TY - JOUR
T1 - The NRC0 gene cluster of sensor and helper NLR immune receptors is functionally conserved across asterid plants
AU - Sakai, Toshiyuki
AU - Contreras, Mauricio P.
AU - Martinez-Anaya, Claudia
AU - Lüdke, Daniel
AU - Kamoun, Sophien
AU - Wu, Chih-Hang
AU - Adachi, Hiroaki
N1 - 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.
PY - 2024/9
Y1 - 2024/9
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85199635929&partnerID=8YFLogxK
U2 - 10.1093/plcell/koae154
DO - 10.1093/plcell/koae154
M3 - Article
C2 - 38833594
AN - SCOPUS:85199635929
SN - 1040-4651
VL - 36
SP - 3344
EP - 3361
JO - The Plant Cell
JF - The Plant Cell
IS - 9
ER -