Astaxanthin biofortification enhances tobacco tolerance to lead stress through boosting antioxidant defense, reducing Pb accumulation, and modulating detoxification pathways

Introduction: Heavy metal pollution including lead (Pb) has become one of the serious global issues threatening food security, human health, and the ecosystem. Exogenous application of astaxanthin (ATX), a potent natural antioxidant, has been shown to enhance plant tolerance to various abiotic stresses. However, the role of endogenous ATX in alleviating Pb stress and the underlying molecular mechanisms remain poorly understood. Objectives: This study aimed to systematically investigate the effects and mechanism of endogenous ATX in biofortified tobacco (T-ATX) in promoting plant growth, particularly enhancing plant tolerance to Pb toxicity and blocking Pb pollution. Methods: Pot experiments were employed to investigate plant growth and Pb tolerance as well as Pb absorption and translocation in T-ATX and wild-type (SNN) tobacco seedlings subjected to various doses of Pb stress. Multiple physiological and cellular examinations were conducted, followed by integrated omics approaches in this study. Results: T-ATX plants exhibited an increased plant height, root length, leaf area, and biomass compared to SNN under Pb stress. T-ATX displayed higher levels of chlorophyll, photosynthetic efficiency, antioxidant enzyme activities, and non-enzymatic antioxidants, with improved integrity of subcellular structures. Remarkably, Pb content in various organs and Pb translocation coefficient were significantly reduced in T-ATX. Multiple genes and metabolites associated with antioxidant defense mechanisms, detoxification pathways, carotenoid metabolism, Pb ion transport, and plant hormone signal transduction were significantly upregulated in T-ATX tobacco plants. Conclusion: Endogenous ATX enriched in the T-ATX genotype significantly confers plant healthy performance and high tolerance to Pb stress by enhancing the antioxidant defense system, maintaining cellular structural integrity, reducing Pb absorption and translocation, upregulating detoxification and the related signaling pathways. These findings provide new insights into the endogenous ATX-mediated molecular mechanisms to promote plant growth and mitigate Pb toxicity, establishing a foundation for using ATX-fortified crops for green control technology of heavy metal pollution.