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Project 19
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Project 19

Jane Parker

Toll-related intracellular receptors in plant innate immunity

Max-Planck-Institute for Plant Breeding Research, Cologne

Publications

Brief description in German:
Die Anwesenheit von Pathogenen kann im Wirt durch intrazelluläre NLR Rezeptoren erkannt werden und eine zell-autonome Immunität induzieren. In Pflanzen gehören diese NLR Rezeptoren zu einer großen Proteinfamilie mit zwei strukturellen Hauptunterklassen (TNLs und CNLs) und reagieren auf die Erkennung pathogener Effektoren mit der Aktivierung einer starken Immunantwort.

Wie verschiedene TNL und CNL Rezeptoren jedoch entsprechende konservierte und basale Resistenzmechanismen zur Abwehrprogrammierung ihrer Zellen organisieren, ist bisher kaum verstanden.

Wir interessieren uns für die Aktivierung solcher am Chromatin wirkender TNL Rezeptorkomplexe und deren Signalfunktion. In diesem Zusammenhang untersuchen wir in der Modellpflanze Arabidopsis eine durch Pathogene verursachte Effektor-induzierte Immunität (ETI), die durch das TNL Rezeptorenpaar RRS1 und RPS4 im Zusammenspiel mit dem Immunregulator EDS1 eine transkriptionelle Neuprogrammierung im pflanzlichen Zellkern vermittelt. RRS1 funktioniert hierbei als Sensor von pathogenen Effektoren und ist durch eine WRKY Domäne, die einer pflanzlichen Familie von Transkriptonsfaktoren entstammt, an der DNA verankert.

 

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Summary
We’re interested in understanding how plants activate and fine-tune their innate immune responses. Using the plant model species Arabidopsis thaliana in association with biotrophic or hemi-biotrophic pathogens we’re working to identify key decision-making ‘nodes’ in pathogen recognition and resistance, to elucidate how such regulatory nodes connect to the cellular reprogramming machinery (through transcriptional and post-transcriptional processes) and to position disease resistance pathways within the broader environment sensing network.

Cell-autonomous immunity is achieved by intracellular nucleotide-binding/leucine-rich-repeat (NLR) receptors sensing pathogen attack. Members of an expanded family of plant NLR receptors, in two major structural sub-classes (Toll-Interleukin1-Receptor domain-NLRs, known as TNLs and Coiled-Coil domain-NLRs, CNLs), recognize interference by pathogen effectors in different cell compartments to trigger a robust innate immune response.

How TNL and CNL receptors converge on a conserved basal resistance machinery to reprogram cells for defence is poorly understood. We study effector-triggered immunity (ETI) mediated by a TNL receptor pair, RRS1 and RPS4, which operates inside nuclei together with the basal immunity regulator, EDS1, to induce transcriptional reprogramming and pathogen resistance.

EDS1 has an essential nuclear function in pathogen resistance which can be uncoupled from host programmed cell death (pcd) that often accompanies ETI. EDS1 associations with several nuclear TNL receptors suggests it connects different TNLs molecularly to downstream defence pathways. Recent analysis of RRS1/RPS4 complex activation by Laurent Deslandes and colleagues at LIPM-CNRS/INRA (Toulouse) together with our group at MPIPZ shows that RRS1/RPS4 directly intercepts a broad sweep immune-suppressing activity of a bacterial pathogenicity factor (effector) targeting a family of defensive WRKY transcription factors (TFs). RRS1/RPS4 achieves this by integrating a WRKY DNA-binding domain as an effector target decoy within the RRS1 receptor protein.

Based on current data, we hypothesize that critical TNL receptor signalling events leading to resistance take place at the chromatin. Our aims are to
(i) characterize TNL receptor complexes in healthy and resistance-activated plant tissues,
(ii) measure TNL chromatin association dynamics and relate these to EDS1-dependent gene expression outputs,
(iii) explore functional relationships between TNL receptors, EDS1 and the transcription machinery.

Our results will provide important insights to how immune receptors connect to and reprogram cells for effective resistance.

List of publications resulting from the project
Peer-reviewed publications:
Le Roux C, Huet G, Jauneau A, Camborde L, Trémousaygue D, Kraut A, Zhou B, Levaillant M, Adachi H, Yoshioka H, Rafaele S, Berthomé R, Couté Y, Parker JE and Deslandes L. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell, 161, 1074-1088.

Williams, S.J., Hoon Sohn, K., Wan, L., Bernoux, M., Sarris, P. F., Segonzac, C., Ve, T., Ma, Y., Saucet, S. B., Ericsson, D. J., Casey, L. W., Lonhienne, T., Winzor, D. J., Zhang, X., Coerdt, A., Parker, J. E., Dodds, P. N., Kobe, B. and Jonathan D. G. Jones. 2014. Structural Basis for Assembly and Function of a Heterodimeric Plant Immune Receptor. Science 344, 299-303.

Heidrich, K., Tsuda, K., Blanvillain-Baufumé, S., Wirthmueller, L., Bautor, J. and Parker, J.E. 2013. Arabidopsis TNL-WRKY domain receptor RRS1 contributes to temperature conditioned RPS4 auto-immunity. Frontiers Plant Sci. 4: 403.

Zbierzak, A.M., Porfirova, S., Griebel, T., Melzer, M., *Parker, J.E. and *Dörmann, P. 2013. A TIR-NBS protein encoded by Arabidopsis Chilling Sensitive 1 (CHS1) limits chloroplast damage and cell death at low temperature. Plant J. 75:539-552. *Corresponding authors.

Kim, T-H., Kunz, H-H., Bhattacharjee, S., Hauser, F., Park, J., Engineer, C., Liu, A., Ha, T., Parker, J.E., Gassmann, W. and Schroeder, J.I. 2012. Natural variation in small molecule-induced TIR-NB-LRR signaling induces root growth arrest via EDS1- and PAD4-complexed R protein VICTR in Arabidopsis. Plant Cell 24: 5177-5192.

Shin, J., Heidrich, K., Sanchez-Villarreal, A., Parker, J.E. and Davis, S.J. 2012. TIME FOR COFFEE represses MYC2 protein accumulation to provide time-of-day regulation of jasmonate signaling. Plant Cell 24: 2470-2482.

Heidrich, K., Wirthmueller, L., Tasset, C., Pouzet, C., Deslandes, L. and Parker, J.E. 2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science, 334: 1401-1404.

Kim, T.-H., Hauser, F., Ha, T., Xue, S., Böhmer, M., Nishimura, N., Munemasa, S., Hubbard, K., Peine, N., Lee, B.., Lee, S., Robert, N., Parker, J.E. and Schröder, J.I. 2011. Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway. Curr Biol. 21:990-997.

Cheng, Y.T, Wiermer, M., Germain, H., Bi, D., Xu, F., Garcia, A.V., Wirthmüller, L., Depres, C., Parker, J.E., Zhang, Y. and Li, X. (2009). Nuclear pore complex component MOS7/Nup88 is required for plant innate immunity and nuclear accumulation of defense regulators. Plant Cell 21: 2503-2516.

Birker, D., Heidrich, K., Takahara, H., Narusaka, M., Deslandes, L., Narusaka, Y., Reymond, M., *Parker, J.E. and *O’Connell, R. (2009). A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 60(4):602-13. * joint corresponding author.

Kwon, C., Neu, C., Pajonk, S., Yun, H.-S., Lipka, U., Humphry, M.E., Bau, S., Straus, M., Rampelt, H., El Kasmi, F., Jürgens, G., Parker, J., Panstruga, R., Lipka, V. and Schulze-Lefert, P. (2008). Co-option of a default secretory pathway for plant immune responses, Nature 451: 835-840.

Mühlenbock, P., Szechyńska-Hebda, M., Płaszczyca, M., Baudo, M., Mullineaux. P.M., Parker, J.E., Karpińska, B. and Karpiński, S. (2008). Chloroplast signalling and LESION SIMULATING DISEASE 1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20: 2339-2356.

Wirthmüller, L., Zhang, Y., Jones, J.D.G. and Parker, J.E. (2007). Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defence. Curr. Biol. 17: 2023-2029.

Reviews:
Cui H, Tsuda K, Parker JE. 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66, 487-511.

Parker JE. 2014. Co-opting the cell-cycle machinery for plant immunity. Cell Host Microbe 16, 707-709.

Griebel T, Maekawa T and Parker JE. 2014. Nucleotide-binding oligomerization domain-like receptor cooperativity in effector-triggered immunity. Trends Immunol. 35, 562-570.

Heidrich, K., Blanvillain-Baufumé, S. and Parker, J.E. 2012. Molecular and spatial constraints on NB-LRR receptor signaling. Curr. Opin. Plant Biol. 15: 385-391.

Garcia, A.V. and Parker, J.E. (2009). Heaven’s Gate: Nuclear accessibility and activities of plant immune regulators. Trends Plant Sci. 19: 479-487.

J.E. Parker. (2009). The quest for long-distance signals in plant systemic immunity. Science Signalling 2: pe31.

Panstruga, R., Parker, J.E. and Schulze-Lefert, P. (2009). Cell SnapShot: Plant immune response pathways. Cell 135: 978.e1-978.e3.

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