Proline–Nitrogen Metabolic Coordination Mediates Cold Priming-Induced Freezing Tolerance in Maize

Cold stress critically restricts maize seedling growth in Northeast China, yet the mechanism by which cold priming (CP) enhances cold tolerance through proline–nitrogen metabolic networks remains unclear. This study systematically investigated CP’s synergistic regulation in cold-tolerant (<i>H...

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Main Authors: Zhijia Gai, Lei Liu, Na Zhang, Jingqi Liu, Lijun Cai, Xu Yang, Ao Zhang, Pengfei Zhang, Junjie Ding, Yifei Zhang
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/10/1415
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Summary:Cold stress critically restricts maize seedling growth in Northeast China, yet the mechanism by which cold priming (CP) enhances cold tolerance through proline–nitrogen metabolic networks remains unclear. This study systematically investigated CP’s synergistic regulation in cold-tolerant (<i>Heyu27</i>) and cold-sensitive (<i>Dunyu213</i>) maize using a two-phase temperature regime (priming induction/stress response) with physiological and multivariate analyses. CP alleviated cold-induced photosynthetic inhibition while maintaining a higher chlorophyll and photosynthetic rate, though biomass responses showed varietal specificity, with <i>Heyu27</i> minimizing growth loss through optimized carbon–nitrogen allocation. Antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were pre-activated during early stress, effectively scavenging reactive oxygen species (ROS) and reducing malondialdehyde (MDA) accumulation, with <i>Heyu27</i> showing superior redox homeostasis. CP enhanced proline accumulation via bidirectional enzyme regulation (upregulating ∆<sup>1</sup>-pyrroline-5-carboxylate synthase/reductase [P5CS/P5CR], inhibiting proline dehydrogenase [ProDH]) and reprogrammed nitrogen metabolism through glutamate dehydrogenase/isocitrate dehydrogenase (GDH/ICDH)-mediated ammonium conversion to glutamate, alleviating nitrogen dysregulation while supplying proline precursors. Principal component analysis revealed divergent strategies: <i>Heyu27</i> prioritized proline–antioxidant synergy, whereas <i>Dunyu213</i> emphasized photosynthetic adjustments. These findings demonstrate that CP establishes “metabolic memory” through optimized proline–nitrogen coordination, synergistically enhancing osmoregulation, reactive oxygen species (ROS) scavenging, and nitrogen utilization. This study elucidates C<sub>4</sub>-specific cold adaptation mechanisms, advancing cold-resistant breeding and stress-resilient agronomy.
ISSN:2223-7747