Iron plaque formation confers plant hypoxia tolerance by regulating root oxygen dynamics and respiratory metabolism

Iron plaque, a phenomenon widely found in wetland plants, is an accumulation of metal (hydr)oxides precipitated on root surfaces primarily driven by rhizosphere oxidation. However, the potential function of iron plaque on plant hypoxia tolerance is largely ignored. Thus, the effects of iron plaque on root O2 dynamics and respiratory metabolism were investigated using the seedlings of Aegiceras corniculatum. O2 microelectrodes were applied to determine partial pressure of oxygen (pO2) within roots, while respiratory metabolism was analyzed using enzyme activity assay kits, transcriptomics and real-time quantitative PCR (qRT-PCR). Visible reddish plaques were observed on the roots of field-collected A. corniculatum seedlings, forming a coating that appeared to penetrate the intercellular spaces of the outer one to two cell layers. The data further revealed a significant role of iron plaque in elevating pO2 within roots, which can mitigate hypoxic inhibition and benefit plant performance under hypoxic stresses. Compared with non-plaque roots, roots with iron plaque exhibited significantly higher adenosine triphosphate (ATP), elevated tricarboxylic acid (TCA) respiration rates, and upregulated TCA cycle-associated enzymes and genes. Besides, suppressed anaerobic fermentation-associated byproducts (e.g., ethanol) and enzymes/genes (e.g., alcohol dehydrogenase and its encoding gene AcADH1) were simultaneously observed in the roots with iron plaque due to enhanced root internal pO2. Suppressed glycolysis pathway was also observed in the roots with iron plaque, indicating less consumption of carbon resources under hypoxic stresses. In conclusion, this study provided evidence for an interesting link between iron plaque and increased O2 retention within roots, which improved the efficiency of ATP yield through respiratory metabolism.