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 (Fig.1).

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 study the molecular basis of damage-associated immune activation in plants.

 

 

Identification of bacterial PAMPs and their corresponding receptors

 

We have been able to identify bacteria-derived patterns that trigger immunity-associated responses in Arabidopsis. These comprise, for example, protein fragments of Ralstonia solanacearum cell extracts. Upon purification to homogeneity, such a pattern will be used to identify the corresponding plant pattern recognition receptor.

 

 

Fig. 1: Identification of new D/P/MAMPs and their receptors

 

 

Likewise, bacterial peptidoglycan preparations (PGN) from different bacterial sources (S. aureus, E. coli, B. subtilis, P. syringae pv. tomato, Xanthomonas campestris pv. campestris) trigger immunity-associated defenses in Arabidopsis. The Arabidopsis PGN perception system is mechanistically different from that for bacterial flagellin or fungal chitin. An Arabidopsis plasma membrane protein carrying two ectopic LysM domains (LYM3) has been implicated in PGN binding, PGN sensitivity (Fig.2) and plant immunity to bacterial infection. As this PGN binding protein lacks a cytoplasmic signaling domain, we now aim at understanding how the PGN signal is transduced across the plant plasma membrane.

 

Fig. 2: PGN-induced FRK1 marker gene expression is abolished in lym3 mutants

 

NEP1-like Proteins as triggers of plant innate immunity

 

Plants do not only respond to non self-representing microbial patterns, but also have the ability to sense endogenous, self-representing stress-associated ‘danger’ signals (‘damage-associated molecular patterns’, DAMPs). Such plant signals comprise breakdown products of cell wall pectins or cellulose, that are released during microbial infection by microbial hydrolytic enzymes or that are generated through the activities of microbial toxins. Necrosis and ethylene inducing protein 1-like proteins (NLPs) constitute a protein superfamily of which members are produced by various phytopathogenic microorganisms. NLPs trigger leaf necrosis, and stimulate immunity-associated defenses in dicotyledonous plants, including Arabidopsis.

NLPs were proposed to have dual functions in plant pathogen interactions acting both as triggers of immune responses and as toxin-like virulence factors. The crystal structure of an NLP from the phytopathogenic oomycete Pythium aphanidermatum revealed significant fold conservation between NLPs and pore-forming cytolytic toxins produced by marine organisms (actinoporins) (Fig.3).

Expression of oomycete NLPs in an nlp-deficient P. carotovorum strain restored bacterial virulence, suggesting that NLPs of prokaryotic and eukaryotic origins are orthologous proteins. NLP mutant protein analyses revealed that identical structural features of the protein were required for cytotoxicity and for bacterial virulence, indicating that NLPs are virulence factors that contribute to host infection by plasma membrane destruction and cytolysis. In addition, NLP-mediated phytotoxicity and plant defense activation share identical fold requirements, suggesting that toxin-mediated interference with host integrity causes plant immune activation. Phytotoxin-induced cellular damage-associated activation of plant defenses is reminiscent of microbial toxin-induced inflammasome activation in vertebrates and, thus, constitutes a conserved element in eukaryote innate immunity.

 

 

Fig. 3: A common toxin fold mediates microbial phytotoxicity

 

 

ZMBP Research activities 2011 (pdf-file)

 

 

Publications

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

 

Lenz, H.D., Haller, E., Melzer, E., Gust, A.A. and Nürnberger, T. Autophagy controls plant basal immunity in a pathogenic lifestyle-dependent manner. Autophagy, 7, 773-774 (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., Gust, A.A. and Nürnberger, T. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J, 66, 818-830 (2011).

 

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

 

Nürnberger, T., Küfner, I. The role of the plasma membrane in microbial sensing and innate immunity. Plant Cell Monographs: The plant plasma membrane (series Eds. B. Schulz, A. Murphy). Springer-Verlag Berlin-Heidelberg. Vol. 19, pp. 471-484 (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.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., Nürberger, 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). * joint last and corresponding author

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., Nürnberger, T.  Signal transduction in plant defense responses to fungal infection. In: Fungal disease resistance in plants: Biochemistry, Molecular Biology and Genetic Engineering. (Punja, Z. K., ed.) Vol. X Haworth Press, Inc. Binghamton, NY, USA, 1-30 (2004).

 

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. USA 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). * joint first author; +corresponding author.

 

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).