Rapid local and systemic jasmonate signalling drives the initiation and establishment of plant systemic immunity

nature plants Article https://doi.org/10.1038/s41477-025-02178-4 Rapid local and systemic jasmonate signalling drives the initiation and establishment of plant systemic immunity Received: 16 May 2024 Accepted: 17 November 2025 Published online: 6 January 2026 Trupti Gaikwad1,6,8, Susan Breen 1,7,8, Emily Breeze1,8, Erin Stroud1,8, Rana Hussain1, Satish Kulasekaran2, Nestoras Kargios1, Fay Bennett1, Marta de Torres-Zabala3, David Horsell4, Lorenzo Frigerio 1, Pradeep Kachroo 5 & Murray Grant 1 Check for updates Successful recognition of pathogen effectors by plant disease resistance proteins, or effector-triggered immunity (ETI), contains the invading pathogen through localized hypersensitive cell death. ETI also activates long-range signalling to establish broad-spectrum systemic acquired resistance (SAR). Here we describe a sensitive luciferase (LUC) reporter that captures the spatial–temporal dynamics of SAR signal generation, propagation and establishment in systemic responding leaves following ETI. JASMONATE-INDUCED SYSTEMIC SIGNAL 1 (JISS1) encodes an endoplasmic-reticulum-localized protein of unknown function. JISS1::LUC captured very early ETI-elicited SAR signalling, which surprisingly was not affected by classical SAR mutants but was dependent on calcium and was also wound responsive. Both jasmonate biosynthesis and perception mutants abolished JISS1::LUC signalling and SAR to Pseudomonas syringae. Furthermore, we discovered that ETI initiated jasmonate-dependent systemic surface electrical potentials. These surface potentials were dependent on both glutamate receptors and JISS1, despite neither JISS1 loss-of-function nor glutamate receptor mutants altering SAR to Pseudomonas syringae. We thus demonstrate that jasmonate signalling, usually associated with antagonism of defence against biotrophs, is crucial to the rapid initiation and establishment of SAR systemic defence responses (including the activation of systemic surface potentials) and that JISS1::LUC serves as a reporter to further dissect these pathways. Despite the discovery of plant systemic acquired resistance (SAR) over a century ago, our knowledge of the signalling processes underlying the establishment, propagation and especially initiation of this response remains fragmentary. Classically, SAR is established following effector-triggered immunity (ETI) leading to the hypersensitive response (HR). SAR has also been reported to be activated via pathogen-associated molecular pattern recognition and virulent bacterial phytopathogens, although the latter has also been reported to trigger systemic induced susceptibility1,2. A full list of affiliations appears at the end of the paper. Nature Plants | Volume 12 | January 2026 | 152–163 Multiple molecules are implicated in SAR induction, including salicylic acid (SA) and its volatile derivative methyl salicylate, azelaic acid (AZA), glycerol-3-phosphate, dehydroabietinal, pipecolic acid (Pip) and N-hydroxy-pipecolic acid (NHP). More recently, extracellular NAD(P), the volatile monoterpenes α- and β-pinene, vitamin B6 and small RNAs derived from TAS3a were shown to induce SAR3–6. HR-generated reactive oxygen species (ROS) and nitric oxide (NO) are integral to ETI-initiated SAR, most likely via C18 unsaturated fatty acid oxidation of chloroplast lipids2,7. Hydrolysis of C18 fatty acids released e-mail: 152 Article from thylakoid membrane monogalactosyldiacylglycerol and digalactosyldiacylglycerol generates AZA8,9. The importance of lipid signalling in SAR is highlighted by the involvement of lipid transfer proteins, AZELAIC ACID INDUCED1 (AZI1) and DEFECTIVE IN INDUCED RESISTANCE1 (DIR1)8. Plants defective in SA, glycerol-3-phosphate, NO or ROS biosynthesis have reduced levels of Pip in distal tissues, reinforcing the complex metabolic interplay in the establishment of SAR10. Airborne defence cues also activate SAR11; thus, one can conclude that multiple signals translocating apoplastically, symplastically12,13 and as volatiles can collectively confer broad-spectrum systemic resistance against diverse pathogens, including viral, bacterial, oomycete, fungal and insect pests2. The synthesis, activities and interactions of these SAR inducers have been extensively reviewed10,14–16. Despite progress in understanding the individual signalling networks leading to SAR, the spatial–temporal dynamics and interactions of various chemical signals in the SAR pathway remain unclear. Recognition of Pseudomonas syringae pv. tomato DC3000 (DC) carrying avrRpm1 (DCavrRpm1)17 by the Resistance to P. maculicola 1 (RPM1) disease resistance protein provides a robust ETI model to dissect signal generation and transduction dynamics underlying SAR. We previously demonstrated that RPM1 activation triggers early increases in cytosolic calcium, beginning ~1.5–2 h post-infection (hpi)18,19, followed by lipid-peroxidation-triggered biophoton generation ~3 hpi20,21 and visible leaf collapse ~6 hpi. RPM1 activation elicits rapid transcriptional reprogramming 4 hpi in systemic leaves, which strongly overlaps with jasmonate-triggered systemic wound responses22. Here we report JASMONATE-INDUCED SYSTEMIC SIGNAL 1 (JISS1), a jasmonate-responsive SAR reporter that captures unexpectedly rapid temporal–spatial dynamics following ETI. We show that SAR requires enzymatic production of a local jasmonate signal that propagates via the vasculature and epidermal cells to systemic leaves and is coupled to calcium- and jasmonate-dependent systemic surface electrical potentials. Results JISS1 expression reveals temporal and spatial dynamics of early effector–resistance gene interactions JISS1 (At5g56980; previously known as A70 (ref. 22)), a protein of unknown function, is an early SAR marker22. To monitor SAR transcriptional dynamics, we fused the promoter of JISS1 and the sequence encoding the first 84 amino acids of JISS1 to luciferase (Extended Data Fig. 1). Homozygous JISS1 promoter::luciferase (JISS1::LUC) lines showed rapid systemic luciferase activity following challenge with DCavrRpm1, but not with virulent DC; the type-III-secretion-system-deficient DChrpA, which elicits pathogen-associated-molecular-pattern-triggered immunity (PTI) responses; or mock challenge (MgCl2) (Fig. 1a). SAR signal propagation was remarkably rapid, with strong luciferase activity first evident in the petiole of the challenged leaf ~3 hpi (Fig. 1b), and within 30 min JISS1::LUC activity was established23,24. This activity spread to adjacent leaves (~4 hpi, Fig. 1b), reaching maximal intensity ~4.5 hpi, ~1 h prior to any visible collapse of the challenged leaf. Challenge with DCavrRpt2 or DCavrRps4 also induced systemic luciferase activity following recognition by Resistance to P. syringae 2 (RPS2)25 and RPS4 (ref. 26), respectively (Fig. 1c). The spatial pattern of systemic luciferase reporter activity was identical for all ETI responses, but initiation timing differed for each resistance (R) protein, cons (...truncated)