A pair of NLRs coordinately modulates NRC3-mediated ETI responses to facilitate age-dependent immunity

Abstract

AbstractTwo NLRs (Nucleotide-binding and Leucine-rich repeat Receptors) adjacent to each other on a locus, termed as paired NLRs, may act separately for effector recognition and subsequent signaling activation to mediate effector-triggered immunity (ETI) in many plants. However, it is largely unknown about their distribution and functions in Solanaceae species, in which NLR-Hs (Helpers NLR REQUIRED FOR CELL DEATHs) have been extensively studied. Here, we identified paired NLRs in Solanaceae species and found they harbor paired NLRs ranging from 6 to 100, which are significantly negatively correlated with the numbers of NLR-Hs.N. benthamianahas six paired NLRs, among which silencing ofNRCXexhibits phenotypes of dwarfism and accelerated senescence. Importantly,NRCX-silencing phenotypes could be restored by simultaneously silencing its head-to-head NLR pair, thus we named it asNRCY. NRCX/Y pair is specific in Solanaceae species. NRCY contains non-canonical walker B and MHD motifs, but could not induce autoactive cell death inN. benthamiana. Instead of that, silencingNRCYimpaired cell death triggered by Sw5b-Nsm and NRC3D480V, indicating NRCY is also an NLR modulator like NRCX. Furthermore, NRCX suppression of Sw5b-Nsm and NRC3-mediated cell death is dependent on NRCY. Remarkably, we found thatNRCXandNRCYexpressions were induced during plant senescence, whileNRCYwas induced more thanNRCX. Accordingly, the plant resistance was stronger during maturation, indicated NRCX/Y might be involved in age-dependent resistance. Our study reveals one of the paired NLRs coordinately regulates ETI to facilitate age-dependent immunity.