OsIPK2 Regulates Seed Vigor by Integrating IP6 Biosynthesis, Auxin Signaling, and H3K27me3 Deposition in Japonica Rice

Seed vigor is a key agronomic trait that integrates germination capacity and seedling establishment, critically influencing rice productivity. Inositol hexakisphosphate (IP₆) serves as a major phosphorus reservoir in seeds, yet its regulatory mechanism in seed vigor remains unclear. Here, we demonstrate that exogenous IP₆ application inhibited seed germination and seedling growth of japonica rice <i>(Oryza sativa</i> L. ssp. <i>japonica cv. Zhonghua11</i>) in a dose-dependent manner; 10 mM IP₆ reduced seed germination by 100%, while 100 μM IP₆ suppressed primary root length by 33.6% compared to the control. This inhibitory effect is likely mediated by antagonizing auxin signaling, as supported by suppressed <i>DR5::GUS</i> expression and altered transcription of auxin-responsive genes. <i>OsIPK2</i>, a key enzyme in IP₆ biosynthesis, showed high expression during early development in rice. RNA interference of <i>OsIPK2</i> led to a 40.8-61.7% reduction in seed IP₆ content, 45.3-65% higher zinc (Zn) and iron (Fe) accumulation, and a 35.4-53.5% lower germination rate compared to wild-type (WT). Conversely, <i>OsIPK2</i>-RNAi seedlings exhibited enhanced growth and resistance to IP₆, which was associated with misregulation of auxin-responsive genes and a decrease in the repressive histone mark H3K27me3 at their loci. Furthermore, endogenous indole-3-acetic acid (IAA) levels significantly reduced in Ri-1 but unchanged in Ri-2, while abscisic acid (ABA) content and the IAA/ABA ratio remained unaltered compared to wild-type. Our findings reveal that <i>OsIPK2</i> balances seed vigor and seedling development by modulating inositol phosphate metabolism, auxin responses, and epigenetic regulation, providing insights for improving seed quality in cereals. Whether the regulatory role of <i>OsIPK2</i> in seed vigor is conserved across other rice subspecies requires further investigation.