Heavy metal contamination threatens crop yield and food safety. Rice (Oryza sativa L.), a staple food crop for approximately half of the world’s population, must maintain its yield and quality, despite being grown in paddy fields contaminated by heavy metals. The genetic differences underlying biology in general and agronomic performance in particular between the two subspecies of rice, japonica and indica, have been intensively studied, but their responses to multiple heavy metal stresses remain poorly understood. This study investigated the divergent heavy metal resistance mechanisms between japonica (cv. Nipponbare, hereafter referred to as Nip) and indica (cv. 9311) under Cd, Cu, Mn, Zn, and Fe stress conditions. Survival assays revealed novel subspecies-specific tolerance patterns: Nip exhibited greater tolerance to Cd, Mn, Zn, and Fe, with significantly higher survival rates (e.g., 100 % vs. 0 % under Mn after 28 days) compared to 9311, which only showed marginally greater tolerance to Cu (5.3 % survival after 55 days). Physiologically, we identified divergent spatiotemporal “toolkits” underlying resistance: Nip prioritized root-centric osmoprotection via soluble sugar accumulation and early activation of shoot POD/CAT enzymes to mitigate oxidative damage, while 9311 relied on shoot-oriented soluble sugar/proline accumulation and late-phase POD/SOD induction. Critically, we established root metal sequestration as a key mechanism in Nip, which restricted Cd/Cu/Mn translocation to shoots, reducing grain metal accumulation and safeguarding crop safety. In contrast, 9311 exhibited enhanced shoot-oriented metal redistribution, exacerbated aerial toxicity, and risked yield loss under prolonged stress. These findings have advanced understanding by revealing that subspecies-specific adaptation arises from coordinated regulation of osmolyte/antioxidant dynamics and metal partitioning strategies, providing a mechanistic basis for targeted breeding to improve crop resilience in metal-polluted fields.
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