Crosstalk between the unfolded protein response and pathways that regulate pathogenic development in Ustilago maydis

Plant Cell

Volumn 25, Issue 10, 2013, Pages 4262-4277

  Heimel, Kai ^a,b   Freitag, Johannes ^c,d   Hampel, Martin ^a   Ast, Julia ^c   Bölker, Michael ^c,d   Kämper, Jörg ^b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d LOEWE Research Center for Synthetic Microbiology (SYNMIKRO)   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; FUNGI; USTILAGO MAYDIS;

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; FUNGAL PROTEIN;

ENDOPLASMIC RETICULUM STRESS; FUNGAL MATING TYPE GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; USTILAGO;

BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; ENDOPLASMIC RETICULUM STRESS; FUNGAL PROTEINS; GENES, MATING TYPE, FUNGAL; MOLECULAR SEQUENCE DATA; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; USTILAGO; ZEA MAYS;

EID: 84888398095     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.115899     Document Type: Article

References (84)

1. Aichinger, C., Hansson, K., Eichhorn, H., Lessing, F., Mannhaupt, G., Mewes, W., and Kahmann, R. (2003). Identification of plantregulated genes in Ustilago maydis by enhancer-trapping mutagenesis. Mol. Genet. Genomics 270: 303-314.
2. Baumann, S., Pohlmann, T., Jungbluth, M., Brachmann, A., and Feldbrügge, M. (2012). Kinesin-3 and dynein mediate microtubuledependent co-transport of mRNPs and endosomes. J. Cell Sci. 125: 2740-2752.
3. Böhmer, C., Böhmer, M., Bölker, M., and Sandrock, B. (2008). Cdc42 and the Ste20-like kinase Don3 act independently in triggering cytokinesis in Ustilago maydis. J. Cell Sci. 121: 143-148.
4. Bölker, M., Genin, S., Lehmler, C., and Kahmann, R. (1995). Genetic regulation of mating, and dimorphism in Ustilago maydis. Can. J. Bot. 73: 320-325.
5. Bölker, M., Urban, M., and Kahmann, R. (1992). The a mating type locus of U. maydis specifies cell signaling components. Cell 68: 441-450.
6. Bottin, A., Kämper, J., and Kahmann, R. (1996). Isolation of a carbon source-regulated gene from Ustilago maydis. Mol. Gen. Genet. 253: 342-352.
7. Brachmann, A., König, J., Julius, C., and Feldbrügge, M. (2004). A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol. Genet. Genomics 272: 216-226.
8. Brachmann, A., Weinzierl, G., Kämper, J., and Kahmann, R. (2001). Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol. Microbiol. 42: 1047-1063.
9. Byrd, A.E., and Brewer, J.W. (2012). Intricately regulated: A cellular toolbox for fine-tuning XBP1 expression and activity. Cells 1: 738-753.
10. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G., and Ron, D. (2002). IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96.
11. Casso, D.J., Liu, S., Biehs, B., and Kornberg, T.B. (2012). Expression and characterization of Drosophila signal peptide peptidase-like (sppL), a gene that encodes an intramembrane protease. PLoS ONE 7: e33827.
12. Chawla, A., Chakrabarti, S., Ghosh, G., and Niwa, M. (2011). Attenuation of yeast UPR is essential for survival and is mediated by IRE1 kinase. J. Cell Biol. 193: 41-50.
13. Cheon, S.A., Jung, K.W., Chen, Y.L., Heitman, J., Bahn, Y.S., and Kang, H.A. (2011). Unique evolution of the UPR pathway with a novel bZIP transcription factor, Hxl1, for controlling pathogenicity of Cryptococcus neoformans. PLoS Pathog. 7: e1002177.
14. Christensen, J.J. (1963). Corn smut induced by Ustilago maydis. Am. Phytopathol. Soc. Monogr. 2.
15. Colot, H.V., Park, G., Turner, G.E., Ringelberg, C., Crew, C.M., Litvinkova, L., Weiss, R.L., Borkovich, K.A., and Dunlap, J.C. (2006). A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. USA 103: 10352-10357.
16. Cox, J.S., Chapman, R.E., and Walter, P. (1997). The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol. Biol. Cell 8: 1805-1814.
17. Cox, J.S., and Walter, P. (1996). A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391-404.
18. Di Stasio, M., Brefort, T., Mendoza-Mendoza, A., Münch, K., and Kahmann, R. (2009). The dual specificity phosphatase Rok1 negatively regulates mating and pathogenicity in Ustilago maydis. Mol. Microbiol. 73: 73-88.
19. Djamei, A., and Kahmann, R. (2012). Ustilago maydis: Dissecting the molecular interface between pathogen and plant. PLoS Pathog. 8: e1002955.
20. Djamei, A., et al. (2011). Metabolic priming by a secreted fungal effector. Nature 478: 395-398.
21. Doehlemann, G., Wahl, R., Horst, R.J., Voll, L.M., Usadel, B., Poree, F., Stitt, M., Pons-Kühnemann, J., Sonnewald, U., Kahmann, R., and Kämper, J. (2008b). Reprogramming a maize plant: Transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 56: 181-195.
22. Doehlemann, G., Wahl, R., Vranes, M., de Vries, R.P., Kämper, J., and Kahmann, R. (2008a). Establishment of compatibility in the Ustilago maydis/maize pathosystem. J. Plant Physiol. 165: 29-40.
23. Feng, X., et al. (2011). HacA-independent functions of the ER stress sensor IreA synergize with the canonical UPR to influence virulence traits in Aspergillus fumigatus. PLoS Pathog. 7: e1002330.
24. Fernández-Alvarez, A., Elías-Villalobos, A., and Ibeas, J.I. (2009). The O-mannosyltransferase PMT4 is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell 21: 3397-3412.
25. Fernández-Álvarez, A., Marín-Menguiano, M., Lanver, D., Jiménez-Martín, A., Elías-Villalobos, A., Pérez-Pulido, A.J., Kahmann, R., and Ibeas, J.I. (2012). Identification of O-mannosylated virulence factors in Ustilago maydis. PLoS Pathog. 8: e1002563.
26. Fordyce, P.M., Pincus, D., Kimmig, P., Nelson, C.S., El-Samad, H., Walter, P., and DeRisi, J.L. (2012). Basic leucine zipper transcription factor Hac1 binds DNA in two distinct modes as revealed by microfluidic analyses. Proc. Natl. Acad. Sci. USA 109: E3084-E3093.
27. Freitag, J., Lanver, D., Böhmer, C., Schink, K.O., Bölker, M., and Sandrock, B. (2011). Septation of infectious hyphae is critical for appressoria formation and virulence in the smut fungus Ustilago maydis. PLoS Pathog. 7: e1002044.
28. Gardner, B.M., and Walter, P. (2011). Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 333: 1891-1894.
29. Harbut, M.B., Patel, B.A., Yeung, B.K., McNamara, C.W., Bright, A.T., Ballard, J., Supek, F., Golde, T.E., Winzeler, E.A., Diagana, T.T., and Greenbaum, D.C. (2012). Targeting the ERAD pathway via inhibition of signal peptide peptidase for antiparasitic therapeutic design. Proc. Natl. Acad. Sci. USA 109: 21486-21491.
30. Hartmann, H.A., Kahmann, R., and Bölker, M. (1996). The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J. 15: 1632-1641.
31. Heimel, K., Scherer, M., Schuler, D., and Kämper, J. (2010a). The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. Plant Cell 22: 2908-2922.
32. Heimel, K., Scherer, M., Vranes, M., Wahl, R., Pothiratana, C., Schuler, D., Vincon, V., Finkernagel, F., Flor-Parra, I., and Kämper, J. (2010b). The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog. 6: e1001035.
33. Heitman, J. (2006). Sexual reproduction and the evolution of microbial pathogens. Curr. Biol. 16: R711-R725.
34. 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.
35. Herzog, B., Popova, B., Jakobshagen, A., Shahpasandzadeh, H., and Braus, G.H. (2013). Mutual cross talk between the regulators Hac1 of the unfolded protein response and Gcn4 of the general amino acid control of Saccharomyces cerevisiae. Eukaryot. Cell 12: 1142-1154.
36. Hetz, C. (2012). The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13: 89-102.
37. Higuchi, R. (1990). Recombinant PCR. In PCR Protocols: A Guide to Methods and Applications, M.A. Innis, D.H. Gelfand, J.J. Sninsky, and T.J. White, eds (San Diego, CA: Academic Press), pp. 177-183.
38. Holliday, R. (1974). Ustilago maydis. In Handbook of Genetics, R.C. King, ed (New York: Plenum Press), pp. 575-595.
39. Hooks, K.B., and Griffiths-Jones, S. (2011). Conserved RNA structures in the non-canonical Hac1/Xbp1 intron. RNA Biol. 8: 552-556.
40. Joubert, A., Simoneau, P., Campion, C., Bataillé-Simoneau, N., Iacomi-Vasilescu, B., Poupard, P., François, J.M., Georgeault, S., Sellier, E., and Guillemette, T. (2011). Impact of the unfolded protein response on the pathogenicity of the necrotrophic fungus Alternaria brassicicola. Mol. Microbiol. 79: 1305-1324.
41. Kaffarnik, F., Müller, P., Leibundgut, M., Kahmann, R., and Feldbrügge, M. (2003). PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J. 22: 5817-5826.
42. Kämper, J. (2004). A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol. Genet. Genomics 271: 103-110.
43. Kämper, J., et al. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
44. Kämper, J., Reichmann, M., Romeis, T., Bölker, M., and Kahmann, R. (1995). Multiallelic recognition: Nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81: 73-83.
45. Kawahara, T., Yanagi, H., Yura, T., andMori, K. (1997). Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol. Biol. Cell 8: 1845-1862.
46. Kawahara, T., Yanagi, H., Yura, T., and Mori, K. (1998). Unconventional splicing of HAC1/ERN4 mRNA required for the unfolded protein response. Sequence-specific and non-sequential cleavage of the splice sites. J. Biol. Chem. 273: 1802-1807.
47. Kohno, K., Normington, K., Sambrook, J., Gething, M.J., and Mori, K. (1993). The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol. Cell. Biol. 13: 877-890.
48. Korennykh, A.V., Egea, P.F., Korostelev, A.A., Finer-Moore, J., Zhang, C., Shokat, K.M., Stroud, R.M., and Walter, P. (2009). The unfolded protein response signals through high-order assembly of Ire1. Nature 457: 687-693.
49. Lanver, D., Mendoza-Mendoza, A., Brachmann, A., and Kahmann, R. (2010). Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22: 2085-2101.
50. Li, H., Korennykh, A.V., Behrman, S.L., and Walter, P. (2010). Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc. Natl. Acad. Sci. USA 107: 16113-16118.
51. Mahlert, M., Leveleki, L., Hlubek, A., Sandrock, B., and Bölker, M. (2006). Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol. Microbiol. 59: 567-578.
52. Martínez, I.M., and Chrispeels, M.J. (2003). Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15: 561-576.
53. Mendoza-Mendoza, A., Berndt, P., Djamei, A., Weise, C., Linne, U., Marahiel, M., Vranes, M., Kämper, J., and Kahmann, R. (2009). Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol. Microbiol. 71: 895-911.
54. Mielnichuk, N., Sgarlata, C., and Pérez-Martín, J. (2009). A role for the DNA-damage checkpoint kinase Chk1 in the virulence program of the fungus Ustilago maydis. J. Cell Sci. 122: 4130-4140.
55. Miller, J.H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
56. Moore, K.A., and Hollien, J. (2012). The unfolded protein response in secretory cell function. Annu. Rev. Genet. 46: 165-183.
57. Mori, K., Sant, A., Kohno, K., Normington, K., Gething, M.J., and Sambrook, J.F. (1992). A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J. 11: 2583-2593.
58. Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A., and de Vries, R.P. (2008). The secretome of the maize pathogen Ustilago maydis. Fungal Genet. Biol. 45 (Suppl 1): S63-S70.
59. Normington, K., Kohno, K., Kozutsumi, Y., Gething, M.J., and Sambrook, J. (1989). S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell 57: 1223-1236.
60. Richie, D.L., Feng, X., Krishnan, K., and Askew, D.S. (2011). Secretion stress and antifungal resistance: An Achilles' heel of Aspergillus fumigatus? Med. Mycol. 49 (suppl. 1): S101-S106.
61. Richie, D.L., Hartl, L., Aimanianda, V., Winters, M.S., Fuller, K.K., Miley, M.D., White, S., McCarthy, J.W., Latgé, J.P., Feldmesser, M., Rhodes, J.C., and Askew, D.S. (2009). A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog. 5: e1000258.
62. Rose, M.D., Misra, L.M., and Vogel, J.P. (1989). KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57: 1211-1221.
63. Rubio, C., Pincus, D., Korennykh, A., Schuck, S., El-Samad, H., and Walter, P. (2011). Homeostatic adaptation to endoplasmic reticulum stress depends on Ire1 kinase activity. J. Cell Biol. 193: 171-184.
64. Rüegsegger, U., Leber, J.H., and Walter, P. (2001). Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107: 103-114.
65. Sambrook, J., Frisch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
66. Scherer, M., Heimel, K., Starke, V., and Kämper, J. (2006). The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18: 2388-2401.
67. Schirawski, J., Böhnert, H.U., Steinberg, G., Snetselaar, K., Adamikowa, L., and Kahmann, R. (2005). Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17: 3532-3543.
68. Schröder, M., Chang, J.S., and Kaufman, R.J. (2000). The unfolded protein response represses nitrogen-starvation induced developmental differentiation in yeast. Genes Dev. 14: 2962-2975.
69. Schröder, M., and Kaufman, R.J. (2005). The mammalian unfolded protein response. Annu. Rev. Biochem. 74: 739-789.
70. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, 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.
71. Sexton, A.C., and Howlett, B.J. (2006). Parallels in fungal pathogenesis on plant and animal hosts. Eukaryot. Cell 5: 1941-1949.
72. Shore, G.C., Papa, F.R., and Oakes, S.A. (2011). Signaling cell death from the endoplasmic reticulum stress response. Curr. Opin. Cell Biol. 23: 143-149.
73. Sidrauski, C., and Walter, P. (1997). The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90: 1031-1039.
74. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
75. Skibbe, D.S., Doehlemann, G., Fernandes, J., and Walbot, V. (2010). Maize tumors caused by Ustilago maydis require organspecific genes in host and pathogen. Science 328: 89-92.
76. Tabas, I., and Ron, D. (2011). Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13: 184-190.
77. Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S., and Walter, P. (2000). Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258.
78. 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: 3703-3709.
79. 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: 1285-1300.
80. van Loon, L.C., Rep, M., and Pieterse, C.M. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44: 135-162.
81. Walter, P., and Ron, D. (2011). The unfolded protein response: From stress pathway to homeostatic regulation. Science 334: 1081-1086.
82. Wu, J., and Kaufman, R.J. (2006). From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 13: 374-384.
83. Yi, M., Chi, M.H., Khang, C.H., Park, S.Y., Kang, S., Valent, B., and Lee, Y.H. (2009). The ER chaperone LHS1 is involved in asexual development and rice infection by the blast fungus Magnaporthe oryzae. Plant Cell 21: 681-695.
84. Zarnack, K., Eichhorn, H., Kahmann, R., and Feldbrügge, M. (2008). Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol. Microbiol. 69: 1041-1053.