A genetically unlinked NLR network that modulates plant immunity against diverse pathogens originated from an ancestral gene cluster

NLR immune receptors in the NRC superclade form an intricate network that confers resistance to a multitude of plant pathogens. This network is comprised of sensor NLRs, specialized in detection of pathogen effectors, that require helper NLRs, known as NRCs, to initiate immune responses. The network originated from a linked NLR pair that evolved prior to the divergence of asterids and caryophyllales over 100 million years ago, and expanded to half of all NLRs in some asterid species. We used phylogenomics methods to reconstruct the evolutionary history of the NRC family. One of the NRCs, we termed NRC0, is the only family member shared among different asterid species, leading us to investigate its evolutionary history and genetic organization. In tomato, carrot, coffee and morning glory, NRC0 is closely linked to NLRs that are phylogenetically related to NRC-dependent sensors. This prompted us to hypothesize that the ancestral state of the NRC network is an NLR helper-sensor gene cluster that was present in early asterids. We validated this hypothesis by demonstrating that tomato NRC0 is essential for the hypersensitive cell death induced by its genetically linked NLR. We are testing the degree to which the functional dependency between NRC0 and the linked NLRs is conserved across asterids. These results revealed the evolutionary dynamics of NLR receptor networks and how coevolution with pathogens drivesthe expansion and diversification of NLRs.