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Research article - Peer-reviewed, 2020

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

Duxbury, Zane; Wang, Shanshan; MacKenzie, Craig, I; Tenthorey, Jeannette L.; Zhang, Xiaoxiao; Huh, Sung Un; Hu, Lanxi; Hill, Lionel; Ngou, Pok N.; Ding, Pingtao; Chen, Jian; Ma, Yan; Guo, Hailong; Castel, Baptiste; Moschou, Panagiotis N.; Bernoux, Maud; Dodds, Peter N.; Vance, Russell E.; Jones, Jonathan D. G.

Abstract

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.

Keywords

NLR immune receptors; plant immunity; inflammasome; effector-triggered; immunity

Published in

Proceedings of the National Academy of Sciences of the United States of America
2020, volume: 117, number: 31, pages: 18832-18839
Publisher: NATL ACAD SCIENCES

Authors' information

Duxbury, Zane
University of East Anglia
Wang, Shanshan
University of East Anglia
MacKenzie, Craig
University of East Anglia
Tenthorey, Jeannette L.
University of California Berkeley
Zhang, Xiaoxiao
Commonwealth Scientific and Industrial Research Organisation (CSIRO)
Huh, Sung Un
University of East Anglia
Hu, Lanxi
University of East Anglia
Hill, Lionel
John Innes Centre
Ngou, Pok N.
University of East Anglia
Ding, Pingtao
University of East Anglia
Chen, Jian
Commonwealth Scientific and Industrial Research Organisation (CSIRO)
Ma, Yan
University of East Anglia
Guo, Hailong
University of East Anglia
Castel, Baptiste
University of East Anglia
The Sainsbury Laboratory (TSL)
Swedish University of Agricultural Sciences, Department of Plant Biology
University of Crete
Foundation for Research and Technology - Hellas (FORTH)
Bernoux, Maud
Commonwealth Scientific and Industrial Research Organisation (CSIRO)
Dodds, Peter N.
Commonwealth Scientific and Industrial Research Organisation (CSIRO)

Associated SLU-program

SLU Network Plant Protection

UKÄ Subject classification

Immunology

Publication Identifiers

DOI: https://doi.org/10.1073/pnas.2001185117

URI (permanent link to this page)

https://res.slu.se/id/publ/108297