–41
    [Google Scholar]
  39. 39.
    Kostrewa D, Granzin J, Koch C, Choe H-W, Raghunathan S et al. 1991. Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature 349:178–80
    [Google Scholar]
  40. 40.
    Kronstad J. 2003. Castles and cuitlacoche: the first international Ustilago conference. Fungal Genet. Biol. 38:265–71
    [Google Scholar]
  41. 41.
    Kronstad J, Leong S. 1989. Isolation of two alleles of the b locus of Ustilago maydis. PNAS 86:978–82
    [Google Scholar]
  42. 42.
    Krüger J, Loubradou G, Wanner G, Regenfelder E, Feldbrügge M, Kahmann R. 2000. Activation of the cAMP pathway in Ustilago maydis reduces fungal proliferation and teliospore formation in plant tumors. Mol. Plant Microbe Interact. 13:1034–40
    [Google Scholar]
  43. 43.
    Kües U, Richardson W, Tymon AM, Mutasa ES, Göttgens B et al. 1992. The combination of dissimilar alleles of the and gene complexes, whose proteins contain homeo domain motifs, determines sexual development in the mushroom Coprinus cinereus. Genes Dev 6:568–77
    [Google Scholar]
  44. 44.
    Lanver D, Berndt P, Tollot M, Naik V, Vranes M et al. 2014. Plant surface cues prime Ustilago maydis for biotrophic development. PLOS Pathog 10:e1004272
    [Google Scholar]
  45. 45.
    Lanver D, Mendoza-Mendoza A, Brachmann A, Kahmann R. 2010. Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22:2085–101
    [Google Scholar]
  46. 46.
    Lanver D, Müller AN, Happel P, Schweizer G, Haas FB et al. 2018. The biotrophic development of Ustilago maydis studied by RNA-seq analysis. Plant Cell 30:300–23
    [Google Scholar]
  47. 47.
    Lanver D, Tollot M, Schweizer G, Lo Presti L, Reissmann S et al. 2017. Ustilago maydis effectors and their impact on virulence. Nat. Rev. Microbiol. 15:409–21
    [Google Scholar]
  48. 48.
    Liang L. 2013. The role of Stp1, a secreted effector, in the biotrophic interaction of Ustilago maydis and its host plant maize PhD Thesis Philipps-Universität Marburg
    [Google Scholar]
  49. 49.
    Lin JS, Happel P, Kahmann R. 2021. Nuclear status and leaf tumor formation in the Ustilago maydis–maize pathosystem. New Phytol 231:399–415
    [Google Scholar]
  50. 50.
    Lo Presti L, Kahmann R 2017. How filamentous plant pathogen effectors are translocated to host cells. Curr. Opin. Plant Biol. 38:19–24
    [Google Scholar]
  51. 51.
    Lo Presti L, Zechmann B, Kumlehn J, Liang L, Lanver D et al. 2017. An assay for entry of secreted fungal effectors into plant cells. New Phytol 213:956–64
    [Google Scholar]
  52. 52.
    Ludwig N, Reissmann S, Schipper K, Gonzalez C, Assmann D et al. 2021. A cell surface-exposed protein complex with an essential virulence function in Ustilago maydis. Nat. Microbiol. 6:722–30
    [Google Scholar]
  53. 53.
    Ma L-S, Wang L, Trippel C, Mendoza-Mendoza A, Ullmann S et al. 2018. The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins. Nat. Commun. 9:1–15
    [Google Scholar]
  54. 54.
    Maeser S, Kahmann R. 1991. The Gin recombinase of phage Mu can catalyse site-specific recombination in plant protoplasts. Mol. Gen. Genet. 230:170–76
    [Google Scholar]
  55. 55.
    Mendoza-Mendoza A, Berndt P, Djamei A, Weise C, Linne U et al. 2009. Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol. Microbiol. 71:895–911
    [Google Scholar]
  56. 56.
    Mertens G, Hoffmann A, Blöcker H, Frank R, Kahmann R. 1984. Gin-mediated site-specific recombination in bacteriophage Mu DNA: overproduction of the protein and inversion in vitro. EMBO J 3:2415–21
    [Google Scholar]
  57. 57.
    Molina L, Kahmann R. 2007. An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19:2293–309
    [Google Scholar]
  58. 58.
    Müller P, Aichinger C, Feldbrügge M, Kahmann R. 1999. The MAP kinase kpp2 regulates mating and pathogenic development in Ustilago maydis. Mol. Microbiol. 34:1007–17
    [Google Scholar]
  59. 59.
    Müller P, Weinzierl G, Brachmann A, Feldbrügge M, Kahmann R. 2003. Mating and pathogenic development of the smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot. Cell 2:1187–99
    [Google Scholar]
  60. 60.
    Puhalla JE. 1968. Compatibility reactions on solid medium and interstrain inhibition in Ustilago maydis. Genetics 60:461
    [Google Scholar]
  61. 61.
    Puhalla JE. 1970. Genetic studies of the b incompatability locus of Ustilago maydis. Genet. Res. 16:229–32
    [Google Scholar]
  62. 62.
    Rizzi YS, Happel P, Lenz S, Urs MJ, Bonin M et al. 2021. Chitosan and chitin deacetylase activity are necessary for development and virulence of Ustilago maydis. mBio 12:e03419–20
    [Google Scholar]
  63. 63.
    Romeis T, Brachmann A, Kahmann R, Kämper J. 2000. Identification of a target gene for the bE–bW homeodomain protein complex in Ustilago maydis. Mol. Microbiol. 37:54–66
    [Google Scholar]
  64. 64.
    Romeis T, Kämper J, Kahmann R. 1997. Single-chain fusions of two unrelated homeodomain proteins trigger pathogenicity in Ustilago maydis. PNAS 94:1230–34
    [Google Scholar]
  65. 65.
    Rowell JB. 1955. Functional role of compatibility factors and an in vitro test for sexual compatibility with haploid lines of Ustilago zeae. Phytopathology 45:370–74
    [Google Scholar]
  66. 66.
    Rowell JB, Devay JE. 1954. Genetics of Ustilago zeae in relation to basic problems of its pathogenicity. Phytopathology 44:356–62
    [Google Scholar]
  67. 67.
    Schipper K. 2009. Charakterisierung eines Ustilago maydis Genclusters, das für drei neuartige sekretierte Effektoren kodiert PhD Thesis Philipps-Universität Marburg
    [Google Scholar]
  68. 68.
    Schirawski J, Böhnert HU, Steinberg G, Snetselaar K, Adamikowa L, Kahmann R. 2005. Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17:3532–43
    [Google Scholar]
  69. 69.
    Schirawski J, Mannhaupt G, Münch K, Brefort T, Schipper K et al. 2010. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330:1546–48
    [Google Scholar]
  70. 70.
    Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer W et al. 1990. The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60:295–306
    [Google Scholar]
  71. 71.
    Seiler A, Blöcker H, Frank R, Kahmann R. 1986. The mom gene of bacteriophage Mu: the mechanism of methylation-dependent expression. EMBO J 5:2719–28
    [Google Scholar]
  72. 72.
    Specht CA, Stankis MM, Giasson L, Novotny CP, Ullrich RC. 1992. Functional analysis of the homeodomain-related proteins of the locus of Schizophyllum commune. PNAS 89:7174–78
    [Google Scholar]
  73. 73.
    Spellig T, Bottin A, Kahmann R. 1996. Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252:503–9
    [Google Scholar]
  74. 74.
    Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J et al. 2014. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife 3:e01355
    [Google Scholar]
  75. 75.
    Tanaka S, Gollin I, Rössel N, Kahmann R. 2020. The functionally conserved effector Sta1 is a fungal cell wall protein required for virulence in Ustilago maydis. New Phytol 227:185–99
    [Google Scholar]
  76. 76.
    Tanaka S, Schweizer G, Rössel N, Fukada F, Thines M, Kahmann R. 2019. Neofunctionalization of the secreted Tin2 effector in the fungal pathogen Ustilago maydis. Nat. Microbiol. 4:251–57
    [Google Scholar]
  77. 77.
    Tollot M, Assmann D, Becker C, Altmüller J, Dutheil JY et al. 2016. The WOPR protein Ros1 is a master regulator of sporogenesis and late effector gene expression in the maize pathogen Ustilago maydis. PLOS Pathog 12:e1005697
    [Google Scholar]
  78. 78.
    Wang J, Holden DW, Leong SA. 1988. Gene transfer system for the phytopathogenic fungus Ustilago maydis. PNAS 85:865–69
    [Google Scholar]
  79. 79.
    Wulczyn FG, Bölker M, Kahmann R. 1989. Translation of the bacteriophage Mu mom gene is positively regulated by the phage com gene product. Cell 57:1201–10
    [Google Scholar]
  80. 80.
    Wulczyn FG, Kahmann R. 1991. Translational stimulation: RNA sequence and structure requirements for binding of Com protein. Cell 65:259–69
    [Google Scholar]
  81. 81.
    Zuo W, Ökmen B, Depotter JR, Ebert MK, Redkar A et al. 2019. Molecular interactions between smut fungi and their host plants. Annu. Rev. Phytopathol. 57:411–30
    [Google Scholar]
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