The N-terminal domains of NLR immune receptors exhibit structural and functional similarities across divergent plant lineages

Chia, Khong Sam, Kourelis, Jiorgos, Teulet, Albin, Vickers, Martin, Sakai, Toshiyuki, Walker, Joseph F., Schornack, Sebastian, Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315 and Carella, Philip (2024) The N-terminal domains of NLR immune receptors exhibit structural and functional similarities across divergent plant lineages. The Plant Cell, 36 (7). pp. 2491-2511. ISSN 1040-4651

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Abstract

Nucleotide-binding domain and leucine-rich repeat (NLR) proteins are a prominent class of intracellular immune receptors in plants. However, our understanding of plant NLR structure and function is limited to the evolutionarily young flowering plant clade. Here, we describe an extended spectrum of NLR diversity across divergent plant lineages and demonstrate the structural and functional similarities of N-terminal domains that trigger immune responses. We show that the broadly distributed coiled-coil (CC) and toll/interleukin-1 receptor (TIR) domain families of nonflowering plants retain immune-related functions through translineage activation of cell death in the angiosperm Nicotiana benthamiana. We further examined a CC subfamily specific to nonflowering lineages and uncovered an essential N-terminal MAEPL motif that is functionally comparable with motifs in resistosome-forming CC-NLRs. Consistent with a conserved role in immunity, the ectopic activation of CCMAEPL in the nonflowering liverwort Marchantia polymorpha led to profound growth inhibition, defense gene activation, and signatures of cell death. Moreover, comparative transcriptomic analyses of CCMAEPL activity delineated a common CC-mediated immune program shared across evolutionarily divergent nonflowering and flowering plants. Collectively, our findings highlight the ancestral nature of NLR-mediated immunity during plant evolution that dates its origin to at least ∼500 million years ago.

Item Type: Article
Additional Information: Data availability statement: All relevant accession numbers for raw data are provided in the manuscript. Funding Information: This work was supported by the UKRI (UK Research and Innovation); Biotechnology and Biological Sciences Research Council (BBSRC; JIC/TSL core-funding grants BB/P012574, BBS/E/J/000PR9798, BBS/E/J/000PR9797, BBS/E/J/000PR9796, BBS/E/J/000PR9795), the Gatsby Charitable Foundation (S.S. and S.K.), and University of Illinois Chicago start-up funding (J.F.W.).
Uncontrolled Keywords: plant science ,/dk/atira/pure/subjectarea/asjc/1100/1110
Faculty \ School: Faculty of Science > School of Biological Sciences
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
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Depositing User: LivePure Connector
Date Deposited: 23 Oct 2024 11:30
Last Modified: 25 Oct 2024 15:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/97142
DOI: 10.1093/plcell/koae113

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