B08 - Parker

B08 - Connecting plant TIR-domain NLR receptors to host cell death and pathogen resistance

Jane Parker

Max Planck Institute for Plant Breeding Research
Contact: parker(at)mpipz.mpg.de
For more information visit: Parker lab

Abstract

Nucleotide-binding domain/leucine-rich repeat (NLR) receptors provide a crucial barrier to pathogen infection in mammals and plants. We’re studying plant immune responses mediated by a major class of NLR receptor with N-terminal Toll-Interleukin1-Receptor (TIR) signalling domains. Pathogen-activated TIR-NLRs form oligomeric (resistosome) NADase enzymes which generate a suite of ribosylated nucleotide second messengers. Specific nucleotides regulate distinct host localized cell death and defence stimulating branches, both associated with calcium influxes into host cells. Our aim is to characterize TIR-NLR triggered processes conferring regulated host cell death and cell -to - cell defence potentiation in leaves.

Recent Publications

2025

Huang S, Wang J, Song R, Jia A, Xiao Y, Sun Y, Wang L, Mahr D, Wu Z, Han Z, Li X, Parker JE, Chai J. Balanced plant helper NLR activation by a modified host protein complex. Nature. 2025 Feb 12. doi: https://www.nature.com/articles/s41586-024-08521-710.1038/s41586-024-08521-7. Epub ahead of print. PMID: 39939760.

Project B08 Publications 2nd Funding Period 2024 - 2027

2024

Wu Y, Xu W, Zhao G, Lei Z, Li K, Liu J, Huang S, Wang J, Zhong X, Yin X, Wang Y, Zhang H, He Y, Ye Z, Meng Y, Chang X, Lin H, Wang X, Gao Y, Chai J, Parker JE, Deng Y, Zhang Y, Gao M, He Z. A canonical protein complex controls immune homeostasis and multipathogen resistance. Science. 2024 Dec 20;386(6728):1405-1412. doi: 10.1126/science.adr2138. Epub 2024 Nov 7. PMID: 39509474.

Shen Q, Hasegawa K, Oelerich N, Prakken A, Tersch LW, Wang J, Reichhardt F, Tersch A, Choo JC, Timmers T, Hofmann K, Parker JE, Chai J, Maekawa T. Cytoplasmic calcium influx mediated by plant MLKLs confers TNL-triggered immunity. Cell Host Microbe. 2024 Mar 13:S1931-3128(24)00059-3. doi: 10.1016/j.chom.2024.02.016. Epub ahead of print. PMID: 38513655.

Song W, Liu L, Yu D, Bernardy H, Jirschitzka J, Huang S, Jia A, Jemielniak W, Acker J, Laessle H, Wang J, Shen Q, Chen W, Li P, Parker JE, Han Z, Schulze-Lefert P, Chai J. Substrate-induced condensation activates plant TIR domain proteins. Nature. 2024 Mar 13. doi: 10.1038/s41586-024-07183-9. Epub ahead of print. PMID: 38480885

Locci F and Parker JE* 2024. Plant NLR immunity activation and execution: a biochemical perspective. Open Biol. 14:230387. doi.org/10.1098/rsob.230387

Project B08 Publications 1st Funding Period 2020 - 2023

2023

Zeng, Y., Zheng, Z., Hessler, G., Zou, K., Bautor, J., Stuttmann, J., Xue, L., Parker, J.E., and Cui, .H*. (2023). Arabidopsis PAD4 promotes the maturation and nuclear accumulation of immune-related cysteine protease RD19. J. Exp. Bot. doi.org/10.1093/jxb/erad454

Chai, J.*, Song, W., and Parker, J.E.*. (2023). HH Flor Distinguished Review: New biochemical principles for NLR immunity in plants. Mol. Plant-Microbe Interact. 36: 468-475.doi/10.1094/MPMI-05-23-0073-HHps://doi.org/10.1094/MPMI-05-23-0073-HH

Locci, F., Wang, J., and Parker, J.E.*.( 2023). TIR-domain enzymatic activities at the heart of plant immunity. Curr. Opin. Plant Biol. 74:102373. doi.org/10.1016/j.pbi.2023.102373

Cao, Y., Kümmel, F., Logemann, E., Gebauer, J.M., Lawson, A.W., Yu, D., Uthoff, M., Keller, B., Jirschitzka, J., Baumann, U., Tsuda, K., Chai, J. and Schulze-Lefert, P. (2023) Structural polymorphisms within a common powdery mildew effector scaffold as a driver of coevolution with cereal immune receptors. Proc Natl Acad Sci U S A. doi: 10.1073/pnas.2307604120

Crean, E.E., Bilstein-Schloemer, M., Maekawa, T., Schulze-Lefert, P. and Saur, I.M.L. (2023) A dominant-negative avirulence effector of the barley powdery mildew fungus provides mechanistic insight to barley MLA immune receptor activation. J Exp Bot. doi: 10.1093/jxb/erad285

Feehan, J.M., Wang, J., Sun, X., Choi, J., Ahn, H.K., Ngou, B.P.M., Parker, J.E., Jones, and J.D.G. (2023). Oligomerization of a plant helper NLR requires cell-surface and intracellular immune receptor activation. Proc Natl Acad Sci U S A. 120, e2210406120. doi: 10.1073/pnas.2210406120.

Johanndrees, O., Baggs, E.L., Uhlmann, C., Locci, F., Läßle, H.L., Melkonian, K., Käufer, K., Dongus, J.A., Nakagami, H., Krasileva, K.V., Parker, J.E, Lapin, D. (2023) Variation in plant Toll/Interleukin-1 receptor domain protein dependence on ENHANCED DISEASE SUSCEPTIBILITY 1 Plant Physiology, Volume 191, Issue 1, January 2023, Pages 626–642, https://doi.org/10.1093/plphys/kiac480

2022

Wang,J., Song, W., Chai, J. (2022) Structure, biochemical function and signaling mechanism of plant NLRs. Molecular Plant https://doi.org/10.1016/j.molp.2022.11.011 (review)

Sun, Y., Wang, Y., Zhang, X., Chen, Z., Xia, Y., Wang, L., Sun, Y., Zhang, M., Xiao, Y., Han, Z., Wang, Y., & Chai, J. Plant receptor-like protein activation by a microbial glycoside hydrolase. Nature (2022). https://doi.org/10.1038/s41586-022-05214-x

Förderer, A., Li, E., Lawson, A.W., Deng, Y., Sun, Y., Logemann, E., Zhang, X., Wen, J., Han, Z., Chang, J., Chen, Y., Schulze-Lefert, P., & Chai, J. A wheat resistosome defines common principles of immune receptor channels. Nature (2022) https://doi.org/10.1038/s41586-022-05231-w

Huang S., Jia, A., Song, W., Hessler, G., Meng, Y., Sun, Y., Xu, L., Laessle, H., Jirschitzka, J., Ma, S., Xiao, Y., Yu, D., Hou, J., Liu, R., Sun, H., Liu, X., Han, Z., Chang, J., Parker, J.E., Chai, J. (2022) Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity. Science DOI: 10.1126/science.abq3297

Jia, A., Huang, S,. Song, W., Wang, J., Meng, Y,. Sun, Y., Xu, L., Laessle, H., Jirschitzka, J., Hou, J., Zhang, T., Yu, W., Hessler, G., Li, E., Ma, S., Yu, D., Gebauer, J., Baumann, U., Liu, X., Han, Z., Chang, J., Parker, J.E., Chai, J. (2022) TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity. Science 10.1126/science.abq8180

Lapin, D., Johanndrees, O., Wu, Z., Parker, J.E. (2022) Molecular innovations in plant TIR-based immunity signaling. The Plant Cell 2022: 00: 1-18 https://doi.org/10.1093/plcell/koac035

2021

Parker, J.E., Hessler, G., Cui, H. (2021) A new biochemistry connecting pathogen detection to induced defense in plants. New Phytologist https://doi.org/10.1111/nph.17924

Pruitt, R.N., Locci, F., Wanke, F., Zhang, L., Saile, S.C., Joe, A., Karelina, D., Hua, C., Fröhlich, K., Wan, W.-L., Hu, M., Rao, S., Stolze, S.C., Harzen, A., Gust, A.A., Harter, K., Joosten, M.H.A.J., Thomma, B.P.H.J., Zhou, J.-M., Dangl, J.L., Weigel, D., Nakagami, H., Oecking, C., El Kasmi, F., Parker, J.E., & Nürnberger, T. (2021) EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature. https://doi.org/10.1038/s41586-021-03829-0

Bauer, S., Yu, D., Lawson, A.W., Saur, I.M.L., Frantzeskakis, L., Kracher, B., Logemann, E., Chai, J., Maekawa, T., Schulze-Lefert, P. (2021) The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold. PLoS Pathog 17(2): e1009223. doi:10.1371/journal.ppat.1009223

Mahdi, L.K., Huang, M., Zhang, X., Nakano, R.T., Kopp, L.B., Saur, I.M.L., Jacob, F., Kovacova, V., Lapin, D., Parker, J.E., Murphy, J.M., Hofmann, K., Schulze-Lefert, P., Chai, J., Maekawa, T. (2020) Discovery of a Family of Mixed Lineage Kinase Domain-like Proteins in Plants and Their Role in Innate Immune Signaling. Cell Host & Microbe https://doi.org/10.1016/j.chom.2020.08.012

Sun, X., Lapin, D., Feehan, J.M., Stolze, S.C., Kramer, K., Dongus, J.A., Rzemieniewski, J., Blanvillain-Baufumé, S., Harzen, A., Bautor, J., Derbyshire, P., Menke, F.L.H., Finkemeier, I., Nakagami, H., Jones, J.D.G., & Parker, J.E.(2021) Pathogen effector recognition-dependent association of NRG1 with EDS1 and SAG101 in TNL receptor immunity. Nature Communications 12, Article number: 3335 https://doi.org/10.1038/s41467-021-23614-x

Xing, Y., Xu, N., Bhandari, D.,D., Lapin, D., Sun, X., Luo, X., Wang, Y., Cao, J., Wang, H., Coaker, G., Parker, J.,E., Liu, J. Bacterial effector targeting of a plant iron sensor facilitates iron acquisition and pathogen colonization. The Plant Cell Koab075 https://doi.org/10.1093/plcell/koab075

Zhao, C., Tang, Y., Wang. J., Zeng, Y., Sun, H., Zheng, Z., Su, R., Schneeberger, K., Parker, J.E., Cui, H. (2021) A mis‐regulated cyclic nucleotide‐gated channel mediates cytosolic calcium elevation and activates immunity in Arabidopsis. New Phytologist doi:10.1111/nph.17218

2020

Project related Publications

2011 - 2019

Bhandari, D.D., Lapin, D., Kracher, B., von Born, P., Bautor, J., Niefind. K., and Parker J.E. (2019). An EDS1 heterodimer signalling surface enforces timely reprogramming of immunity genes in Arabidopsis. Nat. Commun. 10, 722.

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.

Hu, Z., Zhou, Q., Zhang, C., Fan, S., Cheng, W., Zhao, Y., Shao, F., Wang, H.W., Sui, S.F., and Chai, J. (2015). Structural and biochemical basis for induced self-propagation of NLRC4. Science 350, 399-404.

Maekawa, T., Cheng, W., Spiridon, L.N., Toller, A., Lukasik, E., Saijo, Y., Liu, P.Y., Shen, Q.H., Micluta, M.A., Somssich, I.E., …, Chai, J., and Schulze-Lefert, P. (2011). Coiled-Coil Domain-Dependent Homodimerization of Intracellular Barley Immune Receptors Defines a Minimal Functional Module for Triggering Cell Death. Cell Host Microbe 9, 187-199.

Lu, X., Kracher, B., Saur, I.M.-L., Bauer, S., Ellwood, S.R., Wise, R., Yaeno, T., Maekawa, T., and Schulze-Lefert, P. (2016) Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. Proc Natl Acad Sci U S A 113, E6486–E6495.

Rietz, S., Stamm, A., Malonek, S., Wagner, S., Becker, D., Medina-Escobar, N., Vlot, A.C., Feys, B.J., Niefind, K., and Parker, J.E. (2011). Different roles of EDS1 bound to and dissociated from PAD4 in Arabidopsis immunity. New Phytol. 191, 107-119

Saur, I.M., Bauer, S., Kracher, B., Lu, X., Franzeskakis, L., Muller, M.C., Sabelleck, B., Kummel, F., Panstruga, R., Maekawa, T., and Schulze-Lefert, P. (2019). Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism. Elife 8, e44471

Wagner, S., Stuttmann, J., Rietz, S., Guerois, R., Brunstein, E., Bautor, J., Niefind, K., and Parker, J.E. (2013). Structural Basis for Signalling by Exclusive EDS1 Heteromeric Complexes with SAG101 or PAD4 in Plant Innate Immunity. Cell Host Microbe 14, 619-630.

Wang, J., Hu, M., Wang, J., Qi, J., Han, Z., Wang, G., Qi, Y., Wang, H.W., Zhou, J.M., and Chai, J. (2019). Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364, eaav5870.

Wang, J., Wang, J., Hu, M., Wu, S., Qi, J., Wang, G., Han, Z., Qi, Y., Gao, N., Wang, H.W.,… and Chai, J. (2019). Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364, eaav5868

Project B08 First funding period 2020 - 2023

B08 - Connecting plant sensor NLRs to host cell death responses

Former participating Project leader:

Jijie Chai

Institute for Biochemistry, University of Cologne
Contact: jchai(at)uni-koeln.de
For more information visit: Chai lab

Paul Schulze-Lefert

Max Planck Institute for Plant Breeding Research
Contact: schlef(at)mpipz.mpg.de
For more information visit: Schulze-Lefert lab

Nucleotide-binding domain/leucine-rich repeat (NLR) receptors provide a crucial barrier to pathogen infection in mammals and plants. In both systems, NLRs sense microbe-mediated perturbations inside host cells and, via conformational switches, induce cell death and anti-microbial pathways leading to disease resistance. This project integrates protein structure-function studies with in vivo molecular and pathology phenotyping, genetics and cell biology to answer fundamental questions about how plant sensor NLRs activate cell death pathways and whether different NLR types converge on the same or distinct cell death machineries in immunity.

UNIVERSITÄT ZU KÖLN

Sonderforschungsbereich 1403