Multi-omics and genetic analysis uncover salicylic acid-mediated core signaling networks for seed longevity in rice

Seed longevity is a critical agronomic trait underpinning crop productivity, yet its regulation remains less understood due to the complexity of interacting signaling pathways. Here, we identified an aging-resistant rice (Oryza sativa L.) cultivar ZH11 that shows a higher seed germination rate and vigor, higher salicylic acid (SA) content, and lower reactive oxygen species (ROS) level than other cultivars (NJ505 and XF9) under aging treatment. Integrated multi-omics analyses revealed six key pathways-oxidative phosphorylation, plant-pathogen interactions, photosynthesis, carbon fixation, ATP-binding cassette (ABC) transport, and hormone signaling-converging on nine core genes (OsUbOR, OsA10, WRKY42, OsPKD, OsPRCW, OsYGD1-1, OsABCB14, OsPYL3, OsNPR1). Deficiency of each of the nine key genes leads to mutants with a phenotype of markedly reduced seed viability. The differential expression of these key genes across ZH11, NJ505, and XF9, together with the dose-dependent rescue of the shortened seed longevity phenotype in NJ505 and XF9 by SA, confirms that SA acts as a key bridge mediating distinct signaling pathways. The interactions between the SA receptor NPR1 (Nonexpressor of Pathogenesis-Related 1) and bZIP03/bZIP28 (Basic Leucine Zipper 03/28) were identified as potential targets and components for regulating seed longevity. Furthermore, the interactions of NPR1-Protein Phosphatase 2C 30 (PP2C30) and PP2C30-bZIP28 further underscored the role of SA signaling in the aging process of rice seeds. Our findings provide mechanistic insights into seed viability regulation and offer genetic targets for breeding crops with extended seed storage potential and quality for sustainable agriculture.