Induced proximity of a TIR signaling domain on a plant-mammalian NLR chimera activates defense in plants

Autor: Zane Duxbury, Hailong Guo, Shanshan Wang, Maud Bernoux, Baptiste Castel, Xiaoxiao Zhang, Peter N. Dodds, Russell E. Vance, Jonathan D. G. Jones, Sung Un Huh, J. Chen, Pok N. Ngou, Pingtao Ding, Jeannette L. Tenthorey, Lanxi Hu, Yan Ma, Panagiotis N. Moschou, Craig MacKenzie, Lionel Hill
Přispěvatelé: University of East Anglia [Norwich] (UEA), Austrian Academy of Sciences (OeAW), University of California [Berkeley], University of California, Fred Hutchinson Cancer Research Center [Seattle] (FHCRC), Commonwealth Scientific and Industrial Research Organisation [Canberra] (CSIRO), University of Canberra, Kunsan National University, University of Georgia [USA], John Innes Centre [Norwich], National University of Singapore (NUS), Swedish University of Agricultural Sciences (SLU), University of Crete [Heraklion] (UOC), Foundation for Research and Technology - Hellas (FORTH), Laboratoire des Interactions Plantes Microbes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Biotechnology and Biological Sciences Research Council (BBSRC) : BB/M008193/1, Rural Development Administration (RDA) : PJ01365301, China Scholarship Council, Biotechnology and Biological Sciences Research Council (BBSRC) : BB/R012172/1, Marie Sklodowska-Curie Action Individual Fellowship : 656011, European Project: 669926,H2020,ERC-2014-ADG,ImmunityByPairDesign(2015), European Project: 656243,H2020,H2020-MSCA-IF-2014,PERFECTION(2016), University of California [Berkeley] (UC Berkeley), University of California (UC), Biotechnology and Biological Sciences Research Council (BBSRC)
Jazyk: angličtina
Rok vydání: 2020
Předmět:
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Proceedings of the National Academy of Sciences of the United States of America, National Academy of Sciences, 2020, 117 (31), pp.18832-18839. ⟨10.1073/pnas.2001185117⟩
Proceedings of the National Academy of Sciences of the United States of America, 2020, 117 (31), pp.18832-18839. ⟨10.1073/pnas.2001185117⟩
ISSN: 0027-8424
1091-6490
Popis: Significance Animal NLRs form wheel-like structures called inflammasomes upon perception of pathogen-associated molecules. The induced proximity of the signaling domains at the center of the wheel is hypothesized to recruit caspases for the first step of immune signal transduction. We expressed a plant-animal NLR fusion to demonstrate that induced proximity of TIR signaling domains from plant NLRs is sufficient to activate plant immune signaling. This demonstrates that a signaling-competent inflammasome can be formed from known, minimal components. The intrinsic NADase activity of plant TIRs is necessary for immune signaling, but fusions to a bacterial or a mammalian TIR domain with NADase activity, which also lead to accumulation of NAD+ hydrolysis products (e.g. cyclic ADP-ribose), were unable to activate immune signaling.
Plant and animal intracellular nucleotide-binding, leucine-rich repeat (NLR) immune receptors detect pathogen-derived molecules and activate defense. Plant NLRs can be divided into several classes based upon their N-terminal signaling domains, including TIR (Toll-like, Interleukin-1 receptor, Resistance protein)- and CC (coiled-coil)-NLRs. Upon ligand detection, mammalian NAIP and NLRC4 NLRs oligomerize, forming an inflammasome that induces proximity of its N-terminal signaling domains. Recently, a plant CC-NLR was revealed to form an inflammasome-like hetero-oligomer. To further investigate plant NLR signaling mechanisms, we fused the N-terminal TIR domain of several plant NLRs to the N terminus of NLRC4. Inflammasome-dependent induced proximity of the TIR domain in planta initiated defense signaling. Thus, induced proximity of a plant TIR domain imposed by oligomerization of a mammalian inflammasome is sufficient to activate authentic plant defense. Ligand detection and inflammasome formation is maintained when the known components of the NLRC4 inflammasome is transferred across kingdoms, indicating that NLRC4 complex can robustly function without any additional mammalian proteins. Additionally, we found NADase activity of a plant TIR domain is necessary for plant defense activation, but NADase activity of a mammalian or a bacterial TIR is not sufficient to activate defense in plants.
Databáze: OpenAIRE
Externí odkaz: