Soybean tolerance to waterlogging is achieved by detoxifying root lactate via lactate dehydrogenase in leaves and metabolizing malate and succinate

Waterlogging is a significant stressor for crops, particularly in lowland regions where soil conditions exacerbate the problem. Waterlogged roots experience hypoxia, disrupting oxidative phosphorylation and triggering metabolic reorganization to sustain energy production. Here, we investigated the metabolic aspects that differentiate two soybean sister lines contrasting for waterlogging tolerance. After 11 days of waterlogging, roots of the tolerant line (PELBR15-7015C) modulated their fermentative metabolism by exporting key metabolites (lactate, malate, and succinate) to the shoot. These metabolites were metabolized in the leaves, supporting photosynthesis and facilitating sugar export to the roots, sustaining a root-shoot-root cycling process. In contrast, the sensitive line (PELBR15-7060) entered a quiescent state, depleting its carbon stock and accumulating protective metabolites. Our study reveals that long-term waterlogging tolerance is primarily achieved through lactate detoxification in the leaves, along with malate and succinate metabolism, enabling root metabolism to withstand hypoxia. This mechanism offers new insights into crop resilience under waterlogged conditions, with implications for modern agriculture as climate change intensifies the frequency and duration of such stress events.