Transcriptomic and metabolomic approaches elucidate the systemic response of wheat plants under waterlogging

Extreme weather conditions lead to significant imbalances in crop productivity, which in turn affect food security. Flooding events cause serious problems for many crop species such as wheat. Although metabolic readjustments under flooding are important for plant regeneration, underlying processes remain poorly understood. Here, we investigated the systemic response of wheat to waterlogging using metabolomics and transcriptomics. A 12 d exposure to excess water triggered nutritional imbalances and disruption of metabolite synthesis and translocation, reflected by reductions in plant biomass and growth performance. Metabolic and transcriptomic profiling in roots, xylem sap, and leaves indicated anaerobic fermentation processes as a local response in roots. Differentially expressed genes and ontological categories revealed that carbohydrate metabolism plays an important role in the systemic response. Analysis of the composition of xylem exudates revealed decreased root-to-shoot translocation of nutrients, hormones, and amino acids. Interestingly, among all metabolites measured in xylem exudates, alanine was the most abundant. Immersion of excised leaves derived from waterlogged plants in alanine solution led to increased leaf glucose concentration. Our results suggest an important role of alanine not only as an amino-nitrogen donor but also as a vehicle for carbon skeletons to produce glucose de novo and meet the energy demand during waterlogging. Metabolic and transcriptomic changes in wheat highlight alanine as the major root-to-shoot translocated and systemically acting metabolite for balancing carbon and nitrogen between roots and shoots.