Research Group Nürnberger




Prof. Dr. T. Nürnberger
ZMBP - Center for Plant Molecular Biology
Plant Biochemistry
University of Tübingen
Auf der Morgenstelle 32
D-72076 Tübingen
Germany
phone: ++49-(0)7071-29-76658
fax: ++49-(0)7071-29-5226
email: nuernberger(at)zmbp.uni-tuebingen.de



Research

Pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) to microbial infection constitutes an evolutionarily ancient type of immunity that is characteristic of all multicellular eukaryotic systems. Microbial patterns activating plant PTI comprise bacterial flagellin, lipopolypolysaccharides, peptidoglycans or oomycete or fungus-derived proteins, peptides or glucan and chitin oligomers. Plant pattern recognition receptors mediate microbial pattern sensing and subsequent immune activation.

Our research aims at a deeper molecular understanding of microbial pattern recognition in plant immunity. In particular, we work on the identification of novel microbial patterns and their corresponding plant pattern recognition receptors. We further want to build cassettes of PRRs ('PRR stacking', PRR 'pyramiding') for conferring durable PTI to crop plants.

 

 

Identification of bacterial PAMPs and their cognate pattern recognition receptors, and exploitation of plant PRRs to engineer resistant crops

 

Over the past years, we have identified three microbe-associated patterns and their cognate pattern recognition receptors that trigger immunity-associated responses in Arabidopsis.

 

(I) Bacterial peptidoglycans (PGN) from S. aureus, E. coli, B. subtilis, P. syringae pv. tomato, or Xanthomonas campestris are recognized by a ternary complex made of three LysM domain proteins. GPI-anchored LYM1 and LYM3 proteins are implicated in PGN binding whereas CERK1, a LysM domain receptor kinase, mediates transmembrane signaling. We have further identified a plant lysozyme (LYS1) which is produced and secreted upon bacterial infection or pattern treatment. LYS1 is capable of releasing soluble PGN fragments from intact bacterial surfaces that serve as ligands for the LYM1 LYM3 CERK1 receptor. LYS1 as well as the PGN receptor complex contribute to plan immunity as genetic inactivation of the encoding genes resulted in enhanced bacterial growth.

Literature: Gust, JBC (2007); Willmann, PNAS (2011); Gust, TIPS (2012); Liu, eLife (2015)

 

 

(II) Necrosis and ethylene inducing protein 1-like proteins (NLPs) constitute a protein superfamily of which members are produced by various phytopathogenic bacteria, fungi and oomycetes. NLPs trigger leaf necrosis, and stimulate immunity-associated defenses in dicotyledonous plants, including Arabidopsis. Nlp20-mediated defenses are subject to microbial effector suppression. Arabidopsis and related Brassicaceae species respond to a 20-amino acid motif (nlp20) conserved within most NLP proteins with the activation of PTI. The nlp20 pattern is sensed by the leucine-rich repeat (LRR) receptor protein RLP23. RLP23 forms a constitutive heterodimeric complex with the LRR receptor kinase SOBIR1 and recruits the LRR-RK BAK1 upon ligand binding. RLP23 contributes to PTI and stable expression of RLP23 in potato confers enhanced immunity to infection against NLP-producing pathogens, such as Phytophthora infestans and Sclerotinia sclerotiorum.

Literature: Fellbrich, Plant J (2002); Qutob, Plant Cell (2006); He, Cell (2006), Shan, Cell Host Microbe (2008); Ottmann, PNAS (2009); Böhm, PLOS Pathogens (2014); Oome, PNAS (2014); Albert, Nature Plants (2015)

 

(III) Most proteobacteria produce a proteinaceous pattern that is recognized by the LRR receptor protein RLP32 in a manner mechanistically similar to RLP23.

 

NEP1-like Proteins as major microbial virulence factors

NLPs are major microbial virulence factors that are produced by numerous phytopathogenic bacteria, fungi or oomycetes. NLPs exert cytolytic activities on dicot plant cells, but not on monocot cells. 3D crystal structures of NLP proteins revealed significant fold conservation to pore-forming cytolytic toxins produced by marine organisms (actinoporins) or bacteria (hemolysins, aegerolysins), suggesting that NLPs belong to a superfamily of pore-forming toxins. NLPs bind to the sugar chains of glucosyl inositol phosporylceramides (GIPCs), the major plant sphingolipids. Host toxin sensitivity is brought about by the length of the glycosyl chain that determines proper positioning of the toxin prior to membrane insertion and pore formation. Monocot GIPCs usually carry longer glycosyl chains such as compared to those found in dicot GIPCs, thus explaining why monocot plants are largely tolerant to NLP cytolysins.

Literature: Qutob, Plant Cell (2006); Ottmann, PNAS (2009); Albert, Nature Plants (2015); Lenarcic, Science (2017)

 

Publications

Lenarcic T, Albert I, Böhm H, Hodnik V, Pirc K, Zavec AB, Podobnik M, Pahovnik D, Zagar E, Pruitt R, Greimel P, Yamaji-Hasegawa A, Kobayashi T, Zienkiewicz A, Gömann J, Mortimer JC, Fang L, Mamode-Cassim A, Deleu M, Lins L, Oecking C, Feussner I, Mongrand S, Anderluh G, Nürnberger T. Eudicot-specific sphingolipids determine host selectivity of microbial NLP cytolysins. Science 358: 1431-1434 (2017).

Gust AA, Pruitt R, Nürnberger T. Sensing Danger: Key to activating plant immunity. Trends Plant Sci 22:779-791 (2017).

Fan L, Chae E, Gust AA, Nürnberger T. Isolation of novel MAMP-like activities and identification of cognate pattern recognition receptors in Arabidopsis thaliana using next-generation sequencing (NGS)-based mapping. Curr Protoc. Plant Biol. DOI: 10.1002/cppb.20056 (2017).

Zhang L, Ni H, Du X, Wang S, Ma XW, Nürnberger T, Guo HS, Hua C. The Verticillium-specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections. New Phytol. 215: 368-381 (2017).

Reinhard, A., Nürnberger, T. Steady-state and kinetics-based affinity determination in effector-effector target interactions. Libo Shan & Ping He (Eds.) Edition Plant Pattern Recognition Receptors, Methods in Molecular Biology, Springer, 1578:81-108. doi: 10.1007/978-1-4939-6859-6_7 (2017).

Klionsky DJ, Abdelmohsen K, .. Nürnberger T, .. Zughaier SM. Guidelines for the use and interpretation of assays for monitoring autophagy III Autophagy 12: 1-222 (2016).

Albert, I., Böhm, H., Albert, M., Feiler, C.E., Imkampe, J., Wallmeroth, N., Brancato, C., Raaymakers, T.M., Oome, S., Zhang, H., Krol, E., Grefen, C., Gust, A.A., Chai, J., Hedrich, H., Van den Ackerveken, G., Nürnberger, T. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nature Plants doi:10.1038/nplants.2015.140 (2015).

Oome, S., Raaymakers, T.M., Cabral, A., Samwel, S., Böhm, H., Albert, A., Nürnberger, T., Van den Ackerveken, G. Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111:16955-16960 (2014).

Böhm, H., Albert, I., Oome, S., Raaymakers, T.M., Van den Ackerveken, G., Nürnberger, T. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immnity in Arabidopsis. PLOS Pathogens 10(11): e1004491. doi:10.1371/journal.ppat.1004491 (2014).

Antolin-Llovera, M., Petutschnig, E.M., Ried, M.K., Lipka, V., Nürnberger, T., Parniske, M., Robatzek, S. Knowing your friends and foes - plant receptor-like kinases as initiators of symbiosis or defence. New Phytol. 204:791-802 (2014).

Petutschnig, E.K., Stolze, M., Lipka, U., Kopischke, M., Horlacher, J., Valerius, O., Rozhon, W., Gust, A.A., Kemmerling, B., Poppenberger, B., Braus, G.H., Nürnberger, T., Lipka, V. A novel CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) mutant with enhanced pathogen-induced cell death and altered receptor procesing. New Phytol. 204:955-967 (2014).

Liu, X., Grabherr, H., Willmann, R., Kolb, D., Brunner, F., Bertsche, U., Kühner, D., Franz-Wachtel, M., Amin, B., Felix, G., Ongena, M., Nürnberger, T., Gust, A.A. Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis. eLIFE e01990 (2014).

Böhm, H., Albert, I., Fan, L., Reinhard, A., Nürnberger, T. Immune receptor complexes at the plant cell surface. Curr. Opin. Plant Biol. 20C:47-54 (2014).

Halter, T., Imkampe, J., Mazzotta, S., Wierzba, M., Postel, S., Bücherl, C., Kiefer, C., Stahl, M., Chinchilla, D., Wang, X., Nürnberger, T., Zipfel, C., Clouse, S., Borst, J.W., Boeren, S., de Vries, S.C., Tax, F., Kemmerling, B. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr. Biol. 24:134-143 (2014).

Wawra, S., Djamei, A., Küfner, I., Nürnberger, T., Kahmann, R., van West, P. In vitro translocation experiments with RXLR-reporter fusion proteins of Avr1b from Phytophthora sojae and AVR3a from Phytophthora infestans fail to demonstrate autonomous uptake in plant and animal cells. Mol. Plant-Microbe Interact. 26:528-536 (2013).

Tintor, N., Ross, A., Kanehara, K., Yamada, K., Fan, L., Kemmerling, B., Nürnberger, T. , Tsuda, K., Saijo, Y. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc. Natl. Acad. Sci. U.S.A. 110:6211-6216 (2013).

Santhanam, P., Esse, P., Albert, I., Faino, L., Nürnberger, T., Thomma, B. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant-Microbe Interact. 26:278-286 (2013).

Klionsky DJ, Abdalla FC, .. Nürnberger T, .. Zuckerbraun B. Guidelines for the use and interpretation of assays for monitoring autophagy II. Autophagy 4:445-544 (2012).

Willmann, R., Nürnberger, T. How plant lysin motif receptors get activated: lessons learned from structural biology. Sci Signal. 5:pe28 (2012).

Gust, A.A., Nürnberger, T. Plant Immunology: A life or death switch. Nature 486:198-199 (2012).

Gust, A.A., Willmann, R., Desaki, Y., Grabherr, H.M., Nürnberger, T. Plant LysM proteins: Modules mediating symbiosis and immunity. Trends Plant Sci. 17:495-502 (2012).

Brunner, F., Nürnberger, T. Identification of immunogenic microbial patterns takes the fast lane. Proc. Natl. Acad. Sci. U.S.A 109:4029-4030 (2012).

Cabral, A., Oome, S., Sander, N., Küfner, I., Nürnberger, T., Van den Ackerveken, G. Non-toxic Nep1-like proteins of the downy mildew pathogen Hyaloperonospora arabidopsidis; repression of necrosis-inducing activity by a surface-exposed region. Mol. Plant-Microbe Interact. 25:697-708 (2012).

Willmann, R., Lajunen, H.M., Erbs, G., Newman, M.A., Kolb, D., Tsuda, K., Katagiri, F., Fliegmann, J., Bono, J.-J., Cullimore, J.V., Jehle, A.K., Götz, F., Kulik, A., Molinaro, A., Lipka, V., Gust, A.A., Nürnberger, T. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl. Acad. Sci. U.S.A 108:19824-19829 (2011).

Kemmerling, B., Halter, T., Mazzotta, S., Mosher, S., Nürnberger, T. A genome-wide survey for Arabidopsis leucine-rich repeat receptor kinases implicated in plant immunity. Frontiers Plant Biol. 2:88 doi:10.3389/fpls.2011.00088 (2011).

Reiss, K., Kirchner, E., Gijzen, M., Zocher, G., Löffelhardt, B., Nürnberger, T., Stehle, T., Brunner, F. Structural and phylogenetic analyses of the GP42 transglutaminase from Phytophthora sojae reveal an evolutionary relationship between oomycetes and marine Vibrio bacteria. J. Biol. Chem. 286:42585-42593 (2011).

Lenz, H.D., Vierstra, R.D., Nürnberger, T., Gust, A.A. ATG7 contributes to plant basal immunity towards fungal infection. Plant Signal. Behav. 6:1040-1042 (2011).

Lenz, H.D., Haller, E., Melzer, E. Gust, A.A., Nürnberger, T. Autophagy controls plant basal immunity in a pathogenic lifestyle-dependent manner. Autophagy 7:773-774 (2011).

Thomma, B.P.H.J., Nürnberger, T., Joosten, M.H.A.J. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4-15 (2011).

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.L., Gust, A.A., Nürnberger, T. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 66:818-830 (2011).

Nürnberger, T., Küfner, I. The role of the plasma membrane in microbial sensing and innate immunity. Plant Cell Monographs Vol. 19 (Eds. A. Murphy, W. Peer, B. Schulz,). Springer-Verlag Heidelberg. P. 471-483 (2011).

Haapalainen, M., Engelhardt, E., Küfner, I., Li, C.-M., Nürnberger, T., Lee, J., Romantschuk, M., Taira, S. Functional mapping of harpin HrpZ of Pseudomonas syringae reveals the sites responsible for protein oligomerization, lipid interactions and plant defence induction. Mol. Plant Pathol. 12:151-166 (2011).

Brock, A.K., Willmann, R., Kolb, D., Grefen, L., Lajunen, H.M., Bethke, G., Lee, J., Nürnberger, T., Gust, A.A. The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Physiol. 153:1098-1111 (2010).

Gust, A., Brunner, F., Nürnberger, T. Biotechnological concepts for improving plant immunity. Curr. Opin. Biotechnol. 21:1-7 (2010).

Postel, S., Küfner, I., Beuter, C., Mazzotta, S., Schwedt, A., Borlotti, A., Halter, T., Kemmerling, B., Nürnberger, T. The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur. J. Cell Biol. 89:169-174 (2010).

Küfner, I., Ottmann, C., Oecking, C., Nürnberger, T. Cytolytic toxins as triggers of plant immune response. Plant Signal. Behav.4, 977-979 (2009).

Ottmann, C., Luberacki, B., Küfner, I., Koch, W., Brunner, F., Weyand, M., Mattinen, L., Pirhonen, M., Anderluh, G., Seitz, H.U., Nürnberger, T.*, Oecking; C.* A common toxin fold mediates microbial attack and plant defense. Proc. Natl. Acad. Sci. USA 25:10359-10364 (2009).

Nürnberger, T., Kemmerling, B. Pathogen-associated molecular patterns (PAMP) and PAMP-triggered immunity. Annu. Plant Rev. 34:16-47, edited by J. Parker, Wiley-Blackwell (2009).

Motteram, J., Küfner, I., Deller, S., Brunner, F., Hammond-Kosack, K.E., Nürnberger, T., Rudd, J.J. Molecular characterization and functional analysis of MgNLP; the sole NPP1-domain containing protein from the fungal wheat leaf pathogen Mycosphaerella graminicola. Mol. Plant Microbe Interact. 22:790-799 (2009).

Nürnberger, T., Kemmerling, B. PAMP-triggered basal immunity in plants. Adv. Bot. Res. 51:2-38, edited by L.C. Van Loon, Elsevier Publishers (2009).

Kumar, M., Busch, W., Birke, H., Kemmerling, B., Nürnberger, T., Schöffl, F. Heat shock factors HsfB1 and HsfB2 are involved in the regulation of PDF1.2 expression and pathogen resistance in Arabidopsis. Mol. Plant 2:152-165 (2009).

Engelhardt, S., Lee, J., Gäbler, Y., Kemmerling, B., Haapalainen, M.-L., Li, C.-M., Wei, Z., Keller, H., Joosten, M., Taira, S., Nürnberger, T. Separable roles of the Pseudomonas syringae pv. phaseolicola accessory protein HrpZ1 in ion-conducting pore formation and activation of plant immunity. Plant J. 57:706-717 (2009).

Shan, L., He, P., Li, J., Heese, A., Peck, S.C., Nürnberger, T., Martin, G.B., Sheen, J. Bacterial Effectors Target BAK1 to Disrupt MAMP Receptor Signaling Complexes and Impede Plant Innate Immunity. Cell Host Microbe 4:17-27 (2008).

Sanabria, N., Goring, D., Nürnberger, T., Dubery, I. Self/non-self perception and recognition mechanisms in plants; a comparison of self-incompatibility and innate immunity. New Phytol. 178:503-514 (2008).

Nürnberger, T., Kemmerling, B. Pathogen-associated molecular patterns (PAMP) and PAMP-triggered immunity. In: Annual Plant Reviews Vol. 34. Plant Disease Resistance. Blackwell Publishing. Pp. 16-47 (2008).

Kemmerling, B., Nürnberger, T. Brassinosteroid-independent functions of the BRI1-Associated kinase BAK1/SERK3. Plant Signal. Behav. 3, 116-119 (2008).

Kemmerling, B., Schwedt, A., Rodriguez, P., Mazzotta, S., Nürnberger, T. The Arabidopsis BRI1-Associated receptor Kinase 1 (BAK1) controls infection-induced cell death and immunity to necrotrophic fungal infection. In: Biology of Plant-Microbe Interactions Voil. 6, Chapter 7 (CD ISBN 978-0-9654625-5-6) (2008).

Nürnberger, T. The type III secretion sytem of phytopathogenic bacteria. Int. J. Med. Microbiol. 297S1, 30 (2007).

Gust, A.A., Biswas, R., Lenz, H.D., Rauhut, T., Ranf, S., Kemmerling, B., Götz, F., Glawischnig, E., Lee, J., Felix, G., Nürnberger, T. Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J. Biol. Chem. 282, 32338-32348 (2007).

Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nürnberger, T., Jones, J.D.G., Felix, G., Boller, T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defense. Nature 448, 497-500 (2007).

Kemmerling, B., Schwedt, A., Rodriguez, P., Mazzotta, S., Frank, M., Abu Qamar, S., Mengiste, T., Betsuyaku, S., Parker, J.E., Müssig, C., Thomma, B.P.H.J., Albrecht, C., de Vries, S.E., Hirt, H., Nürnberger, T. A brassinolide-independent role for the BRI1 Associated receptor Kinase 1 (BAK1) in plant cell death control. Curr. Biol. 17, 1116-1122 (2007).

Diepold, A., Li, G., Lennarz, W.J., Nürnberger, T., Brunner, F. The Arabidopsis Atpng1 gene encodes a peptide:N-glycanase. Plant J. 52, 94-104 (2007).

Qutob, D., Kemmerling, B., Brunner, F., Küfner, I., Engelhardt, S., Gust, A.A., Luberacki, B., Seitz, H.U., Stahl, D., Rauhut, T., Glawischnig, E., Schween, G., Lacombe, B., Watanabe, N., Lam, E., Schlichting, R., Scheel, D., Nau, K., Dodt, G., Hubert, D., Gijzen, M., Nürnberger, T. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18, 3721-3744 (2006).

Nürnberger, T., Kemmerling, B. Receptor protein kinases - pattern recognition receptors in plant immunity. Trends Plant Sci. 11, 519-522 (2006).

He, P., Shan, L., Lin, N.-C., Martin, G.B, Kemmerling, B., Nürnberger, T., Sheen, J. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563-575 (2006).

Gijzen, M., Nürnberger, T. Necrosis-inducing proteins from plant pathogens: Recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67, 1800-1807 (2006).

Nürnberger, T., Kemmerling, B. Signal perception and transduction in plant innate immunity. In: Communication in plants. (Baluska, F., Mancuso, S. Volkmann, D., eds.) Springer-Verlag Berlin-Heidelberg, 95-109 (2006).

Racape, J., Belbahri, L., Engelhardt, S., Lacombe, B., Lee, J., Lochman, J., Marais, A., Nicole, M., Nürnberger, T., Parlange, F., Puverel, S., Keller, H. Ca2+-dependent lipid binding and membrane integration of PopA, a harpin-like elicitor of the hypersensitive response in tobacco. Mol. Microbiol. 58, 1406-1420 (2005).

Nürnberger, T., Lipka, V. Non-host resistance in plants - an overview. Mol. Plant Pathol. 6, 335-345 (2005).

Halim, V.A., Hunger, A., Macioszek, V., Landgraf, P., Nürnberger, T., Scheel, D., Rosahl, S. The oligopeptide

elicitor Pep-13 induces salicylic acid-dependent and - independent defense reactions in potato. Physiol. Mol. Plant Pathol. 64, 311-318 (2005).

Li, C.M., Haapalainen, M., Lee, J., Nürnberger, T., Romantschuk, M., Taira, S. Harpin of Pseudomonas syringae pv. phaseolicola harbours a protein binding site. Mol. Plant Microbe Interact. 18, 60-66 (2005).

Piater, L.A., Nürnberger, T., Dubery, I.A. Identification of a lipopolysaccharide responsive erk-like MAP kinase in tobacco leaf tissue. Mol. Plant Pathol. 5, 331-342 (2004).

Lee, J., Nürnberger, T. Is pore formation activity of HRP Z required for defense activation in plant cells? In: Developments in Plant Pathology Vol. 10, Kluwer Academic Publishers, Dordrecht, pp. 165-173 (2004).

Nürnberger, T., Brunner, F., Kemmerling, B., Piater, L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198, 249-266 (2004).

Scheel, D., Hahlbrock, K., Jabs, T., Nürnberger, T., Sacks, W.R. Specific recognition of a fungal oligopeptide elicitor by parsley cells. In: Advances in Molecular Genetics of Plant-Microbe Interactions. (Daniels, M., ed.) Kluwer Academic Publishers Dordrecht, Boston, London Vol. 3, 313-318 (1994).

Hahlbrock, K., Bednarek, P., Ciolkowski, I., Hamberger, B., Heise, A., Liedgens, H., Logemann, E., Nürnberger, T., Schmelzer, E., Somssich, I.E., Tan, J. Non-self recognition, transcriptional reprogramming and secondary metabolite accumulation during plant/pathogen interactions. Proc. Natl. Acad. Sci. U.S.A 100, 14569-14576 (2003).

Kroj, T., Rudd, J.J., Nürnberger, T., Gäbler, Y., Lee, J., Scheel, D. Mitogen-activated protein kinases play an essential role in oxidative burst-independent expression of pathogenesis-related genes in parsley. J. Biol. Chem. 278, 2256-2264 (2003).

Brunner, F., Rosahl, S., Lee, J., Rudd, J.J., Geiler, C., Kauppinen, S., Rasmussen, G., Scheel, D., Nürnberger, T. Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J. 24, 6681-6688 (2002).

Fellbrich, G., Romanski, A., Varet, A., Blume, B., Brunner, F., Engelhardt, S., Felix, G., Kemmerling, B., Krzymowska, M., Nürnberger, T. NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J. 32, 375-390 (2002).

Nürnberger, T., Brunner, F. 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 (2002).

Varet, A., Parker, J., Tornero, P., Nass, N., Nürnberger, T., Dangl, J.L., Scheel, D., Lee, J. NHL25 and NHL3, two NDR1/HIN1-like genes in Arabidopsis thaliana with potential role(s) in plant defense. Mol. Plant Microbe Interact. 15, 608-616 (2002).

Brunner, F., Wirtz, W., Rose, J.K.C., Darvill, A.G., Govers, F., Scheel, D., Nürnberger, T. A ß-glucosidase/xylosidase from the phytopathogenic oomycete, Phytophthora infestans. Phytochemistry 59, 689-696 (2002).

Veit, S., Wörle, J.M., Nürnberger, T., Koch, W., Seitz, H.U. A novel protein elicitor (PaNie) from Pythium aphanidermatum induces dual defense responses in carrot and Arabidopsis. Plant Physiol. 127, 832-841 (2001).

Nürnberger, T., Scheel, D. Signal transmission in the plant immune response. Trends Plant Sci. 6, 372-379 (2001).

Luderer, R., Rivas, S., Nürnberger, T., Mattei, B., Van den Hooven, H.W., Van der Hoorn, R.A.L., Romeis, T., Wehrfritz, J.-M., Blume, B., Nennstiel, D., Zuidema, D., Vervoort, J., De Lorenzo, G., Jones, J.D.G., De Wit, P.J.G.M., Joosten, M.H.A.J. No evidence for binding between resistance gene product Cf-9 of tomato and avirulence gene product AVR9 of Cladosporium fulvum. Mol. Plant Microbe Interact. 14, 867-876 (2001).

Lee, J., Klessig, D.F., Nürnberger, T. A harpin binding site to tobacco plasma membranes mediates SIPK-dependent activation of the defense-related gene, HIN1. Plant Cell, 13, 1079-1093 (2001).

Lee, J., Klüsener, B., Tsiamis, G., Stevens, C., Neyt, C., Cornelis, G.R., Panopoulos, N.J., Weiler, E.W., Mansfield, J., Nürnberger, T. HrpZPsph from the plant pathogen Pseudomonas syringae pv. phaseolicola is exported by the type III secretion pathway and forms an ion-conducting pore in vitro. Proc. Natl. Acad. Sci. U.S.A., 98, 289-294 (2001).

Blume, B., Nürnberger, T., Nass, N., Scheel, D. Receptor-mediated rise in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell, 12, 1425-1440 (2000).

Fellbrich, G., Blume, B., Brunner, F., Hirt, H., Kroj, T., Ligterink, W., Romanski, A., Nürnberger, T. Phytophthora parasitica elicitor-induced reactions in cells of Petroselinum crispum. Plant Cell Physiol., 41, 692-701 (2000).

Abel, S., Nürnberger, T., Ahnert, V., Krauss, G.-J., Glund, K. Induction of an extracellular cyclic nucleotide phosphodiesterase as an accessory ribonucleolytic activity during phosphate starvation of cultured tomato cells. Plant Physiol. 122, 543-552 (2000).

Scheel, D., Blume, B., Brunner, F., Fellbrich, G., Dalboge, H., Hirt, H., Kauppinen, S., Kroj, T., Ligterink, W., Nürnberger, T., Tschöpe, M., Zinecker, H., zur Nieden, U. Receptor-mediated signal transduction in plant defense. In: Biology of Plant-Microbe Interactions. (De Wit, P.J.G.M., Bisseling, T., Stiekema, W., eds.), Vol. 2, IS-MPMI, St. Paul, MN, USA, 131-135 (2000).

Nürnberger, T. Signal perception in plant pathogen defense. Cell. Mol. Life Sci. 55, 167-182 (1999).

Nennstiel, D., Scheel, D., Nürnberger, T. Characterization and partial purification of an oligopeptide elicitor receptor from parsley (Petroselinum crispum). FEBS Lett. 431, 405-410 (1998).

Nürnberger, T., Nennstiel, D. Fungal peptide elicitors: Signals mediating pathogen recognition in plants. Invited Trends Article. Z. Naturforsch. 53c, 141-150 (1998).

Zimmermann*, S., Nürnberger*,+ , T., Frachisse, J.-M., Wirtz, W., Guern, J., Hedrich, R., Scheel, D. Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc. Natl. Acad. Sci. U.S.A. 94, 2751-2755 (1997).

Nürnberger, T., Wirtz, W., Nennstiel, D., Hahlbrock, K., Jabs, T., Zimmermann, S., Scheel, D. Signal perception and intracellular signal transduction in plant pathogen defense. J. Recept. Signal Transduct. Res. 17, 127-136 (1997).

Nennstiel, D., Hahlbrock, K., Jabs, T., Scheel, D., Wirtz, W., Zimmermann, S., Nürnberger, T. Signal perception and intracellular transduction in the Phytophthora sojae/parsley interaction. In : Physical Stresses in Plants: Genes and their Products for Tolerance. (Grillo, S. and Leone, A., eds.), Springer-Verlag Heidelberg, 261-270 (1996).

Wirtz, W., Nennstiel, D., Jabs, T., Zimmermann, S., Scheel, D., Nürnberger, T. Signal perception and intracellular signal transduction in plant pathogen defense. In: Biology of Plant-Microbe Interactions. (Stacey, G., Mullin, B., Gresshoff. P., eds.), Vol. 1, IS-MPMI, St. Paul, MN, USA, 21-26 (1996).

Honee, G., Nürnberger, T. Molecular genetics of fungal plant pathogens and signal perception and transduction in plant-fungus interactions. Eur. J. Plant Pathol. 101, 579-583 (1995).

Hahlbrock, K., Scheel, D., Logemann, E., Nürnberger, T., Parniske, M., Reinold, S., Sacks, W. R., Schmelzer, E. Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells. Proc. Natl. Acad. Sci. U.S.A., 92, 4150-4157 (1995).

Nürnberger, T., Nennstiel, D., Hahlbrock, K., Scheel, D. Covalent cross-linking of the Phytophthora megasperma oligopeptide elicitor to its receptor in parsley membranes. Proc. Natl. Acad. Sci. U.S.A., 92, 2338-2342 (1995).

Sacks, W.R., Nürnberger, T., Hahlbrock, K., Scheel, D. Molecular characterization of nucleotide sequences encoding the extracellular glycoprotein elicitor from Phytophthora megasperma. Mol. Gen. Genet., 246, 45-55 (1995).

Nürnberger,T., Nennstiel, D., Jabs, T., Sacks, W.R., Hahlbrock, K., Scheel, D. High-affinity binding of a fungal oligopeptide at parsley plasma membranes triggers multiple defense responses. Cell, 78, 449-460 (1994).

Diekmann, W., Herkt, B., Low, P., Nürnberger, T., Scheel, D., Terschüren, C., Robinson, D. G. Visualization of elicitor-binding loci at the plant cell surface. Planta, 195, 126-137 (1994).

 

Scheel, D., Hahlbrock, K., Jabs, T., Nürnberger, T., Sacks, W.R. Specific recognition of a fungal oligopeptide elicitor by parsley cells. In: Advances in Molecular Genetics of Plant-Microbe Interactions. (Daniels, M., ed.) Kluwer Academic Publishers Dordrecht, Boston, London Vol. 3, 313-318 (1994).

Nürnberger, T., Colling, C., Hahlbrock, K., Jabs, T., Renelt, A., Sacks, W.R., Scheel, D. Perception and transduction of an elicitor signal in cultured parsley cells. In: Molecular Botany: Signals and the Environment. (Bowles, D., ed.) Portland Press London and Chapel Hill, 60, 173-182 (1994).

Nürnberger T., Colling, C., Hahlbrock, K., Jabs, T., Renelt, A., Sacks, W. R., Scheel, D. Perception and transduction of an elicitor signal in cultured parsley cells. Biochem. Soc. Symp. 60, 173-182 (1994).

Renelt, A., Colling, C., Hahlbrock, K., Nürnberger, T., Parker, J.E., Sacks, W.R., Scheel, D. Studies on elicitor recognition and signal transduction in plant defense. J. Exp. Bot. 44, 257-268 (1993).

Sacks, W.R., Ferreira, P., Hahlbrock, K., Jabs, T., Nürnberger, T., Renelt, A., Scheel, D. Elicitor recognition and intracellular signal transduction in plant defense. In: Advances in Molecular Genetics of Plant-Microbe Interactions. (Nester, E., ed.) Kluwer Academic Publishers Dordrecht, Boston, London Vol. 2 485-496 (1993).

Abel, S., Jost, W., Nürnberger, T., Löffler, A., Glund, K. Ribonucleases in cell suspension cultures of tomato. In: Structure, Mechanism and Function of Ribonucleases. (Cuchillo, C.M., De Lorens, R., Nogies, W.V., eds.) Vol. 1, 169-174, Barcelona (1991).

Glund, K., Nürnberger, T., Abel, S., Jost, W., Preisser, J., Komor, E. Intracellular Pi compartmentation during phosphate starvation-triggered induction of an extracellular ribonuclease in tomato cell culture. In: Progress in Plant Cellular and Molecular Biology. (Nijkamp, H.J.J., Van Der Plas, L.W.H., Van Aartrijk, J., eds.) Kluwer Academic Publishers Dordrecht, Boston, London, Vol. 1, 336-342 (1990).

Nürnberger, T., Abel, S., Jost, W., Glund, K. Induction of an extracellular ribonuclease in cultured tomato cells upon phosphate starvation. Plant Physiol. 92, 970-976 (1990).