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. 2024 Jul;243(1):345-361.
doi: 10.1111/nph.19818. Epub 2024 May 17.

The nucleotide-binding domain of NRC-dependent disease resistance proteins is sufficient to activate downstream helper NLR oligomerization and immune signaling

Mauricio P Contreras #  1 , Hsuan Pai #  1 , Rebecca Thompson  1 , Clemence Marchal  1 , Jules Claeys  1 , Hiroaki Adachi  1 , Sophien Kamoun  1
Affiliations
Free article

The nucleotide-binding domain of NRC-dependent disease resistance proteins is sufficient to activate downstream helper NLR oligomerization and immune signaling

Mauricio P Contreras et al. New Phytol. 2024 Jul.
Free article

Abstract

Nucleotide-binding domain and leucine-rich repeat (NLR) proteins with pathogen sensor activities have evolved to initiate immune signaling by activating helper NLRs. However, the mechanisms underpinning helper NLR activation by sensor NLRs remain poorly understood. Although coiled coil (CC) type sensor NLRs such as the Potato virus X disease resistance protein Rx have been shown to activate the oligomerization of their downstream helpers NRC2, NRC3 and NRC4, the domains involved in sensor-helper signaling are not known. Here, we used Agrobacterium tumefaciens-mediated transient expression in Nicotiana benthamiana to show that the nucleotide-binding (NB) domain within the NB-ARC of Rx is necessary and sufficient for oligomerization and immune signaling of downstream helper NLRs. In addition, the NB domains of the disease resistance proteins Gpa2 (cyst nematode resistance), Rpi-amr1, Rpi-amr3 (oomycete resistance) and Sw-5b (virus resistance) are also sufficient to activate their respective downstream NRC helpers. Using transient expression in the lettuce (Lactuca sativa), we show that Rx (both as full length or as NB domain truncation) and its helper NRC2 form a minimal functional unit that can be transferred from solanaceous plants (lamiids) to Campanulid species. Our results challenge the prevailing paradigm that NLR proteins exclusively signal via their N-terminal domains and reveal a signaling activity for the NB domain of NRC-dependent sensor NLRs. We propose a model in which helper NLRs can perceive the status of the NB domain of their upstream sensors.

Keywords: NB‐LRR; NOD; helper NLR; immunology; innate immunity; oligomerization; plant immunity.

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References

    1. Adachi H, Contreras MP, Harant A, Wu C‐h, Derevnina L, Sakai T, Duggan C, Moratto E, Bozkurt TO, Maqbool A et al. 2019a. An N‐terminal motif in NLR immune receptors is functionally conserved across distantly related plant species. eLife 8: e49956.
    1. Adachi H, Derevnina L, Kamoun S. 2019b. NLR singletons, pairs, and networks: evolution, assembly, and regulation of the intracellular immunoreceptor circuitry of plants. Current Opinion in Plant Biology 50: 121–131.
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    1. Ahn HK, Lin X, Olave‐Achury AC, Derevnina L, Contreras MP, Kourelis J, Wu CH, Kamoun S, Jones JD. 2023. Effector‐dependent activation and oligomerization of plant NRC class helper NLRs by sensor NLR immune receptors Rpi‐amr3 and Rpi‐amr1. EMBO Journal 42: e111484.
    1. Bendahmane A, Kanyuka K, Baulcombe DC. 1999. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11: 781–791.

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