Region-specific responses of wheat adventitious roots to waterlogging stress.

Abstract

Waterlogging is a major abiotic stress that restricts global wheat production. Although adventitious root formation and aerenchyma development are key adaptive strategies to waterlogging, the spatial mechanisms underlying root adaptation remain unclear. Here, we systematically analyzed the anatomical, physiological, and metabolic responses in the basal (RB), middle (RM), and tip (RT) regions of wheat adventitious roots under different waterlogging durations. Aerenchyma formation was most pronounced in the root middle, which also exhibited the highest levels of reactive oxygen species (ROS) and antioxidant enzyme activities. Phytohormone profiling revealed distinct spatial regulation: ethylene levels increased steadily and localized mainly in the root tip, while abscisic acid, gibberellins, and jasmonic acid accumulated predominantly in the basal and middle, peaking at 24 h of waterlogging. Metabolomic and spatial imaging analyses revealed that prolonged waterlogging induced increases in metabolites related to carbon/energy metabolism and antioxidant defense, and promoted the tissue-specific accumulation of non-enzymatic antioxidants (e.g., glutathione and ascorbate) around the endodermis region and root tip. In conclusion, these findings revealed that wheat adventitious roots employ a coordinated, region-specific strategy of integrating enzymatic antioxidant defense, aerenchyma development, hormonal signaling, and spatially compartmentalized metabolites to develop waterlogging tolerance.