SICOPID_Activation and regulation of plasma membrane receptor signaling complexes controlling plant development and immunity, and their connection to downstream signaling cascades

• Applicants: Professor Michael Hothorn, Ph.D.; Professor Yvon Jaillais, Ph.D.; Professor Dr. Zachary Nimchuk; Professor Dr. Thorsten Nürnberger; Professor Dr. Cyril Zipfel
• Subject Area: Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems ; Plant Cell and Developmental Biology
• Term: from 2018 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 354195343

• Final Report Year: 2022

Final Report Abstract

The SICOPID project aimed at characterizing how different signaling complexes embedded in cellular membrane of plant cells can sense and transmit different signals. Plants have evolved a unique set of membrane receptor kinases and receptor-like proteins that enable cells to sense different extracellular signals. The joint project has analyzed how these receptors can sense foreign and plant-generated peptide ligands to activate developmental pathways, or the plant immune system. Next, specific downstream molecular switches, namely protein kinases were identified that enable the transmission of the signal from the cell membrane to the cell’s interior, where changes in gene activity can generate the desired signaling outputs. It was found that receptor kinases and receptor-like proteins use a partially common, partially unique set of downstream components in plant immune signaling. The project has in addition characterized different regulatory systems that can affect the propagation of the receptor signal. (1) Protein phosphatases that can negatively regulate the function of receptor kinases, and (2) MAKR protein inhibitors that can bind to specific receptor kinases to block their activation. Taken together, plant receptor kinases and receptor-like proteins have evolved to sense a large set of different ligands to control various aspects of plant development and to form the first defense layer of the plant immune system. The SICOPID project has characterized in molecular terms how signaling specificity is achieved in several different pathways, and has identified enzymes and inhibitor proteins that have the ability to modulate the signaling capacity of specific receptors. Finally, genetic tools have been developed that enable to investigate the impact of constitutive activation of plant receptor kinases on plant development and immune signaling.

Publications

• Comparing Arabidopsis receptor kinase and receptor protein‐mediated immune signaling reveals BIK1‐dependent differences. New Phytologist, 221(4), 2080-2095.
  Wan, Wei‐Lin; Zhang, Lisha; Pruitt, Rory; Zaidem, Maricris; Brugman, Rik; Ma, Xiyu; Krol, Elzbieta; Perraki, Artemis; Kilian, Joachim; Grossmann, Guido; Stahl, Mark; Shan, Libo; Zipfel, Cyril; van Kan, Jan A. L.; Hedrich, Rainer; Weigel, Detlef; Gust, Andrea A. & Nürnberger, Thorsten
  
• Crystal structure of the leucine-rich repeat ectodomain of the plant immune receptor kinase SOBIR1. Acta Crystallographica Section D Structural Biology, 75(5), 488-497.
  Hohmann, Ulrich & Hothorn, Michael
  
• Plant cell surface immune receptor complex signaling. Current Opinion in Plant Biology, 50, 18-28.
  Wan, Wei-Lin; Fröhlich, Katja; Pruitt, Rory N.; Nürnberger, Thorsten & Zhang, Lisha
  
• The Nanoscale Organization of the Plasma Membrane and Its Importance in Signaling: A Proteolipid Perspective. Plant Physiology, 182(4), 1682-1696.
  Jaillais, Yvon & Ott, Thomas
  
• BAM1/2 receptor kinase signaling drives CLE peptide-mediated formative cell divisions in Arabidopsis roots. Proceedings of the National Academy of Sciences, 117(51), 32750-32756.
  Crook, Ashley D.; Willoughby, Andrew C.; Hazak, Ora; Okuda, Satohiro; VanDerMolen, Kylie R.; Soyars, Cara L.; Cattaneo, Pietro; Clark, Natalie M.; Sozzani, Rosangela; Hothorn, Michael; Hardtke, Christian S. & Nimchuk, Zachary L.
  
• Constitutive Activation of Leucine-Rich Repeat Receptor Kinase Signaling Pathways by BAK1-INTERACTING RECEPTOR-LIKE KINASE3 Chimera. The Plant Cell, 32(10), 3311-3323.
  Hohmann, Ulrich; Ramakrishna, Priya; Wang, Kai; Lorenzo-Orts, Laura; Nicolet, Joel; Henschen, Agnes; Barberon, Marie; Bayer, Martin & Hothorn, Michael
  
• Low-cost and High-throughput RNA-seq Library Preparation for Illumina Sequencing from Plant Tissue. BIO-PROTOCOL, 10(20).
  Bjornson, Marta; Kajala, Kaisa; Zipfel, Cyril & Ding, Pingtao
  
• Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2. Proceedings of the National Academy of Sciences, 117(5), 2693-2703.
  Okuda, Satohiro; Fujita, Satoshi; Moretti, Andrea; Hohmann, Ulrich; Doblas, Verónica G.; Ma, Yan; Pfister, Alexandre; Brandt, Benjamin; Geldner, Niko & Hothorn, Michael
  
• Activation loop phosphorylation of a non-RD receptor kinase initiates plant innate immune signaling. Proceedings of the National Academy of Sciences, 118(38).
  Bender, Kyle W.; Couto, Daniel; Kadota, Yasuhiro; Macho, Alberto P.; Sklenar, Jan; Derbyshire, Paul; Bjornson, Marta; DeFalco, Thomas A.; Petriello, Annalise; Font, Farre Maria; Schwessinger, Benjamin; Ntoukakis, Vardis; Stransfeld, Lena; Jones, Alexandra M. E.; Menke, Frank L. H. & Zipfel, Cyril
  
• Auxin-Regulated Reversible Inhibition of TMK1 Signaling by MAKR2 Modulates the Dynamics of Root Gravitropism. Current Biology, 31(1), 228-237.e10.
  Marquès-Bueno, Maria Mar; Armengot, Laia; Noack, Lise C.; Bareille, Joseph; Rodriguez, Lesia; Platre, Matthieu Pierre; Bayle, Vincent; Liu, Mengying; Opdenacker, Davy; Vanneste, Steffen; Möller, Barbara K.; Nimchuk, Zachary L.; Beeckman, Tom; Caño-Delgado, Ana I.; Friml, Jiří & Jaillais, Yvon
  
• Importance of tyrosine phosphorylation for transmembrane signaling in plants. Biochemical Journal, 478(14), 2759-2774.
  Mühlenbeck, Henning; Bender, Kyle W. & Zipfel, Cyril
  
• Meet your MAKR: the membrane‐associated kinase regulator protein family in the regulation of plant development. The FEBS Journal, 289(20), 6172-6186.
  Novikova, Daria D.; Korosteleva, Anastasia L.; Mironova, Victoria & Jaillais, Yvon
  
• Molecular mechanisms of early plant pattern-triggered immune signaling. Molecular Cell, 81(17), 3449-3467.
  DeFalco, Thomas A. & Zipfel, Cyril
  
• The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature, 598(7881), 495-499.
  Pruitt, Rory N.; Locci, Federica; Wanke, Friederike; Zhang, Lisha; Saile, Svenja C.; Joe, Anna; Karelina, Darya; Hua, Chenlei; Fröhlich, Katja; Wan, Wei-Lin; Hu, Meijuan; Rao, Shaofei; Stolze, Sara C.; Harzen, Anne; Gust, Andrea A.; Harter, Klaus; Joosten, Matthieu H. A. J.; Thomma, Bart P. H. J.; Zhou, Jian-Min ... & Nürnberger, Thorsten
  
• The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nature Plants, 7(5), 579-586.
  Bjornson, Marta; Pimprikar, Priya; Nürnberger, Thorsten & Zipfel, Cyril
  
• A conserved module regulates receptor kinase signalling in immunity and development. Nature Plants, 8(4), 356-365.
  DeFalco, Thomas A.; Anne, Pauline; James, Sean R.; Willoughby, Andrew C.; Schwanke, Florian; Johanndrees, Oliver; Genolet, Yasmine; Derbyshire, Paul; Wang, Qian; Rana, Surbhi; Pullen, Anne-Marie; Menke, Frank L. H.; Zipfel, Cyril; Hardtke, Christian S. & Nimchuk, Zachary L.
  
• Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1. Nature Communications, 13(1).
  Fan, Li; Fröhlich, Katja; Melzer, Eric; Pruitt, Rory N.; Albert, Isabell; Zhang, Lisha; Joe, Anna; Hua, Chenlei; Song, Yanyue; Albert, Markus; Kim, Sang-Tae; Weigel, Detlef; Zipfel, Cyril; Chae, Eunyoung; Gust, Andrea A. & Nürnberger, Thorsten