The NRC0 gene cluster of sensor and helper NLR immune receptors is functionally conserved across asterid plants

Sakai, Toshiyuki, Contreras, Mauricio P., Martinez-Anaya, Claudia, Lüdke, Daniel, Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315, Wu, Chih-Hang and Adachi, Hiroaki (2024) The NRC0 gene cluster of sensor and helper NLR immune receptors is functionally conserved across asterid plants. The Plant Cell, 36 (9). pp. 3344-3361. ISSN 1040-4651

[thumbnail of Sakai_etal_2024_ThePlantCell]
Preview
PDF (Sakai_etal_2024_ThePlantCell) - Published Version
Available under License Creative Commons Attribution.

Download (1MB) | Preview

Abstract

Nucleotide-binding domain and leucine-rich repeat-containing receptor (NLR) proteins can form complex receptor networks to confer innate immunity. An NLR-REQUIRED FOR CELL DEATH (NRC) is a phylogenetically related node that functions downstream of a massively expanded network of disease resistance proteins that protect against multiple plant pathogens. In this study, we used phylogenomic methods to reconstruct the macroevolution of the NRC family. One of the NRCs, termed NRC0, is the only family member shared across asterid plants, leading us to investigate its evolutionary history and genetic organization. In several asterid species, NRC0 is genetically clustered with other NLRs that are phylogenetically related to NRC-dependent disease resistance genes. This prompted us to hypothesize that the ancestral state of the NRC network is an NLR helper-sensor gene cluster that was present early during asterid evolution. We provide support for this hypothesis by demonstrating that NRC0 is essential for the hypersensitive cell death that is induced by its genetically linked sensor NLR partners in 4 divergent asterid species: tomato (Solanum lycopersicum), wild sweet potato (Ipomoea trifida), coffee (Coffea canephora), and carrot (Daucus carota). In addition, activation of a sensor NLR leads to higher-order complex formation of its genetically linked NRC0, similar to other NRCs. Our findings map out contrasting evolutionary dynamics in the macroevolution of the NRC network over the last 125 million years, from a functionally conserved NLR gene cluster to a massive genetically dispersed network.

Item Type: Article
Additional Information: Data availability statement: All large-scale data are provided in the manuscript and supplementary datasets. Funding Information: This work was funded by the Gatsby Charitable Foundation, Biotechnology and Biological Sciences Research Council (BBSRC, UK, BB/WW002221/1, BB/V002937/1, BBS/E/J/000PR9795, and BBS/E/J/000PR9796) and the European Research Council (BLASTOFF). H.A. was funded by the Japan Science and Technology Agency, Precursory Research for Embryonic Science and Technology (JPMJPR21D1). C.-H.W. was funded by the 2030 Cross-Generation Young Scholars Program of the National Science and Technology Council, Taiwan (NSTC 112-2628-B-001-007). C.M.-A. is grateful to have enrolled in the DGAPA-PASPA UNAM Program, which financed a sabbatical year at The Sainsbury Laboratory.
Uncontrolled Keywords: plant science ,/dk/atira/pure/subjectarea/asjc/1100/1110
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: 23 Oct 2024 10:30
Last Modified: 17 Dec 2024 01:41
URI: https://ueaeprints.uea.ac.uk/id/eprint/97133
DOI: 10.1093/plcell/koae154

Downloads

Downloads per month over past year

Actions (login required)

View Item View Item