Waterlogging stress priming at the seedling stage alleviates waterlogging damage at the heading stage in wheat

Waterlogging stress increasingly threatens global wheat production, yet effective, genotype-specific mitigation strategies remain limited. Here, we investigated whether short-term waterlogging pre-exposure (treated as priming, 24 h or 48 h) at the seedling stage alleviates yield losses caused by subsequent waterlogging at the heading stage in two wheat cultivars with contrasting tolerance (tolerant Yangmai 20, YM20; sensitive Jimai 22, JM22). Priming effectively mitigated yield loss, but efficacy was highly dependent on genotype and priming duration. In YM20, both priming durations reduced yield loss from ∼30% to <10%, primarily due to maintaining grains per spike. In JM22, only 24 h priming conferred significant yield protection; 48 h priming became detrimental, reducing grain weight even without subsequent stress. Priming induced a persistent aerenchyma memory in adventitious roots months later, but maximal aerenchyma formation was not required for yield protection. Instead, the best-performing treatment (24 h-primed YM20) minimized structural investment and prioritized antioxidant capacity (CAT, GSH), sustained ethylene acclimation memory (ACO activity), and selectively upregulated genes involved in manganese ion response and plant–pathogen interaction. miRNA sequencing revealed divergent molecular strategies: YM20 mobilized distinct regulatory networks under 24 h and 48 h priming, whereas JM22 exhibited a less coordinated response. Collectively, seedling-stage waterlogging priming can confer long-lasting tolerance to reproductive-stage waterlogging, but success depends on cultivar tolerance and precise priming duration. Optimized priming offers a cost-effective strategy to enhance wheat resilience under increasingly flood-prone climates, provided protocols are tailored to the inherent acclimation capacity of each genotype.