Alarmone ((p)ppGpp) signalling tunes Arabidopsis thaliana nuclear gene expression to shape the balance of plant immune outcomes

RSH enzymes (RelA/SpoT homologs) synthesize ppGpp (guanosine tetra-/pentaphosphate) in plastids, regulating organelle function. More importantly, whether ppGpp acts as a simple rheostat on immune output or determines which mode of defence a plant deploys remains poorly understood. Using Arabidopsis thaliana lines with high (RSH3OX) or null (rshq) ppGpp levels, we show that ppGpp controls nuclear-encoded defence genes in salicylic acid (SA) and jasmonic acid (JA) metabolism, including hormone-inactivating enzymes in RSH3OX and MeSA-to-SA conversion genes in rshq. Conversely, pathogen infection induces the ppGpp synthases RSH2 and RSH3, with induction preceding defence gene activation and requiring SA biosynthesis and a functional Type III secretion system. RSH3OX plants are hypersusceptible to Pseudomonas syringae pv. tomato DC3000, show impaired pattern-triggered immunity, and exhibit an accelerated decline in photosynthetic efficiency, while rshq plants show enhanced resistance to P. syringae but increased susceptibility to the necrotrophic fungus Botrytis cinerea. Using an inducible line to acutely elevate ppGpp, we confirm this susceptibility is directly caused by ppGpp levels, not a chronic developmental consequence of RSH3OX. Together, these results indicate that ppGpp governs the mode of immune execution rather than simply scaling its magnitude, acting as a chloroplast-based checkpoint linking organellar status to the nuclear defence transcriptome.