The sugar-sensing kinase OSK3-mediated destabilization of OsbZIP58 promotes pre-harvest sprouting in rice under high...

Pre-harvest sprouting (PHS) is a major problem in cereal production, severely reducing yield and grain quality, particularly under high-temperature (HT) and excessive-rainfall conditions during grain filling. However, the molecular mechanisms by which HT triggers seed dormancy breakdown and promotes PHS remain largely unknown. In this study, we reveal that the rice transcription factor OsbZIP58, previously implicated in seed storage reserve accumulation, integrates HT-induced sugar depletion into precocious seed dormancy release. By combining DNA affinity purification sequencing, chromatin immunoprecipitation-qPCR, and genetic epistasis analyses, we show that OsbZIP58 directly activates the abscisic acid-responsive gene RAB16A while repressing the α-amylase gene OsAmy3D, thereby maintaining seed dormancy under normal conditions. Meanwhile, the energy-sensing sucrose non-fermenting-1-related protein kinase 1-family kinase OSK3, a direct upstream regulator, phosphorylates OsbZIP58 at Ser46 to promote its proteasomal degradation, consequently derepressing OsAmy3D expression. Mechanistically, HT accelerates grain filling and causes premature sugar depletion, which activates OSK3 to trigger OsbZIP58 degradation, thereby releasing OsAmy3D activity to increase starch hydrolysis and soluble sugar levels in seeds, ultimately leading to PHS. Elevated soluble sugar levels restrain OSK3 hyperactivation under HT through a negative-feedback mechanism. Furthermore, haplotype analysis reveals that natural variation in the OsbZIP58 locus is associated with variation in PHS susceptibility among rice accessions. Collectively, our work uncovers the OSK3-OsbZIP58-OsAmy3D module in regulating PHS in response to HT and establishes a previously unrecognized signaling cascade that integrates cellular energy status with developmental timing and thermal stress, providing genetic targets for breeding climate-resilient PHS-resistant cereals.