Publikationsserver der Universitätsbibliothek Marburg
Titel:Functional characterization of the Ustilago maydis virulence gene scp2
Autor:Krombach, Sina
Weitere Beteiligte: Kahmann, Regine (Prof. Dr.)
Veröffentlicht:2016
URI:https://archiv.ub.uni-marburg.de/diss/z2017/0051
DOI: https://doi.org/10.17192/z2017.0051
URN: urn:nbn:de:hebis:04-z2017-00515
DDC: Pflanzen (Botanik)
Titel (trans.):Funktionelle Charakterisierung des Virulenzgen Scp2 (sterol carrier protein 2) von U. maydis
Publikationsdatum:2016-12-20
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Peroxisom, Corn smut, peroxisome, Maisbeulenbrand

Summary:
The causative agent of the corn smut disease Ustilago maydis infects its host plant Zea mays by specialized infection structures, so-called appressoria, which are formed upon perception of chemical and physical stimuli on the leave surface. During the colonization process U. maydis secretes effector proteins that help to establish a biotrophic interaction. These effector proteins harbor an N-terminal hydrophobic secretion signal that targets them to the classical secretory pathway. In recent years, however, the existence of unconventionally secreted proteins has been uncovered which reach the extracellular space independently of the classical ER-Golgi system. In the present study the non-specific lipid transfer protein Scp2 (sterol carrier protein 2) of U. maydis was analyzed, which was identified as a putative candidate for unconventional protein secretion. Scp2 lacks a classical N-terminal signal peptide but exhibits a peroxisomal targeting signal (PTS1). A quantitative real-time PCR approach revealed that scp2 is up-regulated during early stages of plant colonization. Microscopic analyses demonstrated that the ability of scp2 deletion strains to form appressoria on artificial surfaces was significantly decreased. Furthermore, deletion of scp2 caused a virulence defect that appeared to result from a reduced efficiency of plant cuticle penetration. These defects are unlikely to result from deficiency in peroxisomal β- oxidation. In contrast to scp2 deletion strains, the infection of maize plants with a strain overexpressing scp2 under the cmu1 promoter triggered strong plant defense reactions. Two Scp2 paralogs were shown to localize in peroxisomes but deletion of the respective genes revealed no effect on U. maydis virulence. With the help of colony secretion assays it was demonstrated that small amounts of Scp2 are unconventionally secreted. The export of Scp2 via the classical ER-Golgi route, however, could not complement the virulence phenotype of the scp2 mutant strain, suggesting that the virulence defect is unconnected to the extracellular population of the protein. Surprisingly, peroxisomes and lipid droplets in the scp2 deletion strains displayed an altered distribution during filamentation on parafilm and on the plant surface. Based on these results, it is proposed that Scp2 affects appressorium development by influencing the distribution of peroxisomes and lipid droplets and thus constitutes a novel player in plant surface penetration.

Bibliographie / References

  1. Kunze, M., Pracharoenwattana, I., Smith, S. M., Hartig, A. (2006). A central role for the peroxisomal membrane in glyoxylate cycle function. Biochim Biophys Acta, 1763, 1441-1452.
  2. Park, S. Y., Jauh, G. Y., Mollet, J. C., Eckard, K. J., Nothnagel, E. A., Walling, L. L., Lord, E. M. (2000). A lipid transfer-like protein is necessary for lily pollen tube adhesion to an in vitro stylar matrix. Plant Cell, 12, 151-164.
  3. Livak, K. J., Schmittgen, T. D. (2001). Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402-408.
  4. Krügel, H., Fiedler, G., Haupt, I., Sarfert, E., Simon, H. (1988). Analysis of the nourseothricin-resistance gene (nat) of Streptomyces noursei. Gene, 62, 209-217.
  5. Lo Presti, L., Zechmann, B., Kumlehn, J., Liang, L., Lanver, D., Tanaka, S., Bock, R., Kahmann, R. (2016). An assay for entry of secreted fungal effectors into plant cells. New Phytol.
  6. Binns, D., Januszewski, T., Chen, Y., Hill, J., Markin, V. S., Zhao, Y., Gilpin, C., Chapman, K. D., Anderson, R. G., Goodman, J. M. (2006). An intimate collaboration between peroxisomes and lipid bodies. J Cell Biol, 173, 719-731.
  7. Hammond, G. R., Machner, M. P., Balla, T. (2014). A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J Cell Biol, 205, 113-126.
  8. Kämper, J. (2004). A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Molecular Genetics and Genomics, 271, 103-110.
  9. Stock, J., Sarkari, P., Kreibich, S., Brefort, T., Feldbrügge, M., Schipper, K. (2012). Applying unconventional secretion of the endochitinase Cts1 to export heterologous proteins in Ustilago maydis. J Biotechnol, 161, 80-91.
  10. Lanver, D. (2011). Appressorienbildung von Ustilago maydis auf hydrophoben Oberflächen: Regulation durch Membranproteine. Dissertation der Fakultät für Biologie, PhilippsUniversität Marburg.
  11. Zheng, B. S., Ronnberg, E., Viitanen, L., Salminen, T. A., Lundgren, K., Moritz, T., Edqvist, J. (2008). Arabidopsis sterol carrier protein-2 is required for normal development of seeds and seedlings. J Exp Bot, 59, 3485-3499.
  12. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem, 72, 248-254.
  13. Brachmann, A., König, J., Julius, C., Feldbrügge, M. (2004). A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics, 272, 216-226.
  14. Prydz, K., Tveit, H., Vedeler, A., Saraste, J. (2013). Arrivals and departures at the plasma membrane: direct and indirect transport routes. Cell Tissue Res, 352, 5-20.
  15. Redkar, A., Hoser, R., Schilling, L., Zechmann, B., Krzymowska, M., Walbot, V., Döhlemann, G. (2015). A Secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors. Plant Cell, 27, 1332-1351.
  16. Tanaka, S., Brefort, T., Neidig, N., Djamei, A., Kahnt, J., Vermerris, W., Koenig, S., Feussner, K., Feussner, I., Kahmann, R. (2014). A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. Elife, 3, e01355.
  17. Broomfield, P. L., Hargreaves, J. A. (1992). A single amino-acid change in the iron-sulphur protein subunit of succinate dehydrogenase confers resistance to carboxin in Ustilago maydis. Curr Genet, 22, 117-121.
  18. Erdmann, R. (2016). Assembly, maintenance and dynamics of peroxisomes. Biochim Biophys Acta, 1863, 787-789.
  19. Asakura, M., Ninomiya, S., Sugimoto, M., Oku, M., Yamashita, S., Okuno, T., Sakai, Y., Takano, Y. (2009). Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare. Plant Cell, 21, 1291-1304.
  20. Zelinger, E., Hawes, C. R., Gurr, S. J., Dewey, F. M. (2006). Attachment and adhesion of conidia of Stagonospora nodorum to natural and artificial surfaces. Physiological and Molecular Plant Pathology, 68, 209-215.
  21. Voet, D. and Voet, J. G. (2004). Biochemie, 3rd ed., John Wiley & Sons Wanders, R. J. (2014). Metabolic functions of peroxisomes in health and disease. Biochimie, 98, 36-44.
  22. Bruns, C., McCaffery, J. M., Curwin, A. J., Duran, J. M., Malhotra, V. (2011). Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J Cell Biol, 195, 979-992.
  23. Zechner, R., Madeo, F. (2009). Cell biology: Another way to get rid of fat. Nature, 458, 1118- 1119.
  24. Silva, B. M., Prados-Rosales, R., Espadas-Moreno, J., Wolf, J. M., Luque-Garcia, J. L., Goncalves, T., Casadevall, A. (2014). Characterization of Alternaria infectoria extracellular vesicles. Med Mycol, 52, 202-210.
  25. Brefort, T., Tanaka, S., Neidig, N., Döhlemann, G., Vincon, V., Kahmann, R. (2014). Characterization of the largest effector gene cluster of Ustilago maydis. PLoS Pathog, 10, e1003866.
  26. Mortimer, C. E., Müller, U. (2003). Chemie: Das Basiswissen der Chemie, 8th ed. , Thieme Müller, A. N., Ziemann, S., Treitschke, S., Assmann, D., Döhlemann, G. (2013). Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog, 9, e1003177.
  27. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
  28. Wei, W., Zhu, W., Cheng, J., Xie, J., Li, B., Jiang, D., Li, G., Yi, X., Fu, Y. (2013). CmPEX6, a gene involved in peroxisome biogenesis, is essential for parasitism and conidiation by the sclerotial parasite Coniothyrium minitans. Appl Environ Microbiol, 79, 3658-3666.
  29. Kwolek-Mirek, M., Zadrag-Tecza, R. (2014). Comparison of methods used for assessing the viability and vitality of yeast cells. Fems Yeast Research, 14, 1068-1079.
  30. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol, 43, 205-227.
  31. Day, P. R., Anagnostakis, S. L. (1971). Corn smut dikaryon in culture. Nat New Biol, 231, 19- 20.
  32. Bebber, D. P., Ramotowski, M. A. T., Gurr, S. J. (2013). Crop pests and pathogens move polewards in a warming world. Nature Climate Change, 3, 985-988.
  33. Heimel, K., Freitag, J., Hampel, M., Ast, J., Bölker, M., Kämper, J. (2013). Crosstalk between the unfolded protein response and pathways that regulate pathogenic development in Ustilago maydis. Plant Cell, 25, 4262-4277.
  34. Freitag, J., Ast J., Bölker, M. (2012). Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature, 485, 522-525.
  35. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (1987). Current Protocols in Molecular Biology, Greene Publishing Associates/Wiley Interscience.
  36. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol, 98, 503-517.
  37. 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 U S A, 86, 5878-5882.
  38. Banuett, F., Herskowitz, I. (1996). Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development, 122, 2965-2976.
  39. Rabouille, C., Malhotra, V., Nickel, W. (2012). Diversity in unconventional protein secretion. Journal of Cell Science, 125, 5251-5255.
  40. Jansen, G., Wu, C., Schade, B., Thomas, D. Y., Whiteway, M. (2005). Drag&Drop cloning in yeast. Gene, 344, 43-51.
  41. Ast, J., Stiebler, A. C., Freitag, J., Bölker, M. (2013). Dual targeting of peroxisomal proteins. Front Physiol, 4, 297.
  42. Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., Gurr, S. J. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature, 484, 186-194.
  43. Schirawski, J., Böhnert, H. U., Steinberg, G., Snetselaar, K., Adamikowa, L., Kahmann, R. (2005). Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell, 17, 3532-3543.
  44. Gibson, D. G., Young, L., Chuang, R. Y., Venter, J. C., Hutchison, C. A., 3rd, Smith, H. O. (2009). Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods, 6, 343-345.
  45. Curwin, A. J., Brouwers, N. (2016). ESCRT-III drives the final stages of CUPS maturation for unconventional protein secretion. 5.
  46. Maruyama, J., Kitamoto, K. (2013). Expanding functional repertoires of fungal peroxisomes: contribution to growth and survival processes. Front Physiol, 4, 177.
  47. Takenouchi, T., Tsukimoto, M., Iwamaru, Y., Sugama, S., Sekiyama, K., Sato, M., Kojima, S., Hashimoto, M., Kitani, H. (2015). Extracellular ATP induces unconventional release of glyceraldehyde-3-phosphate dehydrogenase from microglial cells. Immunol Lett, 167, 116-124.
  48. Inoue, K., Suzuki, T., Ikeda, K., Jiang, S., Hosogi, N., Hyon, G. S., Hida, S., Yamada, T., Park, P. (2008). Extracellular matrix of Magnaporthe oryzae may have a role in host adhesion during fungal penetration and is digested by matrix metalloproteinases (vol 73, pg 388, 2007). Journal of General Plant Pathology, 74, 96-96.
  49. Raposo, G., Stoorvogel, W. (2013). Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol, 200, 373-383.
  50. Falomir Lockhart, L. J., Burgardt, N. I., Ferreyra, R. G., Ceolin, M., Ermacora, M. R., Corsico, B. (2009). Fatty acid transfer from Yarrowia lipolytica sterol carrier protein 2 to phospholipid membranes. Biophys J, 97, 248-256.
  51. Bendtsen, J. D., Jensen, L. J., Blom, N., Von Heijne, G., Brunak, S. (2004). Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel, 17, 349-356.
  52. Blitzer, E. J., Vyazunova, I., Lan, Q. (2005). Functional analysis of AeSCP-2 using gene expression knockdown in the yellow fever mosquito, Aedes aegypti. Insect Mol Biol, 14, 301-307.
  53. Wang, Z. Y., Soanes, D. M., Kershaw, M. J., Talbot, N. J. (2007). Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid beta-oxidation during appressorium-mediated plant infection. Mol Plant Microbe Interact, 20, 475-491.
  54. Edqvist, J., Blomqvist, K. (2006). Fusion and Fission, the Evolution of Sterol Carrier Protein2. Journal of Molecular Evolution, 62, 292-306.
  55. Gallegos, A. M., Atshaves, B. P., Storey, S. M., Starodub, O., Petrescu, A. D., Huang, H., McIntosh, A. L., Martin, G. G., Chao, H., Kier, A. B., Schroeder, F. (2001). Gene structure, intracellular localization, and functional roles of sterol carrier protein-2. Prog Lipid Res, 40, 498-563.
  56. Campbell, M. T., Proctor, C. A., Dou, Y., Schmitz, A. J., Phansak, P., Kruger, G. R., Zhang, C., Walia, H. (2015). Genetic and molecular characterization of submergence response identifies Subtol6 as a major submergence tolerance locus in maize. PLoS One, 10, e0120385.
  57. Fukunaga, K., Hill, J., Vigouroux, Y., Matsuoka, Y., Sanchez, G. J., Liu, K., Buckler, E. S., Doebley, J. (2005). Genetic diversity and population structure of teosinte. Genetics, 169, 2241-2254.
  58. Schuster, M., Schweizer, G., Reissmann, S., Kahmann, R. (2016). Genome editing in Ustilago maydis using the CRISPR-Cas system. Fungal Genet Biol, 89, 3-9.
  59. Grieve, A. G., Rabouille, C. (2011). Golgi bypass: skirting around the heart of classical secretion. Cold Spring Harb Perspect Biol, 3.
  60. Ramos-Pamplona, M., Naqvi, N. I. (2006). Host invasion during rice-blast disease requires carnitine-dependent transport of peroxisomal acetyl-CoA. Mol Microbiol, 61, 61-75.
  61. Zhao, H., Xu, C., Lu, H. L., Chen, X., St Leger, R. J., Fang, W. (2014). Host-to-pathogen gene transfer facilitated infection of insects by a pathogenic fungus. PLoS Pathog, 10, e1004009.
  62. Petre, B., Kamoun, S. (2014). How do filamentous pathogens deliver effector proteins into plant cells? PLoS Biol, 12, e1001801.
  63. Müller, O., Schreier, P. H., Uhrig, J. F. (2008). Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol Genet Genomics, 279, 27- 39.
  64. Brachmann, A., Weinzierl, G., Kämper, J., Kahmann, R. (2001). Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol, 42, 1047-1063.
  65. Aichinger, C., Hansson, K., Eichhorn, H., Lessing, F., Mannhaupt, G., Mewes, W., Kahmann, R. (2003). Identification of plant-regulated genes in Ustilago maydis by enhancer-trapping mutagenesis. Mol Genet Genomics, 270, 303-314.
  66. Hewald, S. (2005). Identifizierung und Charakterisierung zweier für die Produktion extrazellulärer Glykolipide verantwortlichen Gencluster in Ustilago maydis. Dissertation der Fakultät für Biologie, Philipps-Universität Marburg.
  67. Baes, M., Huyghe, S., Carmeliet, P., Declercq, P. E., Collen, D., Mannaerts, G. P., Van Veldhoven, P. P. (2000). Inactivation of the peroxisomal multifunctional protein-2 in mice impedes the degradation of not only 2-methyl-branched fatty acids and bile acid intermediates but also of very long chain fatty acids. J Biol Chem, 275, 16329-16336.
  68. Snetselaar, K. M. M., C.W. (1993). Infection of maize stigmas by Ustilago maydis: Light and electron microscopy. Phytopathology, 83, 843-850.
  69. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature, 444, 97-101.
  70. Donaldson, M. E., Meng, S., Gagarinova, A., Babu, M., Lambie, S. C., Swiadek, A. A., Saville, B. J. (2013). Investigating the Ustilago maydis/Zea mays pathosystem: transcriptional responses and novel functional aspects of a fungal calcineurin regulatory B subunit. Fungal Genet Biol, 58-59, 91-104.
  71. Bohlmann, R. (1996). Isolierung und Charakterisierung von filamentspezifisch exprimierten Genen aus Ustilago maydis. Dissertation der Fakultät für Biologie, LudwigMaximilians-Universität München.
  72. Steinberg, G., Schliwa, M., Lehmler, C., Bölker, M., Kahmann, R., McIntosh, J. R. (1998). Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. Journal of Cell Science, 111, 2235-2246.
  73. Snetselaar, K. M. M., C.W. (1994). Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol. Res., 98, 347-355.
  74. Wriessnegger, T., Gubitz, G., Leitner, E., Ingolic, E., Cregg, J., de la Cruz, B. J., Daum, G. (2007). Lipid composition of peroxisomes from the yeast Pichia pastoris grown on different carbon sources. Biochim Biophys Acta, 1771, 455-461.
  75. Frolov, A., Miller, K., Billheimer, J. T., Cho, T. H., Schroeder, F. (1997). Lipid specificity and location of the sterol carrier protein-2 fatty acid-binding site: a fluorescence displacement and energy transfer study. Lipids, 32, 1201-1209.
  76. Skibbe, D. S., Döhlemann, G., Fernandes, J., Walbot, V. (2010). Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science, 328, 89- 92.
  77. Strable, J., Scanlon, M. J. (2009). Maize (Zea mays): a model organism for basic and applied research in plant biology. Cold Spring Harb Protoc, 2009, pdb emo132.
  78. Dunn, M. F., Ramirez-Trujillo, J. A., Hernandez-Lucas, I. (2009). Major roles of isocitrate lyase and malate synthase in bacterial and fungal pathogenesis. Microbiology, 155, 3166-3175.
  79. Nickel, W., Rabouille, C. (2009). Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol, 10, 148-155.
  80. Michels, P. A., Bringaud, F., Herman, M., Hannaert, V. (2006). Metabolic functions of glycosomes in trypanosomatids. Biochim Biophys Acta, 1763, 1463-1477.
  81. Wanders, R. J. A., Waterham, H. R., Ferdinandusse, S. (2016). Metabolic interplay between peroxisomes and other subcellular organelles including mitochondria and the endoplasmic reticulum. Frontiers in Cell and Developmental Biology, 3.
  82. 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., Kahmann, R. (2011). Metabolic priming by a secreted fungal effector. Nature, 478, 395-398.
  83. Sambrook, J., Frisch, E. F.,Maniatis, T. (1989). Molecular Cloning: A laboratory manual. Cold Spring Harbour, New York.
  84. Karkowska-Kuleta, J., Kozik, A. (2014). Moonlighting proteins as virulence factors of pathogenic fungi, parasitic protozoa and multicellular parasites. Mol Oral Microbiol, 29, 270-283.
  85. Patkar, R. N., Suresh, A., Naqvi, N. I. (2010). MoTea4-mediated polarized growth is essential for proper asexual development and pathogenesis in Magnaporthe oryzae. Eukaryot Cell, 9, 1029-1038.
  86. 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.
  87. Christianson, T. W., Sikorski, R. S., Dante, M., Shero, J. H., Hieter, P. (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene, 110, 119-122.
  88. Greenspan, P., Mayer, E. P., Fowler, S. D. (1985). Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol, 100, 965-973.
  89. Goroncy, A. K., Murayama, K., Shirouzu, M., Kuramitsu, S., Kigawa, T., Yokoyama, S. (2010). NMR and X-ray structures of the putative sterol carrier protein 2 from Thermus thermophilus HB8 show conformational changes. J Struct Funct Genomics, 11, 247- 256.
  90. García, F. L., Szyperski, T., Dyer, J. H., Choinowski, T., Seedorf, U., Hauser, H., Wuthrich, K. (2000). NMR structure of the sterol carrier protein-2: implications for the biological role. J Mol Biol, 295, 595-603.
  91. Cohen, S. N., Chang, A. C., Hsu L. (1972). Nonchromosomal antibiotic resistance in bacteria: Genetic transformation of Escherichia coli by R-factor DNA. PNAS, USA, 69, 2110- 2114.
  92. Chua, C. E., Lim, Y. S., Lee, M. G., Tang, B. L. (2012). Non-classical membrane trafficking processes galore. J Cell Physiol, 227, 3722-3730.
  93. Liu, F., Zhang, X., Lu, C., Zeng, X., Li, Y., Fu, D., Wu, G. (2015). Non-specific lipid transfer proteins in plants: presenting new advances and an integrated functional analysis. J Exp Bot, 66, 5663-5681.
  94. Shai, N., Schuldiner, M., Zalckvar, E. (2016). No peroxisome is an island - Peroxisome contact sites. Biochim Biophys Acta, 1863, 1061-1069.
  95. Döhlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D., Kahmann, R. (2009). Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog, 5, e1000290.
  96. Anjard, C., Loomis, W. F. (2005). Peptide signaling during terminal differentiation of Dictyostelium. Proc Natl Acad Sci U S A, 102, 7607-7611.
  97. Meinecke, M., Bartsch, P., Wagner, R. (2016). Peroxisomal protein import pores. Biochim Biophys Acta, 1863, 821-827.
  98. Girzalsky, W., Saffian, D., Erdmann, R. (2010). Peroxisomal protein translocation. Biochim Biophys Acta, 1803, 724-731.
  99. Steinberg, S. J., Dodt, G., Raymond, G. V., Braverman, N. E., Moser, A. B., Moser, H. W. (2006). Peroxisome biogenesis disorders. Biochim Biophys Acta, 1763, 1733-1748.
  100. Gabaldón, T. (2010). Peroxisome diversity and evolution. Philos Trans R Soc Lond B Biol Sci, 365, 765-773.
  101. Rodriguez-Serrano, M., Romero-Puertas, M. C., Sparkes, I., Hawes, C., del Río, L. A., Sandalio, L. M. (2009). Peroxisome dynamics in Arabidopsis plants under oxidative stress induced by cadmium. Free Radic Biol Med, 47, 1632-1639.
  102. del Río, L. A. (2011). Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys, 506, 1-11.
  103. Corpas, F. J., Barroso, J. B., del Río, L. A. (2001). Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci, 6, 145-150.
  104. Freitag, J., Ast, J., Linne, U., Stehlik, T., Martorana, D., Bölker, M., Sandrock, B. (2014). Peroxisomes contribute to biosynthesis of extracellular glycolipids in fungi. Mol Microbiol, 93, 24-36.
  105. Guimaraes, S. C., Schuster, M., Bielska, E., Dagdas, G., Kilaru, S., Meadows, B. R., Schrader, M., Steinberg, G. (2015). Peroxisomes, lipid droplets, and endoplasmic reticulum "hitchhike" on motile early endosomes. J Cell Biol, 211, 945-954.
  106. Salogiannis, J., Egan, M. J., Reck-Peterson, S. L. (2016). Peroxisomes move by hitchhiking on early endosomes using the novel linker protein PxdA. Journal of Cell Biology, 212, 289-296.
  107. Oku, M., Sakai, Y. (2016). Pexophagy in yeasts. Biochim Biophys Acta, 1863, 992-998.
  108. García-Muse, T., Steinberg, G., Pérez-Martin, J. (2003). Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot Cell, 2, 494-500.
  109. Flis, V. V., Fankl, A., Ramprecht, C., Zellnig, G., Leitner, E., Hermetter, A., Daum, G. (2015). Phosphatidylcholine Supply to Peroxisomes of the Yeast Saccharomyces cerevisiae. PLoS One, 10, e0135084.
  110. Krahmer, N., Guo, Y., Wilfling, F., Hilger, M., Lingrell, S., Heger, K., Newman, H. W., Schmidt-Supprian, M., Vance, D. E., Mann, M., Farese, R. V., Jr., Walther, T. C. (2011). Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. Cell Metab, 14, 504- 515.
  111. Steringer, J. P., Bleicken, S., Andreas, H., Zacherl, S., Laussmann, M., Temmerman, K., Contreras, F. X., Bharat, T. A., Lechner, J., Muller, H. M., Briggs, J. A., GarciaSaez, A. J., Nickel, W. (2012). Phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2)- dependent oligomerization of fibroblast growth factor 2 (FGF2) triggers the formation of a lipidic membrane pore implicated in unconventional secretion. J Biol Chem, 287, 27659-27669.
  112. Mendoza-Mendoza, A., Berndt, P., Djamei, A., Weise, C., Linne, U., Marahiel, M., Vranes, M., Kämper, J., Kahmann, R. (2009). Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol Microbiol, 71, 895-911.
  113. Lanver, D., Berndt, P., Tollot, M., Naik, V., Vranes, M., Warmann, T., Münch, K., Rössel, N., Kahmann, R. (2014). Plant surface cues prime Ustilago maydis for biotrophic development. PLoS Pathog, 10, e1004272.
  114. Leenders, F., Tesdorpf, J. G., Markus, M., Engel, T., Seedorf, U., Adamski, J. (1996). Porcine 80-kDa protein reveals intrinsic 17 beta-hydroxysteroid dehydrogenase, fatty acyl-CoA-hydratase/dehydrogenase, and sterol transfer activities. J Biol Chem, 271, 5438-5442.
  115. Neuberger, G., Maurer-Stroh, S., Eisenhaber, B., Hartig, A., Eisenhaber, F. (2003). Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. J Mol Biol, 328, 581-592.
  116. Asakura, M., Yoshino, K., Hill, A. M., Kubo, Y., Sakai, Y., Takano, Y. (2012). Primary and secondary metabolism regulates lipolysis in appressoria of Colletotrichum orbiculare. Fungal Genet Biol, 49, 967-975.
  117. Schrader, M., Costello, J. L., Godinho, L. F., Azadi, A. S., Islinger, M. (2016). Proliferation and fission of peroxisomes - An update. Biochim Biophys Acta, 1863, 971-983.
  118. Alsteens, D., Van Dijck, P., Lipke, P. N., Dufrene, Y. F. (2013). Quantifying the forces driving cell-cell adhesion in a fungal pathogen. Langmuir, 29, 13473-13480.
  119. Robin, J. B., Arffa, R. C., Avni, I., Rao, N. A. (1986). Rapid visualization of three common fungi using fluorescein-conjugated lectins. Invest Ophthalmol Vis Sci., Vol.27, 500-506.
  120. Wegehingel, S., Zehe, C., Nickel, W. (2008). Rerouting of fibroblast growth factor 2 to the classical secretory pathway results in post-translational modifications that block binding to heparan sulfate proteoglycans. FEBS Lett, 582, 2387-2392.
  121. Gee, H. Y., Noh, S. H., Tang, B. L., Kim, K. H., Lee, M. G. (2011). Rescue of DeltaF508- CFTR trafficking via a GRASP-dependent unconventional secretion pathway. Cell, 146, 746-760.
  122. Lensink, M. F., Haapalainen, A. M., Hiltunen, J. K., Glumoff, T., Juffer, A. H. (2002). Response of SCP-2L domain of human MFE-2 to ligand removal: binding site closure and burial of peroxisomal targeting signal. J Mol Biol, 323, 99-113.
  123. Pol, A., Gross, S. P., Parton, R. G. (2014). Review: biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J Cell Biol, 204, 635-646.
  124. Berger, A. C., Vanderford, T. H., Gernert, K. M., Nichols, J. W., Faundez, V., Corbett, A. H. (2005). Saccharomyces cerevisiae Npc2p is a functionally conserved homologue of the human Niemann-Pick disease type C 2 protein, hNPC2. Eukaryot Cell, 4, 1851- 1862.
  125. 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, 2085-2101.
  126. Brown, L. A., Baker, A. (2008). Shuttles and cycles: transport of proteins into the peroxisome matrix (review). Mol Membr Biol, 25, 363-375.
  127. Mullis, K., Faloona, F., Scharf, S., Saiki, R., Horn, G., Erlich, H. (1986). Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb Symp Quant Biol, 51 Pt 1, 263-273.
  128. Cánovas, D., Pérez-Martín, J. (2009). Sphingolipid biosynthesis is required for polar growth in the dimorphic phytopathogen Ustilago maydis. Fungal Genet Biol, 46, 190-200.
  129. Murphy, E. J., Stiles, T., Schroeder, F. (2000). Sterol carrier protein-2 expression alters phospholipid content and fatty acyl composition in L-cell fibroblasts. J Lipid Res, 41, 788-796.
  130. Atshaves, B. P., Storey, S. M., McIntosh, A. L., Petrescu, A. D., Lyuksyutova, O. I., Greenberg, A. S., Schroeder, F. (2001). Sterol carrier protein-2 expression modulates protein and lipid composition of lipid droplets. J Biol Chem, 276, 25324-25335.
  131. Starodub, O., Jolly, C. A., Atshaves, B. P., Roths, J. B., Murphy, E. J., Kier, A. B., Schroeder, F. (2000). Sterol carrier protein-2 localization in endoplasmic reticulum and role in phospholipid formation. Am J Physiol Cell Physiol, 279, C1259-1269.
  132. Schroeder, F., Atshaves, B. P., McIntosh, A. L., Gallegos, A. M., Storey, S. M., Parr, R. D., Jefferson, J. R., Ball, J. M., Kier, A. B. (2007). Sterol carrier protein-2: new roles in regulating lipid rafts and signaling. Biochim Biophys Acta, 1771, 700-718.
  133. Stolowich, N. J., Petrescu, A. D., Huang, H., Martin, G. G., Scott, A. I., Schroeder, F. (2002). Sterol carrier protein-2: structure reveals function. Cellular and Molecular Life Sciences CMLS, 59, 193-212.
  134. Alvarez, F. J., Douglas, L. M., Konopka, J. B. (2007). Sterol-Rich Plasma Membrane Domains in Fungi. Eukaryotic Cell, 6, 755-763.
  135. Lan, Q., Massey, R. J. (2004). Subcellular localization of the mosquito sterol carrier protein2 and sterol carrier protein-x. J Lipid Res, 45, 1468-1474.
  136. Tucker, S. L., Talbot, N. J. (2001). Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol, 39, 385-417.
  137. Reina-Pinto, J. J., Yephremov, A. (2009). Surface lipids and plant defenses. Plant Physiol Biochem, 47, 540-549.
  138. Bölker, M., Urban, M., Kahmann, R. (1992). The a mating type locus of U. maydis specifies cell signaling components. Cell, 68, 441-450.
  139. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, W., Martin, T., Herskowitz, I., Kahmann, R. (1990). The b alleles of Ustilago maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell, 60, 295-306.
  140. Scherer, M., Heimel, K., Starke, V., Kämper, J. (2006). The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell, 18, 2388- 2401.
  141. De Berti, F. P., Capaldi, S., Ferreyra, R., Burgardt, N., Acierno, J. P., Klinke, S., Monaco, H. L., Ermácora, M. R. (2013). The crystal structure of sterol carrier protein 2 from Yarrowia lipolytica and the evolutionary conservation of a large, non-specific lipidbinding cavity. Journal of Structural and Functional Genomics, 14, 145-153.
  142. Marie, M., Dale, H. A., Sannerud, R., Saraste, J. (2009). The function of the intermediate compartment in pre-Golgi trafficking involves its stable connection with the centrosome. Mol Biol Cell, 20, 4458-4470.
  143. Wang, Z. Y., Thornton, C. R., Kershaw, M. J., Li, D. B., Talbot, N. J. (2003). The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol, 47, 1601-1612.
  144. Titorenko, V. I., Rachubinski, R. A. (2001). The life cycle of the peroxisome. Nat Rev Mol Cell Biol, 2, 357-368.
  145. Gao, Q., Goodman, J. M. (2015). The lipid droplet-a well-connected organelle. Front Cell Dev Biol, 3, 49.
  146. Klose, J., Kronstad, J. W. (2006). The Multifunctional β-Oxidation Enzyme Is Required for Full Symptom Development by the Biotrophic Maize Pathogen Ustilago maydis. Eukaryotic Cell, 5, 2047-2061.
  147. de Duve, C. (1969). The peroxisome: a new cytoplasmic organelle. Proc R Soc Lond B Biol Sci, 173, 71-83.
  148. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., Sternberg, M. J. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc, 10, 845-858.
  149. Anderson, P. J. (1985). The recovery of nitrocellulose-bound protein. Anal Biochem, 148, 105- 110.
  150. Nickel, W. (2011). The unconventional secretory machinery of fibroblast growth factor 2. Traffic, 12, 799-805.
  151. Khrunyk, Y. (2010). The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. Dissertation der Fakultät für Biologie, Philipps-Universität Marburg.
  152. Hemetsberger, C., Herrberger, C., Zechmann, B., Hillmer, M., Döhlemann, G. (2012). The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog, 8, e1002684.
  153. Tollot, M., Assmann, D., Becker, C., Altmuller, J., Dutheil, J. Y., Wegner, C. E., Kahmann, R. (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.
  154. McGrath, J. P., Varshavsky, A. (1989). The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature, 340, 400-404.
  155. Schuster, M., Lipowsky, R., Assmann, M. A., Lenz, P., Steinberg, G. (2011). Transient binding of dynein controls bidirectional long-range motility of early endosomes. Proc Natl Acad Sci U S A, 108, 3618-3623.
  156. Giraldo, M. C., Dagdas, Y. F., Gupta, Y. K., Mentlak, T. A., Yi M., Martinez-Rocha, A. L., Saitoh, H., Terauchi, R., Talbot, N. J., Valent, B. (2013). Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat Commun, 4, 1996.
  157. 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., Dou, D. (2014). Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun, 5, 4686.
  158. Malhotra, V. (2013). Unconventional protein secretion: an evolving mechanism. Embo j, 32, 1660-1664.
  159. Ding Y., Robinson D. G., Jiang L. (2014). Unconventional protein secretion (UPS) pathways in plants. Curr Opin Cell Biol, 29, 107-115.
  160. Manjithaya, R., Anjard, C., Loomis, W. F., Subramani, S. (2010). Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol, 188, 537-546.
  161. Zemskov, E. A., Mikhailenko, I., Hsia, R. C., Zaritskaya, L., Belkin, A. M. (2011). Unconventional secretion of tissue transglutaminase involves phospholipid-dependent delivery into recycling endosomes. PLoS One, 6, e19414.
  162. Brefeld, O. (1883). Untersuchungen aus dem Gesamtgebiet der Mykologie. , Heft 5,67-75 Brefort, T., Döhlemann, G., Mendoza-Mendoza, A., Reissmann, S., Djamei, A., Kahmann, R. (2009). Ustilago maydis as a Pathogen. Annual Review of Phytopathology, 47, 423- 445.
  163. Holliday, R. (1974). Ustilago maydis. In King, R.C. (ed.) Handbook of Genetics 1, Plenum Press, New York/USA: 575-595.
  164. Steinberg, G., Perez-Martin, J. (2008). Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol, 18, 61-67.
  165. Djamei, A., Kahmann, R. (2012). Ustilago maydis: dissecting the molecular interface between pathogen and plant. PLoS Pathog, 8, e1002955.
  166. Basse, C. W., Steinberg, G. (2004). Ustilago maydis, model system for analysis of the molecular basis of fungal pathogenicity. Mol Plant Pathol, 5, 83-92.
  167. Kahmann, R., Steinberg, G., Basse, C., Feldbrügge, M., Kämper, J. (2000). Ustilago maydis, the Causative Agent of Corn Smut Disease. In: Fungal Pathology, pp. 347-371 Ed J. W. Kronstad. Dordrecht: Springer Netherlands.
  168. Shoji, J. Y., Kikuma, T., Kitamoto, K. (2014). Vesicle trafficking, organelle functions, and unconventional secretion in fungal physiology and pathogenicity. Curr Opin Microbiol, 20, 1-9.
  169. Soundararajan, S., Jedd, G., Li, X., Ramos-Pamplona, M., Chua, N. H., Naqvi, N. I. (2004). Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell, 16, 1564- 1574.

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