Publikationsserver der Universitätsbibliothek Marburg

Titel:Sensing and degradation of the plant defence hormone salicylic acid by the biotrophic fungus Ustilago maydis
Autor:Rabe, Franziska
Weitere Beteiligte: Kahmann, Regine (Prof. Dr.)
Veröffentlicht:2016
URI:https://archiv.ub.uni-marburg.de/diss/z2016/0663
DOI: https://doi.org/10.17192/z2016.0663
URN: urn:nbn:de:hebis:04-z2016-06636
DDC: Biowissenschaften, Biologie
Titel (trans.):Perzeption und Abbau des Pflanzenabwehrhormons Salicylsäure durch den biotrophen Pilz Ustilago maydis
Publikationsdatum:2016-10-05
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Biologie, Ustilago, salicylate hydroxylase, Pflanzenpathogen, Zink-Cluster-Transkriptionsfaktor, Salicylic acid, Salicylsäure, Ustilago, zinc cluster transcription factor, maize, Mais, Salizylathydroxylase

Summary:
Salicylic acid (SA) belongs to the class of phenolic compounds and is composed of an aromatic ring with one carboxyl- and one hydroxyl group. In plants, it is a key signalling molecule for the regulation of local and systemic defence responses against biotrophic plant pathogens. One model organism to study biotrophic pathogens is Ustilago maydis, the causative agent of corn smut disease. U. maydis employs strategies to interfere with SA production and SA-associated signalling of its host Zea mays. These strategies are considered to supress defence responses and thereby contribute to a successful infection. Moreover, the U. maydis genome encodes three putative salicylate hydroxylases, UMAG_05230, UMAG_03408, and UMAG_05967, which are predicted to degrade SA. For one of these proteins, UMAG_05230 (Shy1), salicylate hydroxylase activity could already be experimentally confirmed. Based on the predicted enzymatic function of these proteins, it was hypothesized that by eliminating SA they could contribute to the suppression of host immunity. To provide insights into the biological role of SA degradation by salicylate hydroxylases in U. maydis, the functional characterization of these genes was continued in this study. It could be demonstrated that U. maydis is able to use SA as carbon source and that Shy1 is essential for SA utilization. Besides shy1 and the second salicylate hydroxylase-related gene UMAG_03408, which were previously shown to be induced during infection, also the third gene of this family, UMAG_05967, was strongly upregulated in these developmental stages. However, although induced during biotrophic growth, no involvement in virulence could be shown for these three genes. Transcriptional profiling revealed that shy1 and the two salicylate hydroxylase-related genes are induced in presence of SA, indicating that U. maydis is able to sense SA. To provide insights into the molecular mechanism of SA perception and signalling, a forward genetic screen was performed. This screen led to the identification of one key regulator for SA sensing, the binuclear zinc cluster transcription factor Rss1. Rss1 is important for SA sensing and modulates the expression of genes that are needed to metabolise SA and tryptophan. Rss1 most likely acts concomitantly as SA sensor and transcriptional activator. Although Rss1 is important for the regulation of SA-responsive genes in axenic culture, transcriptional profiling data provided evidence that additional cues and pathways could exist that regulate these genes during plant colonization. Moreover, virulence assays with rss1 deletion mutants showed that the deletion of rss1 had no impact on virulence in seedling infections.

Bibliographie / References

  1. Jones, A. M., Danielson, J. A., Manojkumar, S. N., Lanquar, V., Grossmann, G., and Frommer, W. B. (2014). Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. Elife 3, e01741.
  2. Kamoun, S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44, 41-60.
  3. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E., and Ryals, J. (1994). A central role of salicylic Acid in plant disease resistance. Science 266, 1247-50.
  4. Rudrappa, T., Quinn, W. J., Stanley-Wall, N. R., and Bais, H. P. (2007). A degradation product of the salicylic acid pathway triggers oxidative stress resulting in down-regulation of Bacillus subtilis biofilm formation on Arabidopsis thaliana roots. Planta 226, 283-97.
  5. DePristo, M. A., Banks, E., Poplin, R., Garimella, K. V., Maguire, J. R., Hartl, C., Philippakis, A. A., del Angel, G., Rivas, M. A., Hanna, M., McKenna, A., Fennell, T. J., Kernytsky, A. M., Sivachenko, A. Y., Cibulskis, K., Gabriel, S. B., Altshuler, D., and Daly, M. J. (2011). A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43, 491- 8.
  6. MacPherson, S., Larochelle, M., and Turcotte, B. (2006). A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70, 583-604.
  7. McCann, M. P., and Snetselaar, K. M. (2008). A genome-based analysis of amino acid metabolism in the biotrophic plant pathogen Ustilago maydis. Fungal Genet Biol 45 Suppl 1, S77-87.
  8. Shulaev, V., Silverman, P., and Raskin, I. (1997). Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385, 718-721.
  9. Liu, P. P., Yang, Y., Pichersky, E., and Klessig, D. F. (2010). Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in arabidopsis. Mol Plant Microbe Interact 23, 82-90.
  10. van der Linde, K., Hemetsberger, C., Kastner, C., Kaschani, F., van der Hoorn, R. A., Kumlehn, J., and Doehlemann, G. (2012). A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell 24, 1285-300.
  11. Struck, C. (2015). Amino acid uptake in rust fungi. Front Plant Sci 6, 40.
  12. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-8.
  13. Schornack, S., van Damme, M., Bozkurt, T. O., Cano, L. M., Smoker, M., Thines, M., Gaulin, E., Kamoun, S., and Huitema, E. (2010). Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci U S A 107, 17421-6.
  14. Hellauer, K., Rochon, M. H., and Turcotte, B. (1996). A novel DNA binding motif for yeast zinc cluster proteins: the Leu3p and Pdr3p transcriptional activators recognize everted repeats. Mol Cell Biol 16, 6096-102.
  15. Wahl, R., Wippel, K., Goos, S., Kamper, J., and Sauer, N. (2010). A novel highaffinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8, e1000303.
  16. Thakur, J. K., Arthanari, H., Yang, F., Pan, S. J., Fan, X., Breger, J., Frueh, D. P., Gulshan, K., Li, D. K., Mylonakis, E., Struhl, K., Moye-Rowley, W. S., Cormack, B. P., Wagner, G., and Naar, A. M. (2008). A nuclear receptor-like pathway regulating multidrug resistance in fungi. Nature 452, 604-9.
  17. Engler, C., Kandzia, R., and Marillonnet, S. (2008). A one pot, one step, precision cloning method with high throughput capability. PLoS One 3, e3647.
  18. Kamper, J. (2004). A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics 271, 103-10.
  19. Sarris, P. F., Duxbury, Z., Huh, S. U., Ma, Y., Segonzac, C., Sklenar, J., Derbyshire, P., Cevik, V., Rallapalli, G., Saucet, S. B., Wirthmueller, L., Menke, F. L., Sohn, K. H., and Jones, J. D. (2015). A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors. Cell 161, 1089-100.
  20. Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M., van der Hoorn, R. A., and Kamoun, S. (2009). Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci U S A 106, 1654-9.
  21. Le Roux, C., Huet, G., Jauneau, A., Camborde, L., Tremousaygue, D., Kraut, A., Zhou, B., Levaillant, M., Adachi, H., Yoshioka, H., Raffaele, S., Berthome, R., Coute, Y., Parker, J. E., and Deslandes, L. (2015). A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161, 1074-88.
  22. Redkar, A., Hoser, R., Schilling, L., Zechmann, B., Krzymowska, M., Walbot, V., and Doehlemann, G. (2015). A Secreted Effector Protein of Ustilago maydis Guides Maize Leaf Cells to Form Tumors. Plant Cell 27, 1332-51.
  23. Tanaka, S., Brefort, T., Neidig, N., Djamei, A., Kahnt, J., Vermerris, W., Koenig, S., Feussner, K., Feussner, I., and Kahmann, R. (2014). A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. Elife 3, e01355.
  24. Hoffman, C. S., and Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of E. coli. Gene 57, 267-272.
  25. Gillissen, B., Bergemann, J., Sandmann, C., Schroeer, B., Bolker, M., and Kahmann, R. (1992). A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68, 647-57.
  26. Gorlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K. H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H., and Ryals, J. (1996). Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8, 629-43.
  27. Gohre, V., and Robatzek, S. (2008). Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46, 189-215.
  28. Dobson, P. D., and Kell, D. B. (2008). Carrier-mediated cellular uptake of pharmaceutical drugs: an exception or the rule? Nat Rev Drug Discov 7, 205-20.
  29. Deslandes, L., and Rivas, S. (2012). Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 17, 644-55.
  30. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H., and Shibuya, N. (2007). CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104, 19613-8.
  31. Mrozik, A., Labuzek, S., and Piotrowska-Seget, Z. (2005). Changes in fatty acid composition in Pseudomonas putida and Pseudomonas stutzeri during naphthalene degradation. Microbiol Res 160, 149-57.
  32. Garcion, C., Lohmann, A., Lamodiere, E., Catinot, J., Buchala, A., Doermann, P., and Metraux, J. P. (2008). Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol 147, 1279- 87.
  33. Rabe, F. (2011). Charakterisierung zweier putativer Salicylathydroxylasen aus Ustilago maydis. Master's thesis, Philipps-Universität Marburg
  34. Schweigert, N., Zehnder, A. J., and Eggen, R. I. (2001). Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ Microbiol 3, 81-91.
  35. Rooney, H. C., Van't Klooster, J. W., van der Hoorn, R. A., Joosten, M. H., Jones, J. D., and de Wit, P. J. (2005). Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308, 1783-6.
  36. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-5.
  37. Nourani, A., Papajova, D., Delahodde, A., Jacq, C., and Subik, J. (1997). Clustered amino acid substitutions in the yeast transcription regulator Pdr3p increase pleiotropic drug resistance and identify a new central regulatory domain. Mol Gen Genet 256, 397-405.
  38. Katsir, L., Schilmiller, A. L., Staswick, P. E., He, S. Y., and Howe, G. A. (2008). COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105, 7100-5.
  39. Mueller, A. N., Ziemann, S., Treitschke, S., Assmann, D., and Doehlemann, G. (2013). Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog 9, e1003177.
  40. Taniguti, L. M., Schaker, P. D., Benevenuto, J., Peters, L. P., Carvalho, G., Palhares, A., Quecine, M. C., Nunes, F. R., Kmit, M. C., Wai, A., Hausner, G., Aitken, K. S., Berkman, P. J., Fraser, J. A., Moolhuijzen, P. M., Coutinho, L. L., Creste, S., Vieira, M. L., Kitajima, J. P., and Monteiro-Vitorello, C. B. (2015). Complete Genome Sequence of Sporisorium scitamineum and Biotrophic Interaction Transcriptome with Sugarcane. PLoS One 10, e0129318.
  41. de Jonge, R., van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., van der Krol, S., Shibuya, N., Joosten, M. H., and Thomma, B. P. (2010). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953-5.
  42. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43, 205-27.
  43. Day, P. R., and Anagnostakis, S. L. (1971). Corn smut dikaryon in culture. Nat New Biol 231, 19-20.
  44. Flor, H. H. (1971). Current Status of the Gene-for-Gene Concept. Annu Rev Phytopathol 9, 275-296.
  45. Heil, M., and Land, W. G. (2014). Danger signals - damaged-self recognition across the tree of life. Front Plant Sci 5, 578.
  46. Garcia-Pedrajas, M. D., Nadal, M., Kapa, L. B., Perlin, M. H., Andrews, D. L., and Gold, S. E. (2008). DelsGate, a robust and rapid gene deletion construction method. Fungal Genet Biol 45, 379-88.
  47. Schell, M. A., and Poser, E. F. (1989). Demonstration, characterization, and mutational analysis of NahR protein binding to nah and sal promoters. J Bacteriol 171, 837- 46.
  48. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98, 503-17.
  49. Vernooij, B., Friedrich, L., Ahl Goy, P., Staub, T., Kessmann, H., and Ryals, J. (1995). 2,6-Dichloroisonicotinic Acid-Induced Resistance to Pathogens Without the Accumulation of Salicylic Acid. MPMI 8, 228-234.
  50. Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chainterminating inhibitors. Proc Natl Acad Sci U S A 74, 5463-7.
  51. Qi, P. F., Johnston, A., Balcerzak, M., Rocheleau, H., Harris, L. J., Long, X. Y., Wei, Y. M., Zheng, Y. L., and Ouellet, T. (2012). Effect of salicylic acid on Fusarium graminearum, the major causal agent of fusarium head blight in wheat. Fungal Biol 116, 413-26.
  52. Rice, P., Longden, I., and Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16, 276-7.
  53. Terfruchte, M., Joehnk, B., Fajardo-Somera, R., Braus, G. H., Riquelme, M., Schipper, K., and Feldbrugge, M. (2014). Establishing a versatile Golden Gate cloning system for genetic engineering in fungi. Fungal Genet Biol 62, 1-10.
  54. Doehlemann, G., Wahl, R., Vranes, M., de Vries, R. P., Kamper, J., and Kahmann, R. (2008). Establishment of compatibility in the Ustilago maydis/maize pathosystem. J Plant Physiol 165, 29-40.
  55. Todd, R. B., and Andrianopoulos, A. (1997). Evolution of a fungal regulatory gene family: the Zn(II)2Cys6 binuclear cluster DNA binding motif. Fungal Genet Biol 21, 388-405.
  56. Sun, J., Phillips, C. M., Anderson, C. T., Beeson, W. T., Marletta, M. A., and Glass, N. L. (2011). Expression and characterization of the Neurospora crassa endoglucanase GH5-1. Protein Expr Purif 75, 147-54.
  57. Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with BurrowsWheeler transform. Bioinformatics 25, 1754-60.
  58. Waadt, R., Hitomi, K., Nishimura, N., Hitomi, C., Adams, S. R., Getzoff, E. D., and Schroeder, J. I. (2014). FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. Elife 3, e01739.
  59. van der Hoorn, R. A., and Kamoun, S. (2008). From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009-17.
  60. Vollmeister, E., Schipper, K., Baumann, S., Haag, C., Pohlmann, T., Stock, J., and Feldbrugge, M. (2012). Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev 36, 59-77.
  61. Lo Presti, L., Lanver, D., Schweizer, G., Tanaka, S., Liang, L., Tollot, M., Zuccaro, A., Reissmann, S., and Kahmann, R. (2015). Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66, 513-45.
  62. Schweizer, P., Buchala, A., and Metraux, J. P. (1997). Gene-Expression Patterns and Levels of Jasmonic Acid in Rice Treated with the Resistance Inducer 2,6- Dichloroisonicotinic Acid. Plant Physiol 115, 61-70.
  63. Kemen, E., Gardiner, A., Schultz-Larsen, T., Kemen, A. C., Balmuth, A. L., RobertSeilaniantz, A., Bailey, K., Holub, E., Studholme, D. J., Maclean, D., and Jones, J. D. (2011). Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol 9, e1001094.
  64. Sharma, R., Mishra, B., Runge, F., and Thines, M. (2014). Gene loss rather than gene gain is associated with a host jump from monocots to dicots in the Smut Fungus Melanopsichium pennsylvanicum. Genome Biol Evol 6, 2034-49.
  65. Kuswandi, C. F. R. (1992). Genetic control of the protocatechuic acid pathway in Aspergillus nidulans. J Gen Microbiol 138, 817-823.
  66. Rowell, J. B., and DeVay, J. E. (1954). Genetics of Ustilago zeae in relation to basic problems of its pathogenicity. Phytopathology, 356-362.
  67. Ternes, C. M., and Schonknecht, G. (2014). Gene transfers shaped the evolution of de novo NAD+ biosynthesis in eukaryotes. Genome Biol Evol 6, 2335-49.
  68. Laurie, J. D., Ali, S., Linning, R., Mannhaupt, G., Wong, P., Guldener, U., Munsterkotter, M., Moore, R., Kahmann, R., Bakkeren, G., and Schirawski, J. (2012). Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24, 1733-45.
  69. Schuster, M., Schweizer, G., Reissmann, S., and Kahmann, R. (2015). Genome editing in Ustilago maydis using the CRISPR-Cas system. Fungal Genet Biol 89, 3-9.
  70. Soanes, D. M., Chakrabarti, A., Paszkiewicz, K. H., Dawe, A. L., and Talbot, N. J. (2012). Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog 8, e1002514.
  71. Kumar, D., and Klessig, D. F. (2003). High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci U S A 100, 16101-6.
  72. Pieterse, C. M., Van der Does, D., Zamioudis, C., Leon-Reyes, A., and Van Wees, S. C. (2012). Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28, 489-521.
  73. Grant, M. R., and Jones, J. D. (2009). Hormone (dis)harmony moulds plant health and disease. Science 324, 750-2.
  74. Petre, B., and Kamoun, S. (2014). How do filamentous pathogens deliver effector proteins into plant cells? PLoS Biol 12, e1001801.
  75. Spoel, S. H., and Dong, X. (2012). How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12, 89-100.
  76. Schuler, D., Wahl, R., Wippel, K., Vranes, M., Munsterkotter, M., Sauer, N., and Kamper, J. (2015). Hxt1, a monosaccharide transporter and sensor required for virulence of the maize pathogen Ustilago maydis. New Phytol 206, 1086-100.
  77. Suzuki, K., Mizuguchi, M., Gomi, T., and Itagaki, E. (1995). Identification of a lysine residue in the NADH-binding site of salicylate hydroxylase from Pseudomonas putida S-1. J Biochem 117, 579-85.
  78. Eppink, M. H., Schreuder, H. A., and Van Berkel, W. J. (1997). Identification of a novel conserved sequence motif in flavoprotein hydroxylases with a putative dual function in FAD/NAD(P)H binding. Protein Sci 6, 2454-8.
  79. Du, H., and Klessig, D. F. (1997). Identification of a Soluble, High-Affinity Salicylic Acid-Binding Protein in Tobacco. Plant Physiol 113, 1319-1327.
  80. Vlot, A. C., Liu, P. P., Cameron, R. K., Park, S. W., Yang, Y., Kumar, D., Zhou, F., Padukkavidana, T., Gustafsson, C., Pichersky, E., and Klessig, D. F. (2008). Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56, 445- 56.
  81. Metraux, J. P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., and Inverardi, B. (1990). Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004-6.
  82. Morris, S. W., Vernooij, B., Titatarn, S., Starrett, M., Thomas, S., Wiltse, C. C., Frederiksen, R. A., Bhandhufalck, A., Hulbert, S., and Uknes, S. (1998). Induced resistance responses in maize. Mol Plant Microbe Interact 11, 643-58.
  83. Mou, Z., Fan, W., and Dong, X. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-44.
  84. Durner, J., and Klessig, D. F. (1995). Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci U S A 92, 11312-6.
  85. Kamper, J., Kahmann, R., Bolker, M., Ma, L. J., Brefort, T., Saville, B. J., Banuett, F., Kronstad, J. W., Gold, S. E., Muller, O., Perlin, M. H., Wosten, H. A., de Vries, R., Ruiz-Herrera, J., Reynaga-Pena, C. G., Snetselaar, K., McCann, M., Perez-Martin, J., Feldbrugge, M., Basse, C. W., Steinberg, G., Ibeas, J. I., Holloman, W., Guzman, P., Farman, M., Stajich, J. E., Sentandreu, R., Gonzalez-Prieto, J. M., Kennell, J. C., Molina, L., Schirawski, J., MendozaMendoza, A., Greilinger, D., Munch, K., Rossel, N., Scherer, M., Vranes, M., Ladendorf, O., Vincon, V., Fuchs, U., Sandrock, B., Meng, S., Ho, E. C., Cahill, M. J., Boyce, K. J., Klose, J., Klosterman, S. J., Deelstra, H. J., OrtizCastellanos, L., Li, W., Sanchez-Alonso, P., Schreier, P. H., Hauser-Hahn, I., Vaupel, M., Koopmann, E., Friedrich, G., Voss, H., Schluter, T., Margolis, J., Platt, D., Swimmer, C., Gnirke, A., Chen, F., Vysotskaia, V., Mannhaupt, G., Guldener, U., Munsterkotter, M., Haase, D., Oesterheld, M., Mewes, H. W., Mauceli, E. W., DeCaprio, D., Wade, C. M., Butler, J., Young, S., Jaffe, D. B., Calvo, S., Nusbaum, C., Galagan, J., and Birren, B. W. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444, 97-101.
  86. Robinson, J. T., Thorvaldsdottir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., and Mesirov, J. P. (2011). Integrative genomics viewer. Nat Biotechnol 29, 24-6.
  87. Thorvaldsdottir, H., Robinson, J. T., and Mesirov, J. P. (2013). Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14, 178-92.
  88. Hennig, J., Malamy, J., Grynkiewicz, G., Indulski, J., and Klessig, D. F. (1993). Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J 4, 593-600.
  89. Eppink, M. H., Schreuder, H. A., and van Berkel, W. J. (1998). Interdomain binding of NADPH in p-hydroxybenzoate hydroxylase as suggested by kinetic, crystallographic and modeling studies of histidine 162 and arginine 269 variants. J Biol Chem 273, 21031-9.
  90. Kazan, K., and Lyons, R. (2014). Intervention of Phytohormone Pathways by Pathogen Effectors. Plant Cell 26, 2285-2309.
  91. Singh, L. (1978). In vitro screening of some chemicals against three phytopathogenic fungi. J. lndian Bot. Soc. 57, 191-195.
  92. Meyer, J. M., Azelvandre, P., and Georges, C. (1992). Iron metabolism in Pseudomonas: salicylic acid, a siderophore of Pseudomonas fluorescens CHAO. Biofactors 4, 23-7.
  93. Visca, P., Ciervo, A., Sanfilippo, V., and Orsi, N. (1993). Iron-regulated salicylate synthesis by Pseudomonas spp. J Gen Microbiol 139, 1995-2001.
  94. Tsukuda, T., Carleton, S., Fotheringham, S., and Holloman, W. K. (1988). Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol Cell Biol 8, 3703-9.
  95. Snetselaar, K. (1994). Light and electron microscopy of Ustilago maydis hyphae in maize. Mycologica 98, 347-355.
  96. Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., and Smyth, G. K. (2015). limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43, e47.
  97. Skibbe, D. S., Doehlemann, G., Fernandes, J., and Walbot, V. (2010). Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328, 89-92.
  98. Linning, R., Lin, D., Lee, N., Abdennadher, M., Gaudet, D., Thomas, P., Mills, D., Kronstad, J. W., and Bakkeren, G. (2004). Marker-based cloning of the region containing the UhAvr1 avirulence gene from the basidiomycete barley pathogen Ustilago hordei. Genetics 166, 99-111.
  99. Djamei, A., Schipper, K., Rabe, F., Ghosh, A., Vincon, V., Kahnt, J., Osorio, S., Tohge, T., Fernie, A. R., Feussner, I., Feussner, K., Meinicke, P., Stierhof, Y. D., Schwarz, H., Macek, B., Mann, M., and Kahmann, R. (2011). Metabolic priming by a secreted fungal effector. Nature 478, 395-8.
  100. Dodge, A. G., and Wackett, L. P. (2005). Metabolism of bismuth subsalicylate and intracellular accumulation of bismuth by Fusarium sp. strain BI. Appl Environ Microbiol 71, 876-82.
  101. Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D. F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113-6.
  102. Peng, R. H., Xiong, A. S., Xue, Y., Fu, X. Y., Gao, F., Zhao, W., Tian, Y. S., and Yao, Q. H. (2008). Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32, 927-55.
  103. Tanaka, S., Han, X., and Kahmann, R. (2015). Microbial effectors target multiple steps in the salicylic acid production and signaling pathway. Front Plant Sci 6, 349.
  104. Sambrook, J., Frisch, E. F., and Maniatis, T. 1989. Molecular Cloning: A laboratory manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, New York.
  105. Enerson, B. E., and Drewes, L. R. (2003). Molecular features, regulation, and function of monocarboxylate transporters: implications for drug delivery. J Pharm Sci 92, 1531-44.
  106. Kamper, J., Reichmann, M., Romeis, T., Bolker, M., and Kahmann, R. (1995). Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81, 73-83.
  107. Cohen, S. N., Chang, A. C., and Hsu, L. (1972). Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A 69, 2110-4.
  108. Fu, Z. Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., Mohan, R., Spoel, S. H., Tada, Y., Zheng, N., and Dong, X. (2012). NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228-32.
  109. Naar, A. M., and Thakur, J. K. (2009). Nuclear receptor-like transcription factors in fungi. Genes Dev 23, 419-32.
  110. Rao, P. V., Moore, K., and Towers, G. H. (1967). O-pyrocatechiuc acid carboxy-lyase from Aspergillus niger. Arch Biochem Biophys 122, 466-73.
  111. Verberne, M. C., Verpoorte, R., Bol, J. F., Mercado-Blanco, J., and Linthorst, H. J. (2000). Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat Biotechnol 18, 779-83.
  112. Schirawski, J., Mannhaupt, G., Munch, K., Brefort, T., Schipper, K., Doehlemann, G., Di Stasio, M., Rossel, N., Mendoza-Mendoza, A., Pester, D., Muller, O., Winterberg, B., Meyer, E., Ghareeb, H., Wollenberg, T., Munsterkotter, M., Wong, P., Walter, M., Stukenbrock, E., Guldener, U., and Kahmann, R. (2010). Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330, 1546-8.
  113. Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D., and Kahmann, R. (2009). Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5, e1000290.
  114. Schweizer, P., Felix, G., Buchala, A., Muller, C., and Metraux, J. P. (1996). Perception of free cutin monomers by plant cells. Plant Journal 10, 331-341.
  115. Rechsteiner, M., and Rogers, S. W. (1996). PEST sequences and regulation by proteolysis. Trends Biochem Sci 21, 267-71.
  116. Takanaga, H., Tamai, I., and Tsuji, A. (1994). pH-dependent and carrier-mediated transport of salicylic acid across Caco-2 cells. J Pharm Pharmacol 46, 567-70.
  117. Mendoza-Mendoza, A., Berndt, P., Djamei, A., Weise, C., Linne, U., Marahiel, M., Vranes, M., Kamper, J., and Kahmann, R. (2009). Physical-chemical plantderived signals induce differentiation in Ustilago maydis. Mol Microbiol 71, 895- 911.
  118. Darvill, A. G., and Albersheim, P. (1984). Phytoalexins and Their Elicitors - a Defense against Microbial Infection in Plants. Annual Review of Plant Physiology and Plant Molecular Biology 35, 243-275.
  119. Kaffarnik, F., Muller, P., Leibundgut, M., Kahmann, R., and Feldbrugge, M. (2003). PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22, 5817-26.
  120. Santner, A., Calderon-Villalobos, L. I., and Estelle, M. (2009). Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5, 301-7.
  121. Tada, Y., Spoel, S. H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., Zuo, J., and Dong, X. (2008). Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952-6.
  122. Dangl, J. L., and Jones, J. D. (2001). Plant pathogens and integrated defence responses to infection. Nature 411, 826-33.
  123. Felix, G., Duran, J. D., Volko, S., and Boller, T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18, 265-76.
  124. Lanver, D., Berndt, P., Tollot, M., Naik, V., Vranes, M., Warmann, T., Munch, K., Rossel, N., and Kahmann, R. (2014). Plant surface cues prime Ustilago maydis for biotrophic development. PLoS Pathog 10, e1004272.
  125. Delahodde, A., Delaveau, T., and Jacq, C. (1995). Positive autoregulation of the yeast transcription factor Pdr3p, which is involved in control of drug resistance. Mol Cell Biol 15, 4043-51.
  126. Sze, I. S., and Dagley, S. (1984). Properties of salicylate hydroxylase and hydroxyquinol 1,2-dioxygenase purified from Trichosporon cutaneum. J Bacteriol 159, 353-9.
  127. Spoel, S. H., Mou, Z., Tada, Y., Spivey, N. W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137, 860-72.
  128. Romeis, T. (2001). Protein kinases in the plant defence response. Curr Opin Plant Biol 4, 407-14.
  129. Jelenska, J., van Hal, J. A., and Greenberg, J. T. (2010). Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc Natl Acad Sci U S A 107, 13177-82.
  130. Huang, W. E., Huang, L., Preston, G. M., Naylor, M., Carr, J. P., Li, Y., Singer, A. C., Whiteley, A. S., and Wang, H. (2006). Quantitative in situ assay of salicylic acid in tobacco leaves using a genetically modified biosensor strain of Acinetobacter sp. ADP1. Plant J 46, 1073-83.
  131. R Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  132. Rao, P. V., Sreeleela, N. S., Premakumar, R., and Vaidyanathan, C. S. (1971). Regulation of the pathway for the degradation of anthranilate in Aspergillus niger. J Bacteriol 107, 100-5.
  133. Doehlemann, G., Wahl, R., Horst, R. J., Voll, L. M., Usadel, B., Poree, F., Stitt, M., Pons-Kuhnemann, J., Sonnewald, U., Kahmann, R., and Kamper, J. (2008b). Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56, 181-95.
  134. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J. (1993). Requirement of salicylic Acid for the induction of systemic acquired resistance. Science 261, 754-6.
  135. Kerbarh, O., Ciulli, A., Howard, N. I., and Abell, C. (2005). Salicylate biosynthesis: overexpression, purification, and characterization of Irp9, a bifunctional salicylate synthase from Yersinia enterocolitica. J Bacteriol 187, 5061-6.
  136. Penn, C. D., and Daniel, S. L. (2013). Salicylate degradation by the fungal plant pathogen Sclerotinia sclerotiorum. Curr Microbiol 67, 218-25.
  137. Katagiri, M., Maeno, H., Yamamoto, S., Hayaishi, O., Kitao, T., and Oae, S. (1965). Salicylate Hydroxylase, a Monooxygenase Requiring Flavin Adenine Dinucleotide. Ii. The Mechanism of Salicylate Hydroxylation to Catechol. J Biol Chem 240, 3414-7.
  138. Malamy, J., Carr, J. P., Klessig, D. F., and Raskin, I. (1990). Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002-4.
  139. Vlot, A. C., Dempsey, D. A., and Klessig, D. F. (2009). Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47, 177-206.
  140. Rocher, F., Chollet, J. F., Jousse, C., and Bonnemain, J. L. (2006). Salicylic acid, an ambimobile molecule exhibiting a high ability to accumulate in the phloem. Plant Physiol 141, 1684-93.
  141. Rivas-San Vicente, M., and Plasencia, J. (2011). Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62, 3321-38.
  142. Dempsey, D. A., Vlot, A. C., Wildermuth, M. C., and Klessig, D. F. (2011). Salicylic Acid biosynthesis and metabolism. Arabidopsis Book 9, e0156.
  143. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E., Uknes, S., Kessmann, H., and Ryals, J. (1994). Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. Plant Cell 6, 959-965.
  144. De Meyer, G., and Hofte, M. (1997). Salicylic Acid Produced by the Rhizobacterium Pseudomonas aeruginosa 7NSK2 Induces Resistance to Leaf Infection by Botrytis cinerea on Bean. Phytopathology 87, 588-93.
  145. Seyfferth, C., and Tsuda, K. (2014). Salicylic acid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming. Front Plant Sci 5, 697.
  146. Rocher, F., Chollet, J. F., Legros, S., Jousse, C., Lemoine, R., Faucher, M., Bush, D. R., and Bonnemain, J. L. (2009). Salicylic acid transport in Ricinus communis involves a pH-dependent carrier system in addition to diffusion. Plant Physiol 150, 2081-91.
  147. Jones, A. M., Lindow, S. E., and Wildermuth, M. C. (2007). Salicylic acid, yersiniabactin, and pyoverdin production by the model phytopathogen Pseudomonas syringae pv. tomato DC3000: synthesis, regulation, and impact on tomato and Arabidopsis host plants. J Bacteriol 189, 6773-86.
  148. Neilands, J. B. (1995). Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270, 26723-6.
  149. Shah, J., Chaturvedi, R., Chowdhury, Z., Venables, B., and Petros, R. A. (2014). Signaling by small metabolites in systemic acquired resistance. Plant J 79, 645- 58.
  150. Schultz, J., Milpetz, F., Bork, P., and Ponting, C. P. (1998). SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95, 5857-64.
  151. Letunic, I., Doerks, T., and Bork, P. (2015). SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43, D257-60.
  152. Snetselaar, K. M., and Mims, C. W. (1992). Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologica 84, 193-203.
  153. Forouhar, F., Yang, Y., Kumar, D., Chen, Y., Fridman, E., Park, S. W., Chiang, Y., Acton, T. B., Montelione, G. T., Pichersky, E., Klessig, D. F., and Tong, L. (2005). Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci U S A 102, 1773-8.
  154. Serino, L., Reimmann, C., Baur, H., Beyeler, M., Visca, P., and Haas, D. (1995). Structural genes for salicylate biosynthesis from chorismate in Pseudomonas aeruginosa. Mol Gen Genet 249, 217-28.
  155. Hanahan, D. (1983). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557-80.
  156. Fu, Z. Q., and Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64, 839-63.
  157. Ryan, C. A., and Pearce, G. (2003). Systemins: a functionally defined family of peptide signals that regulate defensive genes in Solanaceae species. Proc Natl Acad Sci U S A 100 Suppl 2, 14577-80.
  158. Pajerowska-Mukhtar, K. M., Emerine, D. K., and Mukhtar, M. S. (2013). Tell me more: roles of NPRs in plant immunity. Trends Plant Sci 18, 402-11.
  159. Wu, Y., Zhang, D., Chu, J. Y., Boyle, P., Wang, Y., Brindle, I. D., De Luca, V., and Despres, C. (2012). The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1, 639-47.
  160. Moreau, M., Westlake, T., Zampogna, G., Popescu, G., Tian, M., Noutsos, C., and Popescu, S. (2013). The Arabidopsis oligopeptidases TOP1 and TOP2 are salicylic acid targets that modulate SA-mediated signaling and the immune response. Plant J 76, 603-14.
  161. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schafer, W., Martin, T., Herskowitz, I., and Kahmann, R. (1990). The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60, 295-306.
  162. van Esse, H. P., Van't Klooster, J. W., Bolton, M. D., Yadeta, K. A., van Baarlen, P., Boeren, S., Vervoort, J., de Wit, P. J., and Thomma, B. P. (2008). The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20, 1948-63.
  163. Tian, M., von Dahl, C. C., Liu, P. P., Friso, G., van Wijk, K. J., and Klessig, D. F. (2012). The combined use of photoaffinity labeling and surface plasmon resonance-based technology identifies multiple salicylic acid-binding proteins. Plant J 72, 1027-38.
  164. Di Stasio, M., Brefort, T., Mendoza-Mendoza, A., Munch, K., and Kahmann, R. (2009). The dual specificity phosphatase Rok1 negatively regulates mating and pathogenicity in Ustilago maydis. Mol Microbiol 73, 73-88.
  165. Saint-Pierre, B., Miville, L., and Dion, P. (1984). The effects of salicylates on phenomena related to crown gall. Can. J. Bot. 62, 729-734.
  166. Hazelwood, L. A., Daran, J. M., van Maris, A. J., Pronk, J. T., and Dickinson, J. R. (2008). The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74, 2259-66.
  167. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Guldener, U., Mannhaupt, G., Munsterkotter, M., and Mewes, H. W. (2004). The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32, 5539-45.
  168. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. (2004). The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16, 3496-507.
  169. Solomon, P. S., Tan, K. C., and Oliver, R. P. (2003). The nutrient supply of pathogenic fungi; a fertile field for study. Mol Plant Pathol 4, 203-10.
  170. Martins, T. M., Hartmann, D. O., Planchon, S., Martins, I., Renaut, J., and Silva Pereira, C. (2015). The old 3-oxoadipate pathway revisited: new insights in the Mauch, F., Mauch-Mani, B., Gaille, C., Kull, B., Haas, D., and Reimmann, C. (2001). Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. Plant J 25, 67-77.
  171. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-9.
  172. Hawkins, A. R., Lamb, H. K., Moore, J. D., Charles, I. G., and Roberts, C. F. (1993). The pre-chorismate (shikimate) and quinate pathways in filamentous fungi: theoretical and practical aspects. J Gen Microbiol 139, 2891-9.
  173. Klessig, D. F., and Malamy, J. (1994). The salicylic acid signal in plants. Plant Mol Biol 26, 1439-58.
  174. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., and Genome Project Data Processing, S. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-9.
  175. Halestrap, A. P., and Meredith, D. (2004). The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 447, 619-28.
  176. Heimel, K., Scherer, M., Vranes, M., Wahl, R., Pothiratana, C., Schuler, D., Vincon, V., Finkernagel, F., Flor-Parra, I., and Kamper, J. (2010). The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog 6, e1001035.
  177. Khrunyk, Y., Munch, K., Schipper, K., Lupas, A. N., and Kahmann, R. (2010). The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. New Phytol 187, 957-68.
  178. Hemetsberger, C., Herrberger, C., Zechmann, B., Hillmer, M., and Doehlemann, G. (2012). The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 8, e1002684.
  179. Shelest, E. (2008). Transcription factors in fungi. FEMS Microbiol Lett 286, 145-51.
  180. Kradolfer, P., Niederberger, P., and Hutter, R. (1982). Tryptophan degradation in Saccharomyces cerevisiae: characterization of two aromatic aminotransferases. Arch Microbiol 133, 242-8.
  181. Flokova, K., Tarkowska, D., Miersch, O., Strnad, M., Wasternack, C., and Novak, O. (2014). UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105, 147-57.
  182. Liu, T., Song, T., Zhang, X., Yuan, H., Su, L., Li, W., Xu, J., Liu, S., Chen, L., Chen, T., Zhang, M., Gu, L., Zhang, B., and Dou, D. (2014). Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun 5, 4686.
  183. Schell, M. A., Brown, P. H., and Raju, S. (1990). Use of saturation mutagenesis to localize probable functional domains in the NahR protein, a LysR-type transcription activator. J Biol Chem 265, 3844-50.
  184. Steinberg, G., and Perez-Martin, J. (2008). Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol 18, 61-7.
  185. Horst, R. J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann, R., Kamper, J., Sonnewald, U., and Voll, L. M. (2010). Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol 152, 293-308.
  186. Snetselaar, K. M., Bolker, M., and Kahmann, R. (1996). Ustilago maydis Mating Hyphae Orient Their Growth toward Pheromone Sources. Fungal Genet Biol 20, 299-312.
  187. Kahmann, R., Steinberg, G., Basse, C., Feldbruegge, M., and Kämper, J. (2000). Ustilago maydis, the causative agent of corn smut disease. J. W. Kronstad (ed.), Fungal Pathology, Kluwer Academic Publisher, 347-371.


* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten