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; Carella, Philip

doi:10.1093/plcell/koae113

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

Journal Article · Wed Apr 10 04:00:00 EDT 2024 · The Plant Cell

DOI:https://doi.org/10.1093/plcell/koae113· OSTI ID:2471114

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John Innes Centre, Norwich (United Kingdom)
University of East Anglia, Norwich (United Kingdom); Imperial College, London (United Kingdom)
University of Cambridge (United Kingdom)
University of East Anglia, Norwich (United Kingdom)
University of Illinois, Chicago, IL (United States)

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 CC_MAEPL in the nonflowering liverwort Marchantia polymorpha led to profound growth inhibition, defense gene activation, and signatures of cell death. Moreover, comparative transcriptomic analyses of CC_MAEPL 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.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE; Biotechnology and Biological Sciences Research Council (BBSRC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2471114

Journal Information:: The Plant Cell, Journal Name: The Plant Cell Journal Issue: 7 Vol. 36; ISSN 1040-4651

Publisher:: American Society of Plant Biologists (ASPB)Copyright Statement

Country of Publication:: United States

Language:: English

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