NRC immune receptor networks show diversified hierarchical genetic architecture across plant lineages

Plants developed sophisticated immune systems consisting of nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins to repel invading pathogens. The NRC (NLR required for cell death) family is a group of helper NLRs that form a complex genetic network with multiple sensor NLRs to provide resistance against various pathogens of solanaceous plants. However, how the NRC network has evolved and how it functions outside of solanaceous plants is currently unknown. We conducted phylogenomic and macroevolutionary analyses comparing NLRs identified from different lineages of asterids and found that NRC networks showed significant lineage-specific expansion patterns in lamiids but not in Ericales and campanulids. Using transient expression assays in Nicotiana benthamiana, we show that the NRC networks in Ericales and campanulids are simple, with one or two NRC nodes, while the NRC networks of lamiids were complex, with multiple partially redundant NRC nodes. Phylogenetic analyses grouped the NRC helper NLRs into three NRC0 subclades that are conserved, and several family-specific NRC subclades of lamiids that show signatures of diversifying selection. Functional analyses of NRCs and NRC-dependent sensor NLRs from different species revealed that members of the NRC0 subclades are partially interchangeable, with several functioning with NRC0-dependent sensor NLRs across asterids. In contrast, family-specific NRC members in lamiids display a lack of interchangeability, with only a few showing compatibility with sensor NLRs across different plant families. Our findings highlight the distinctive evolutionary patterns of the NRC networks in asterids and provide potential insights into transferring disease resistance across plant lineages.