Exogenous regulators that alleviate waterlogging stress in plants: mechanisms, integration, and translational...

Exogenous regulators mitigate waterlogging stress via a three-tier framework; integrated strategies boost field waterlogging resilience effectively. Waterlogging, an increasingly critical constraint on crop productivity with climate change amplifying extreme precipitation, limits rhizospheric O₂ diffusion to induce hypoxia. This rapidly impairs mitochondrial respiration, forces a shift to low-efficiency glycolysis and fermentation, and accumulates potentially toxic by-products. Upon postanoxic stress, plants face an oxidative burst that compromises membrane integrity, suppresses photosynthesis, and destabilizes yield. Despite inherent adaptive programs (e.g., aerenchyma formation, adventitious rooting), most crops remain vulnerable to prolonged/recurrent waterlogging, necessitating practical interventions complementing genetic improvement. Here, we synthesize evidence that exogenous inputs-including phytohormones, osmoprotectants, antioxidants, gaseous signaling molecules, mineral nutrients, and beneficial microorganisms-mitigate injury by coordinating early signaling, metabolic maintenance, and rhizosphere stabilization. We integrate these effects into a three-tier framework: (i) resetting hypoxia perception/response thresholds, (ii) sustaining energy/redox homeostasis via balanced mitochondrial function and fermentation, and (iii) converting short-term tolerance to sustained recovery through morphological remodeling and rhizosphere improvement. Finally, we outline a translational strategy coupling exogenous regulation with functional microbiomes, targeted genetic improvement, and agronomic management to enhance field robustness and reduce environment-driven "effect drift". Highlights Exogenous regulators improve plant-waterlogging tolerance via a three-layer regulatory framework. A combined application of exogenous substances, microbiome, genetics, and agronomy enhances field waterlogging resistance. Hypoxia response, energy metabolism, and ROS homeostasis are core regulatory targets for stress alleviation.