Publikationsserver der Universitätsbibliothek Marburg
Titel:Die Rolle von programmiertem Zelltod in der epidermalen Resistenz von Gerste
Autor:Hof, Alexander
Weitere Beteiligte: Döhlemann, Gunther (PD Dr.)
Veröffentlicht:2013
URI:https://archiv.ub.uni-marburg.de/diss/z2013/0476
URN: urn:nbn:de:hebis:04-z2013-04767
DOI: https://doi.org/10.17192/z2013.0476
DDC: Biowissenschaften, Biologie
Titel (trans.):The role of programmed cell death during epidermal resistance of barley
Publikationsdatum:2013-10-22
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
plant pathogen, Effektor, Zelltod, Pflanzenpathogen, Resistenz, apoptosis-like cell death, Ustilago, autophagy, Autophagie, Apoptose-ähnlicher Zelltod, Gerste, effector

Zusammenfassung:
Ustilago hordei ist der Erreger von Hartbrand bei Gerste und Hafer. Um pflanzlichen Abwehrreaktionen entgegenzuwirken ist dieser basidiomycete Brandpilz zur Etablierung einer biotrophen Interaktion mit seiner Wirtspflanze auf eine Vielzahl sekretierter Effektor-proteine angewiesen, wobei der Unterdrückung von programmiertem Zelltod eine besondere Rolle zu kommt. Deletionsmutanten für den sekretierten Effektor Pep1 sind hingegen nicht in der Lage die Epidermis zu penetrieren und verursachen zahlreiche Abwehrreaktionen, welche im programmierten Zelltod der attackierten Pflanzenzelle resultieren. Im Maispathogen Ustilago maydis ist der Virulenzfaktor Pep1 funktionell konserviert und inhibiert den PAMP-vermittelten ‚oxidative burst’ durch direkte Interaktion mit apoplastischen Peroxidasen. Infektionen von Gerste mit dem inkompatiblen Nicht-Wirt-Pathogen U. maydis führen ebenfalls zu epidermalem Zelltod, ähnlich einer hypersensitiven Antwort (HR; hypersensitive response). Diese Arbeit beschäftigt sich mit den molekularen und zellulären Prozessen in kompatiblen und inkompatiblen Ustilago/Gerste-Interaktionen. Anhand einer U. hordei Transkriptomanalyse während kompatiblen sowie inkompatiblen Interaktionen wurden 18 Kandidatengene ausgewählt, die auf eine Rolle während der Wirtsbesiedelung untersucht werden sollten. Vorläufige Ergebnisse zeigen bislang fünf Kandidaten mit einer möglichen Virulenzfunktion. Im zweiten Teil der Arbeit wurden die zellulären Reaktionen bei Gerste während Ustilago-Interaktionen untersucht. Hier wurde zwischen der kompatiblen Interaktion mit U. hordei und den inkompatiblen Interaktionen mit dem Nicht-Wirt-Pathogen U. maydis, sowie der U. hordei und U. maydis pep1-Mutante verglichen. Zwar resultiert Inkompatibilität jeweils in programmiertem Zelltod, mittels verschiedener Lebendzellfärbungen, einem enzy-matischen Aktivitätstest und Infektionen Bax Inhibitor-1 (BI-1)-überexprimierender Pflanzen konnte jedoch zwischen zwei verschiedenen Zelltodarten unterschieden werden. Während Autophagie an Zelltod bei pep1-Infektionen beteiligt ist, kommt es in Abhängigkeit von BI-1 zu Apoptose-ähnlichem Zelltod nach U. maydis-Infektion. Dies konnte mittels Transmissionselektronenmikroskopie bestätigt werden. Zusätzlich haben die Bestimmung von Wasserstoffperoxid in Apoplastenflüssigkeit und die Genregulation typischer HR-assoziierter Marker gezeigt, dass eine HR nur duch U. maydis ausgelöst wird, während pep1-Infektionen in einer basalen, PAMP-vermittelten Immunität resultieren. Demnach konnte gezeigt werden, dass verschiedene Zelltodmechanismen die Resistenz von Gerste in Abhängigkeit des infizierenden Pathogens determinieren.

Bibliographie / References

  1. Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B., und Ton, J. (2011). Callose Deposition: A Multifaceted Plant Defense Response. MPMI Vol. 24, No. 2, 2011, pp. 183– 193.
  2. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315: Literaturverzeichnis 117 1398–1401.
  3. Oliva, R., Win, J., Raffaele, S., Boutemy, L., Bozkurt, T.O., Chaparro-Garcia, A., Segretin, M.E., Stam, R., Schornack, S., Cano, L.M., et al. (2010). Recent developments in effector biology of filamentous plant pathogens. Cell Microbiol 12, 705- 715.
  4. Koornneef, A., Leon-Reyes, A., Ritsema, T., Verhage, A., Den Otter, F.C., van Loon, L.C. und Pieterse C.M.J. (2008). Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147(3): 1358-1368.
  5. Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5, 308-316.
  6. Martínez-Espinoza, A.D., García-Pedrajas, M.D. und Gold, S.E. (2002). The Ustilaginales as plant pests and model systems. Fungal Genet. Biol. 35(1): 1-20.
  7. Maraschin, S. de F., Gaussand, G.I., Pulido, A., Olmedilla, A., Lamers, G.E.M., Korthout, H., Spaink, H.P. und Wang, M. (2005). Programmed cell death during the transition from multicellular structures to globular embryos in barley androgenesis. Planta 221: 459–470.
  8. Kämper, J. (2004) A PCR-based system for highly efficient generation of gene replace- ment mutants in Ustilago maydis. Mol. Genet. Genomics, 271, 103–110.
  9. Piszczek, E. und Gutman, W. (2007). Caspase-like proteases and their role in programmed cell death in plants. Acta Physiol. Plant. 29, 391–398.
  10. Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81(1):73-83.
  11. Rojo, E., Martin, R., Carter, C., Zouhar, J., Pan, S., Plotnikova, J., Jin, H., Paneque, M., Sa, J., Baker, B., Ausubel, F.M. und Raikhel, N.V., (2004). VPEγ exhibits a caspase- like activity that contributes to defense against pathogens. Curr. Biol. 14, 1897–1906.
  12. Xiang, T.T., Zong, N., Zou, Y., Wu, Y., Zhang, J. und Xing, W. (2008). Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18, 74-80.
  13. Lord, C.E.N. und Gunawardena, A.H.L.A.N. (2012). Programmed cell death in C. elegans, mammals and plants. EJCB 91: 603-613.
  14. Li, L., Ishdorj, G., Gibson, S.B. (2912). Reactive oxygen species regulation of autophagy in cancer: implications for cancer treatment. Free Radic Biol Med. 53(7):1399-410.
  15. Rubartelli, A. und Lotze, M.T. (2007). Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trend Immunol 28, 429-436.
  16. Isbat, M, Zeba, N., Kim, S.Rund Hong C.B.. (2009). A BAX inhibitor-1 gene in Capsicum annuum is induced under various abiotic stresses and endows multi-tolerance in transgenic tobacco. J Plant Physiol 166: 1685–1693.
  17. Juarez-Montiel, M., Ruiloba de Leon, S., Chavez-Camarillo, G., Hernandez- Rodriguez, C. und Villa-Tanaca, L. (2011). Huitlacoche (corn smut), caused by the phytopathogenic fungus Ustilago maydis, as a functional food. Rev Iberoam Micol 28, 69- 73.
  18. Steinberg, G. und Perez-Martin, J. (2008). Ustilago maydis, a new fungal model system for cell biology. Trend Cell Biol 18, 61-67.
  19. Mackey, D., Holt, B.F., Wiig, A. und Dangl, J.L. (2002). RIN4 Interacts with Pseudomonas syringae Type III Effector Molecules and Is Required for RPM1-Mediated Resistance in Arabidopsis. Cell 108: 743–754.
  20. Mackey, D., Belkhadir, Y., Alonso, J.M., Joseph R. Ecker, J.R. und Dangl, J.L. (2003). Arabidopsis RIN4 Is a Target of the Type III Virulence Effector AvrRpt2 and Modulates RPS2-Mediated Resistance. Cell 112: 379-389.
  21. Nürnberger, T. und Brunner, F. (2002). Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr. Opin. Plant Biol. 5: 318-324.
  22. Watanabe, N. und Lam, E. (2005). Two Arabidopsis Metacaspases AtMCP1b and AtMCP2b Are Arginine/Lysine-specific Cysteine Proteases and Activate Apoptosis-like Cell Death in Yeast. J. Biol. Chem. 280(15): 14691-14699.
  23. Wi, S.G., Singh, A.P., Lee, K.H. und Kim, Y.S. (2005). The pattern of distribution of pectin, peroxidase and lignin in the middle lamella of secondary xylem fibres in alfalfa (Medicago sativa). Annals of Botany 95, 863-868.
  24. Reape, T.J., Molony, E.M. und McCabe, P.F. (2008). Programmed cell death in plants: distinguishing between different modes. J. Exp. Bot. 59(3): 435–444.
  25. The plant apoplasm is an important recipient compartment for nematode secreted proteins. J. Exp. Bot. 62, 1241-1253.
  26. Rodríguez-Serrano, M., Bárány, I., Prem, D., Coronado, M.J., Risueño, M.C. und Testillano, P.S. (2012). NO, ROS, and cell death associated with caspase-like activity increase in stress-induced microspore embryogenesis of barley. J Exp Bot. 63(5):2007- Literaturverzeichnis 121
  27. Zhang, J. und Zhou, J.M. (2010). Plant immunity triggered by microbial molecular signatures. Mol Plant 3, 783-793.
  28. Seo, P.J., Lee, A.-K., Xiang, F. und Park, C.-M. (2008). Molecular and functional profiling of Arabidopsis pathogenesis-related genes: In-sights into their roles in salt response of seed germination. Plant Cell Physiol. 49: 334–344.
  29. Xiang, T.T., Zong, N., Zhang, J., Chen, J.F., Chen, M.S. und Zhou, J.M. (2011). BAK1 is not a target of the Pseudomonas syringae effector AvrPto. Mol. Plant Microbe Interact. 24, 100-107.
  30. Kim, K.S., Min, J.Y. und Dickman MB. (2008). Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol Plant Microbe Interact. 21(5):605-12.
  31. Naito, K., Taguchi, F., Suzuki, T., Inagaki, Y., Toyoda, K., Shiraishi, T. und Ichinose, Y. (2008). Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol Plant Microbe Interact 21:1165-1174.
  32. Rodriguez, J. und Lazebnik, Y. (1999). Caspase-9 and APAF-1 form an active holoenzyme. Genes Dev. 13: 3179-3184.
  33. Reape, T.J. und McCabe, P.F. (2008). Apoptotic-like programmed cell death in plants. New Phytologist 180: 13–26.
  34. Systemic virus-induced gene silencing allows functional characterization of maize genes during biotrophic interaction with Ustilago maydis. New Phytol 189, 471-483.
  35. N.R., Devera, M.E., Liang, X., Tor, M. und Billiar, T. (2007). The grateful dead: damage- associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220, 60-81.
  36. Shao, F., Golstein, C., Ade, J., Stoutemyer, M., Dixon, J.E. und Innes, R.W. (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301, 1230–1233.
  37. Mizushima, N., Yoshimori, T. und Ohsumi, Y. (2011). The Role of Atg Proteins in Autophagosome Formation. Annu. Rev. Cell Dev. Biol. 2011. 27:107–32
  38. Klionsky, D.J. (2005). The molecular machinery of autophagy: unanswered questions. J Cell Sci 118:7–18.
  39. Shen, H.M. und Codogno, P. (2011). Autophagic cell death: Loch Ness monster or endangeres species? Autophagy 7: 457-465.
  40. Stergiopoulos, I. und de Wit, P.J. (2009). Fungal effector proteins. Annu Rev Phytopathol 47, 233-263.
  41. Mentlak, T.A., Kombrink, A., Shinya, T., Ryder, L.S., Otomo, I., Saitoh, H., et al. (2012). Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24, 322-335.
  42. und de Wit, P.J. (2005). Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308, 1783-1786.
  43. van der Hoorn, R.A.L., de Wit, P.J.G.M. und Joosten, M.H.A.J. (2002). Balancing selection favors guarding resistance proteins. Tr. Plant Sci. 7, 67-71.
  44. Sanjuan, M.A., Dillon, C.P., Tait, S.W., Moshiach, S., Dorsey, F., Connell, S. et al. (2009). Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450: 1253–1257.
  45. Williams, B. und Dickman, M. (2008). Plant programmed cell death: can't live with it; can't live without it. Mol. Plant Pathol. 9, 531-544.
  46. Klionsky, D.J., Cregg, J.M., Dunn, W.A. Jr., Emr, S.D., Sakai, Y., Sandoval, I.V., Sibirny, A., Subramani, S., Thumm, M., Veenhuis, M. und Ohsumi Y. (2003). A unified nomenclature for yeast autophagy-related genes. Dev Cell 5:539–545.
  47. van der Linde, K., Hemetsberger, C., Kastner, C., Kaschani, F., van der Hoorn, R.A.L., Kumlehn, J. und Doehlemann, G. (2012). A Maize Cystatin Suppresses Host Immunity by Inhibiting Apoplastic Cysteine Proteases. Plant Cell 24, 1285-1300.
  48. Lenz, H.D., Haller, E., Melzer, E., Kober, K., Wurster, K., Stahl, M., Bassham D.C., Vierstra, R.D, Parker, J.E., Bautor J, Molina, A., Escudero, V., Shindo, T., van der Hoorn, R.A., Gust, A.A. und Nürnberger, T. (2011). Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 66(5):818-30.
  49. Pandey, S.P. und Somssich, I.E. (2009) The role of WRKY transcription factors in plant immunity. Plant physiol. 150, 1648-55.
  50. Vlot, A.C., Dempsey, D.A. und Klessig, D.F. (2009). Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol, Vol 49 47: 177-206.
  51. van der Hoorn, R.A.L. (2008). Plant Proteases: From phenotypes to molecular mechanisms. Annu. Rev. Plant Biol. 59, 191-223.
  52. O'Connell, R. J. und Panstruga, R. (2006). Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171(4): 699-718.
  53. Schulze-Lefert, P. und Panstruga, R. (2003). Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu. Rev. Phytopathol. 41:641–667.
  54. Vanholme, B., De Meutter, J., Tytgat, T., Van Montagu, M., Coomans, A. und Gheysen, G. (2004). Secretions of plant-parasitic nematodes: a molecular update. Gene 332, 13-27.
  55. Koeck, M., Hardham, A.R. und Dodds, P.N. (2011). The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell. Microbiol. 13, 1849-1857.
  56. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N. und Sasakawa, C. (2005). Escape of intracellular Shigella from autophagy. Science 307, 727-731.
  57. van den Burg, H.A., Spronk, C.A., Boeren, S., Kennedy, M.A., Vissers, J.P., Vuister, G.W., de Wit, P.J. und Vervoort, J. (2004). Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein-protein interactions: the chitin-binding site of AVR4 represents a novel binding site on the folding scaffold shared between the invertebrate and the plant chitin-binding domain. J Biol Chem 279, 16786-16796.
  58. Abgrenzung der Eigenleistung Die in dieser Arbeit präsentierten Ergebnisse wurden von mir selbstständig und ohne andere als die hier aufgeführte Hilfe durchgeführt. Dabei erfolgte die Konzipierung der Experimente in Zusammenarbeit mit meinem Betreuer PD Dr. Gunther Döhlemann.
  59. Kamoun, S. (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol. 44: 41-60.
  60. Vleeshouwers, V.G., Driesprong, J.D., Kamphuis, L.G., Torto-Alalibo, T., Van't Slot, K.A., Govers, F., Visser, R.G., Jacobsen, E. und Kamoun, S. (2006) Agroinfection- based high-throughput screening reveals specific recognition of INF elicitins in Solanum. Mol Plant Pathol 7:499–510.
  61. Zimmerman, M., Yurewicz, E. und Patel, G. (1976). A new fluorogenic substrate for chymotrypsin. Anal. biochem. 70, 258-262.
  62. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol. Biol. 32:1125-1134.
  63. Lorenzo, H.K., Susin, S.A., Penninger, J. und G. Kroemer, G. (1999). Apoptosis inducing factor (AIF): a phylogenetically old, caspase-independent effector of cell death. Cell Death and Differentiation 6: 516-524.
  64. Potten, C. und Wilson, J., (2004). Apoptosis – The Life and Death of Cells. Cambridge University Press, Cambridge.
  65. Watanabe, N. und Lam, E. (2006). Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45: 884–894.
  66. Moscou, M.J. und Bogdanove, A.J. (2009). A simple cipher governs DNA recognition by TAL effectors. Science 326:1501.
  67. Whisson, S.C., Boevink, P.C., Moleleki, L., Avrova, A.O., Morales, J.G., Gilroy, E.M., Armstrong, M.R., Grouffaud, S., van West, P., Chapman, S., et al. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450, 115-118.
  68. Xie, Z. und Klionsky, D.J. (2007). Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9:1102–1109.
  69. Seay, M., Patel, S. und Dinesh-Kumar, S.P. (2006). Autophagy and plant innate immunity. Cell. Microbiol. 8, 899-906.
  70. Klionsky, D.J. (2007). Autophagy: from phenomenology to molecular understanding in less then a decade. Net. Rev. Mol. Cell Biol. 8:931-37
  71. Liu, Y., Schiff, M., Czymmek, K., Talloczy, Z., Levine, B. und Dinesh-Kumar, S.P. (2005). Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567-577.
  72. Xu, Q. und Reed, J.C. (1998). Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol. Cell 1: 337-346.
  73. Überexpression auf die U. maydis/Gerste-Interaktion angefertigt, sowie die zugehörigen Daten zur Quantifikation von DAB-und Trypanblau-positiven Zellen erhoben.
  74. Ein Dank gilt natürlich auch Dr. Bernd Zechmann für die Bereitschaft zur Kooperation, für viele freundliche Telefonate und vor allem für die guten TEM-Aufnahmen.
  75. Dr. Bernd Zechmann hat im Rahmen einer Kooperation transmissionselektronenmikroskopische Untersuchun- gen zu kompatiblen und inkompatiblen Interaktionen im Ustilago/Gerste-Pathosystem durchgeführt und die in Abb. 24 dargestellten Aufnahmen angefertigt.
  76. Schipper, K. (2009). Charakterisierung eines Ustilago maydis Genclusters, das für drei neuartige sekretierte Effektoren kodiert. Dissertation, Philipps-Universität Marburg.
  77. Compatibility in the maize -Ustilago maydis interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. Plos Pathog. 9, 1-13.
  78. Mathre, D.E. (1997). Compendium of barley diseases. American Phytopathological Society Press, St. Paul, Minn. USA.
  79. Complex Initiates an Apoptotic Protease Cascade. Cell 91: 479–489.
  80. Oerke, E.-C. (2006). Crop losses to pests; centenary review. Journal of Agricultural Science (2006), 144, 31–43.
  81. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. und Wang, X. (1997). Cytochrome c and dATP-Dependent Formation of Apaf-1/Caspase-9
  82. Vielen lieben Dank natürlich auch an Nina Neidig und Nancy Stolle. Danke für die gemein- same Zeit, die vielen Gespräche, Unterstützung, Durchhaltevermögen und dass wir so gute Freunde geworden sind.
  83. Danke natürlich auch an die Mitglieder der AGs Kahmann und Zuccaro, past and present, für viele Hilfestellungen, Gespräche und Unterstützung. Ein besonderer Dank geht hier an Ria, Anita und Stefan, die den Laboralltag um ein Vielfaches erleichtern.
  84. Ein überaus großer Dank geht an Daniela Aßmann für Expertise, viele Gespräche, das mehr als selbstverständliche Engagement bei der täglich neuen Meisterung aller hordei- Hürden und die beste Boxen-Nachbarschaft ever. Danke Dani, es hat viel Spaß gemacht! Gleichzeitig gilt mein Dank natürlich auch allen aktuellen und ehemaligen Mitgliedern der AG Döhlemann, die den Laboralltag zu etwas Besonderem gemacht haben.
  85. Dennoch möchte ich an dieser Stelle einige Personen hervorheben.
  86. Des Weiteren möchte ich den Mitgliedern meiner Prüfungskommission Herrn Prof. Dr.
  87. Levine, B. und Klionsky, D.J. (2004). Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6:463–477.
  88. Lenz, H.D. (2011). Die Rolle autophagie-assoziierter Proteine in der pflanzlichen Immunantwort. Dissertation. Eberhard Karls Universität. Tübingen.
  89. Jia, Y., McAdams, S.A., Bryan, G.T., Hershey, H.P. und Valent, B. (2000). Direct interaction of resistance gene and avirulation gene products confers rice blast resistance.
  90. Sanger, F., Nicklen, S. und Coulson, A.R. (1977). DNA sequencing with chain- terminating inhibitors. PNAS USA 74: 5463-5467.
  91. Reed, J.C. (1997). Double identity for proteins of the Bcl-2 family. Nature 387: 773-776.
  92. Li, L.Y., Luo, X. und Wang, X. (2001). Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412: 95–99.
  93. Michael Bölker und Herrn Prof. Dr. Erhard Bremer für die Begleitung meiner Arbeit im Rahmen des ‚Thesis Advisory Committee'.
  94. Kawai, M., Pan, L., Reed, J.C. und Uchimiya, H. (1999). Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast. FEBS Lett 464: 143–147.
  95. Kale, S.D., Gu, B., Capelluto, D.G., Dou, D., Feldman, E., Rumore, A., Arredondo, F.D., Hanlon, R., Fudal, I., Rouxel, T., et al. (2010). External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142, 284-295.
  96. Neidig, N. (2013). Funktionelle Analyse des Ustilago maydis Effektorproteins Tin3 im Gencluster 19A. Dissertation. Philipps-Universität Marburg.
  97. van der Linde, K. (2011). Funktionelle Charakterisierung von Wirtsgenen in der Ustilago maydis – Mais-Interaktion. Dissertation. Philipps-Universität Marburg.
  98. Sidhu, G. und Person, C. (1971). Genetic control of virulence in Ustilago hordei. II.
  99. Rowell, J.B. und DeVay, J.E. (1954). Genetics of Ustilago zea in relation to basic problems of its pathogenicity. Phytopathology 44: 356-362.
  100. Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of TEs. Plant Cell 24, 1733-1745
  101. Oerke, E.C. und Dehne, H.W. (1997) Global crop production and the efficacy of crop protection: Current situation of future trends. Eur. J. Plant Pathol. 103: 203-215.
  102. Dr. Gunther Döhlemann hat die in Abb. 19 dargestellten mikroskopischen Aufnahmen zur Auswirkung der BI-1-
  103. Suzuki, K., Kubota, Y., Sekito, T. und Ohsumi, Y. (2007). Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12:209–18
  104. Kiesling, R.L. (1952). Histological studies on covered smut of barley. Ph.D. thesis, Department of Plant Pathology, University of Wisconsin, Madison, Wis. USA Kim, H.E., Du, F., Fang, M. und Wang, X. (2005). Formation of apoptosome is initiated by cytochrome c-induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-
  105. Uren, A.G., Karen O'Rourke, K., Aravind, L., Pisabarro, M.T., Seshagiri, S., Koonin, E.V. und Dixit, V.M. (2000). Identification of Paracaspases and Metacaspases: Two Ancient Families of Caspase-like Proteins, One of which Plays a Key Role in MALT Lymphoma. Molecular Cell 6: 961–967.
  106. Jamir, Y., Guo, M., Oh, H.S., Petnicki-Ocwieja, T., Chen, S., Tang, X., Dickman, M.B., Collmer, A. und Alfano, J.R. (2004). Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J. 37, 554– 565.
  107. Im Folgenden werden weitere, an dieser Arbeit beteiligte Personen sowie deren experi- mentelle Beiträge genannt: Daniela Aßmann hat sämtliche PCR-basierten Untersuchungen zur Verifizierung der U. hordei-Deletions- mutanten durchgeführt (Abb. 13) und war maßgeblich an der in Abb. 14 dargestellten Quantifizierung der Pilzbesiedelung beteiligt.
  108. Morris, S.W., Vernooij, B., Titatarn, S., Starrett, M., Thomas, S., Wiltse, C.C., Frederiksen, R.A., Bhandhufalck, A., Hulbert, S. und Uknes, S. (1998). Induced resistance responses in maize. Mol Plant Microbe Interact 11(7): 643-658.
  109. Tsukuda, T., Carleton, S., Fotheringham, S. und Holloman, W.K. (1988). Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol. Cell. Biol. 8: 3703-3709.
  110. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Snow, B.E., Brothers, G.M. et al. (1999). Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397: 441–446.
  111. Sambrook, J., Frisch, E.F. und Maniatis, T. (1989). Molecular Cloning: A laboratory manual. Cold Spring Harbour, New York.
  112. Mudgett, M.B. (2005). New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56:509-531.
  113. Memelink, J., Verpoorte, R. und Kijne, J.W. (2001). ORCAnization of jasmonate- responsive gene expression in alkaloid metabolism. Trends Plant Sci 6, 212-219.
  114. OverexpressionofBax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. Plant J 33: 425–434.
  115. Massey, .A, Kiffin, R. und Cuervo, A.M. (2004). Pathophysiology of chaperone- mediated autophagy. Int J Biochem Cell Biol 2004;36:2420–2434.
  116. Yaeno, T., Li, H., Chaparro-Garcia, A., Schornack, S., Koshiba, S., Watanabe, S., Kigawa, T., Kamoun, S., Shirasu, K. (2011). Phosphatidylinositol monophosphate- binding interface in the oomycete RXLR effector AVR3a is required for its stability in host Literaturverzeichnis 126 cells to modulate plant immunity. Proc Natl Acad Sci USA, 108:14682-14687.
  117. van der Biezen, E.A. und Jones, J.D.G. (1998). Plant disease-resistance proteins and the gene-for-gene concept. Trends Plant Sci. 23: 454-456.
  118. Römer, P., Hahn, S., Jordan, T., Strauß, T., Bonas, U. und Lahaye, T. (2007). Plant- pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:645-648.
  119. Zipfel, C. und Felix, G. (2005). Plants and animals: a different taste for microbes? Curr. Opin. Plant Biol. 8: 353-360.
  120. Melotto, M., Underwood, W., Koczan, J., Nomura, K. und He, S.Y. (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969-980.
  121. Shah, J. (2009). Plants under attack: systemic signals in defense. Curr. Opin. In Plant Biol. 12:459-464
  122. Nimchuk, Z., Eulgem, T., Holt, B.F. und Dangl, J.L. (2003). Recognition and response in the plant immune system. Annu. Rev. Genet. 37: 579-609.
  123. Pfaffl, M.W., Horgan, G.W. und Dempfle, L. (2002). Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30: 1–10.
  124. Morgan, W. und Kamoun, S. (2007). RXLR effectors of plant pathogenic oomycetes.
  125. Segregations for higher levels of virulence. Can. J. Genetics and Cytology 13:173–178.
  126. van Loon, L.C., Rep, M. und Pieterse, C.M.J. (2006). Significance of Inducible Defense- related Proteins in Infected Plants. Annu. Rev. Phytopathol. 44:135–62.
  127. Rep, M. (2005) Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol Lett 253: 19-27.
  128. Scholze H. und Boch J. (2011) TAL effectors are remote controls for gene activation. Curr. Oprin. Bicrobiol. 14:47-53
  129. Wawra, S., Agacan, M., Boddey, J.A., Davidson, I., Gachon, C.M., Zanda, M., Grouffaud, S., Whisson, S.C., Birch, P.R., Porter, A.J. et al. (2012). The avirulence protein 3a (AVR3a) from the potato pathogen Phytophthora infestans, forms homodimers through its predicted translocation region and does not specifically bind phospholipids. J Biol Chem 287:38101-38109.
  130. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schafer, W., Martin, T., Herskowitz, I. und 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.
  131. Morel, J.B. und Dangl, J.L. (1997). The hypersensitive response and the induction of cell death in plants. Cell Death Diff 4, 671-683.
  132. Lamb, C. und Dixon, R.A. (1997). The oxidative burst in plant disease resistance. Annu rev Plant physiol plant mol biol 48, 251-275.
  133. Jones, J.D. und Dangl, J.L. (2006). The plant immune system. Nature 444, 323-329.
  134. Wang, C. und Youle, R.J. (2009). The role of mitochondria in apoptosis. Ann. Rev.
  135. Mathow, D. (2011). Transkriptomanalyse von Ustilago hordei während der Infektion von Gerste. Masterarbeit. Philipps-Universität Marburg.
  136. Levine, B. und Deretic, V. (2007). Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 7:767–777.
  137. Ustilago maydis, the causative agent of corn smut disease. Fungal Pathology. Kronstad, J.W. (ed.). Kluwer academic publishers. Dodrecht, The Netherlands: 347-371.
  138. Leist, M. und Jäättelä, M. (2001). Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol. 2(8):589-598.
  139. Mendgen, K. und Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 7(8): 352-356.
  140. Leib, K. (2005). Untersuchungen zum Resistenzmechanismus der Gerste (Hordeum vulgare L.) gegenüber dem Gerstenmehltaupilz (Blumeria graminis f. sp. hordei).
  141. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330, 1546-1548.
  142. Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazebnik, Y.A., et al. (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376(6535):37-43.
  143. Snetselaar, K.M. und Mims, C.W. (1994). Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol. Res. 98: 347-355.
  144. Snetselaar, K.M. und Mims, C.W. (1992). Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologica 84: 193-203.
  145. Janjusevic, R., Abramovitch, R. B., Martin, G. B. und Stebbins, C. E. (2006). A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311, 222–226.
  146. Kay, S., Hahn, S., Marois, E., Hause, G. und Bonas, U. (2010). A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 2007, 318:648- 651.
  147. Skibbe, D.S., Doehlemann, G., Fernandes, J. und Walbot, V. (2010) Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science, 328, 89–92.
  148. Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J. 59(3):461-74.
  149. Jan, N., Mahboob-ul-Hussain und Andrabi, K.I. (2008). Programmed cell death or apopto-sis: do animals and plants share anything in common. Biotechnol. Mol. Biol. Rev. 3, 111–126.
  150. Thornberry, N.A., Rano, T.A., Peterson, E.P., Rasper, D.M., Timkey, T., Garcia-Calvo, M., Houtzager, V.M., Nordstrom, P.A., Roy, S., Vaillancourt, J.P., Chapman, K.T. und Nicholson, D.W. (1997). A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem. 272(29):17907-11.
  151. Ishikawa, T., Watanabe, N., Nagano, M., Kawai-Yamada, M. und Lam, E. (2011). Bax inhibitor-1: a highly conserved endoplasmic reticulum-resident cell death sup-pressor. Cell Death Differ. 18, 1271–1278.
  152. Lam, E., Kato, N. und Lawton, M. (2001). Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 484-453.
  153. Kim, H.S., Desveaux, D., Singer, A.U., Patel, P., Sondek, J., Dangl, J.L. (2005). The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc. Natl. Acad. Sci. U.S.A. 102, 6496–6501
  154. Reggiori, F. und Klionsky, D.J. (2002). Autophagy in the eukaryotic cell. Eukaryot Cell 1:11–21.
  155. Linning, R., Lin, D., Lee, N., Abdennadher, M., Gaudet, D., Thomas, P., Mills, D., Kronstad, J. W. und 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.
  156. Mehdy, M.C. (1994). Active Oxygen Species in Plant Defense against Pathogens. Plant Physiol 105, 467-472.
  157. Levine, B. und Yuan, J. (2005). Autophagy in cell death: an innocent convict. J Clin Invest 115:2679–2688.
  158. Yorimitsu, T. und Klionsky, D.J. (2005). Autophagy: molecular machinery for self-eating. Cell Death Differ 12:1542–1552.
  159. Lacomme C. und Santa Cruz, S. (1999). Bax-induced cell death in tobacco is similar to the hypersensitive response. PNAS 96: 7956-7961.
  160. Rosebrock, T.R., Zeng, L., Brady, J.J., Abramovitch, R.B., Xiao, F. und Martin, G.B. (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature, 448, 370–374.
  161. van der Hoorn, R.A.L. und Kamoun, S. (2008). From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009-2017.
  162. Iriti, M. und Faoro, F. (2009). Chitosan as a MAMP, searching for a PRR. Plant signaling & behavior 4, 66-68.
  163. Zong, N., Xiang, T.T., Zou, Y., Chai, J., und Zhou, J.M. (2008). Blocking and triggering of plant immunity by Pseudomonas syringae effector AvrPto. Plant Sig. and Behavior 3:8, 583-585.
  164. Klionsky, D.J. et al. (2008). Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 4(2): 151–175.
  165. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 27: 135–144.
  166. Kroemer, G. und Levine, B. (2008). Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 9:1004–10
  167. Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E.S., Baehrecke, E.H., Blagosklonny, M.V., El-Deiry, W.S., Golstein, P., Green, D.R., Hengartner, M., Knight, R.A., Kumar, S., Lipton, S.A., Malorni, W., Nunez, G., Peter, M.E., Tschopp, J., Yuan, J., Piacentini, M., Zhivotovsky, B., Melino, G., (2009). Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16, 3–11.
  168. Kaffarnik, F., Müller, P., Leibundgut, M., Kahmann, R., und Feldbrügge, M. (2003) PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. Embo J 22: 5817-5826.
  169. Panstruga, R. und Dodds, P.N. (2009). Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324, 748-750.
  170. Kawai-Yamada, M., Hori, Z., Ogawa, T., Ihara-Ohori, Y., Tamura, K., Nagano, M., Ishikawa, T. und Uchimiya, H. (2009). Loss of calmodulin binding to Bax inhibitor-1 affects pseudomonas-mediated hypersensitive response-associated cell death in Arabidopsis thaliana. Journal of Biological Chemistry 284, 27998–28003.
  171. Xu, Q., Zhang, L., (2009). Plant caspase-like proteases in plant programmed cell death. Plant Signal. Behav. 4, 902–904.
  172. Wahl, R., Wippel, K., Goos, S., Kämper, J., Sauer, N. (2010). A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8: e1000308
  173. Thomma, B.P., Nürnberger, T. und Joosten, M.H. (2011). Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell. 23(1):4-15.
  174. Williams, B., Kabbage, M., Kim, H.J., Britt, R. und Dickman MB. (2011). Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog. 7(6):e1002107.
  175. van Doorn, W.G., Beers, E.P., Dangl, J.L., Franklin-Tong, V.E., Gallois, P., Hara- Nishimura, I., Jones, A.M., Kawai-Yamada, M., Lam, E., Mundy, J., Mur, L.A.J., Petersen, M., Smertenko, A., Taliansky, M., Van Breusegem, F., Wolpert, T., Woltering, E., Zhivotovsky, B., Bozhkov, P.V. (2011). Morphological classification of plant cell deaths. Cell Death Differ. 18, 1241–1246.
  176. Vartapetian, A. B., Tuzhikov, A. I., Chichkova, N. V., Taliansky, M. und Wolpert, T. J. (2011). A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ 18: 1289-1297.
  177. Kabbage, M., Williams, B. und Dickman, M.B. (2013). Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathog. 9(4):e1003287.
  178. Vaux, D.L. und Strasser, A. (1996). The molecular biology of apoptosis. PNAS 93: 2239- 2244.
  179. Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax inhibitor-1 (AtBI-1). Proc Natl Acad Sci USA 98: 12295–12300.
  180. Torres, M.A., Jones, J.D. und Dangl, J.L. (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiol 141, 373-378.
  181. Zhang, .L, Xu, Q., Xing, D., Gao, C. und Xiong, H. (2009). Real-time detection of caspase-3-like protease activation in vivo using fluorescence resonance energy transfer during plant programmed cell death induced by ultraviolet C overexposure. Plant Physiol. 150(4):1773-83.
  182. Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A. und de Vries, R.P. (2008). The secretome of the maize pathogen Ustilago maydis. Fungal Gen. Biol. 45: 63- 70.
  183. Schulze-Lefert, P. (2004). Knocking on heaven's wall: pathogenesis o fand resistance to biotrophic fungi at the plant cell wall. Curr. Opin. Plant Biol. 7: 377-383
  184. Mitou, G., Budak, H. und Gozuacik, D. (2009). Techniques to Study Autophagy in Plants. Int. J. Plant Genomics 2009.
  185. Watanabe, N. und Lam, E. (2009). Bax Inhibitor-1, a conserved cell death suppressor, is a key molecular switch downstream from a variety of biotic and abiotic stress signals in plants. Int J Mol Sci 10: 3149–3167.
  186. Kroemer, G., Galluzzi, L. und Brenner, C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99–163.
  187. Zipfel, C. (2009). Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol. 12(4):414-20.
  188. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D., Boller, T. und Felix, G. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749-760.

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