The NLR protein R1L counters Phytophthora infestans to trigger a growth-to-defense switch by degrading SlSPL3 in tomato

Plant immune responses involve sophisticated signaling networks, with effector-triggered immunity (ETI) activated by intracellular nucleotide-binding leucine-rich repeat (NLR) receptors conferring robust resistance. Understanding how ETI-associated receptors engage downstream signaling remains critical. Here, we characterize a novel tomato NLR protein, R1a-Like (R1L), that specifically recognizes the Phytophthora infestans effector AVR1. Upon AVR1 binding, R1L relocalizes from the cytoplasm to both the cytoplasm and nucleus. Genetic and molecular analyses demonstrated that R1L functions as a positive regulator of tomato immunity against P. infestans . Yeast two-hybrid screening identified SQUAMOSA PROMOTER BINDING PROTEIN LIKE 3 (SlSPL3), a positive regulator of plant growth and development, as a direct R1L interactor. SlSPL3 binds to the GTAC-box motif in the promoter of Lipid Transfer Protein 3 ( SlLTP3 ), a negative immune regulator, and activates its expression. R1L counteracts this immunosuppression by promoting ubiquitin-mediated degradation of SlSPL3, thereby enhancing immunity. Thus, the AVR1-R1L-SlSPL3-SlLTP3 axis represents a trade-off mechanism: in uninfected plants, SlSPL3 promotes growth and suppresses immunity via SlLTP3; upon infection, R1L-mediated SlSPL3 degradation activates immunity and represses growth. Our study elucidates a pathogen perception-transcriptional reprogramming-immunity axis, offering insights into plant defense and growth-immunity balance.