An atypical NLR protein modulates the NRC immune receptor network in Nicotiana benthamiana

Adachi, Hiroaki, Sakai, Toshiyuki, Harant, Adeline, Pai, Hsuan, Honda, Kodai, Toghani, Amir Ali, Claeys, Jules, Duggan, Cian, Bozkurt, Tolga O., Wu, Chih-hang and Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315 (2023) An atypical NLR protein modulates the NRC immune receptor network in Nicotiana benthamiana. PLoS Genetics, 19 (1). ISSN 1553-7390

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Abstract

The NRC immune receptor network has evolved in asterid plants from a pair of linked genes into a genetically dispersed and phylogenetically structured network of sensor and helper NLR (nucleotide-binding domain and leucine-rich repeat-containing) proteins. In some species, such as the model plant Nicotiana benthamiana and other Solanaceae, the NRC (NLR-REQUIRED FOR CELL DEATH) network forms up to half of the NLRome, and NRCs are scattered throughout the genome in gene clusters of varying complexities. Here, we describe NRCX, an atypical member of the NRC family that lacks canonical features of these NLR helper proteins, such as a functional N-terminal MADA motif and the capacity to trigger autoimmunity. In contrast to other NRCs, systemic gene silencing of NRCX in N. benthamiana markedly impairs plant growth resulting in a dwarf phenotype. Remarkably, dwarfism of NRCX silenced plants is partially dependent on NRCX paralogs NRC2 and NRC3, but not NRC4. Despite its negative impact on plant growth when silenced systemically, spot gene silencing of NRCX in mature N. benthamiana leaves doesn't result in visible cell death phenotypes. However, alteration of NRCX expression modulates the hypersensitive response mediated by NRC2 and NRC3 in a manner consistent with a negative role for NRCX in the NRC network. We conclude that NRCX is an atypical member of the NRC network that has evolved to contribute to the homeostasis of this genetically unlinked NLR network.

Item Type: Article
Additional Information: Data Availability: RNA-seq data generated in this study have been deposited under the BioProject accessions(https://www.ncbi.nlm.nih.gov/gds): PRJEB55392 and PRJEB55516. All relevant data are within the manuscript and its Supporting Information files. Funding Information: This work was funded by the Gatsby Charitable Foundation (TSL core funding) and Biotechnology and Biological Sciences Research Council (BBS/E/J/000PR9795) awarded to SK. SK also receives funding from the European Research Council (BLASTOFF). HA was funded by the Japan Society for the Promotion of Science (Overseas Research Fellowships, 21K20583 and 22K14893) and Precursory Research for Embryonic Science and Technology (JPMJPR21D1). HA received a salary from Japan Society for the Promotion of Science (Overseas Research Fellowships) and Precursory Research for Embryonic Science and Technology (JPMJPR21D1). More information about the funding sources can be found at the following web addresses: the Gatsby Charitable Foundation (https://www.gatsby.org.uk/), Biotechnology and Biological Sciences Research Council (https://www.ukri.org/councils/bbsrc/), the European Research Council (https://erc.europa.eu), the Japan Society for the Promotion of Science (https://www.jsps.go.jp/english/) and Precursory Research for Embryonic Science and Technology (https://www.jst.go.jp/kisoken/presto/en/index. html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Uncontrolled Keywords: ecology, evolution, behavior and systematics,molecular biology,genetics,genetics(clinical),cancer research,sdg 3 - good health and well-being ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
Faculty of Science > School of Biological Sciences
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 31 Oct 2024 15:30
Last Modified: 21 Nov 2024 03:31
URI: https://ueaeprints.uea.ac.uk/id/eprint/97385
DOI: 10.1371/journal.pgen.1010500

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