Comprehensive transcriptome analysis reveals coordinated multi-organ carbon metabolism responses in Medicago truncatula under water deficit stress

Medicago truncatula ( Mt ) is a relatively drought-tolerant model legume widely cultivated in Australia. Unlike previous studies that focus on specific plant components, this work reanalyses the metabolite pattern along with transcriptome data to understand the integrated response of the entire plant system to water deficit stress. Physiological and transcriptomic analyses of the leaves, taproots, and fibrous roots were performed in response to moderate and severe drought conditions. Our findings revealed that plants prioritize water supply to aboveground organs, leading to a significant decline in the root system water content during active growth. At the whole plant level, a coordinated upregulation involving LEA proteins, proline, and ABA metabolism was observed. Furthermore, carbohydrate metabolism, essential for sustaining tissue growth, was significantly altered by drought stress. Despite the well-established link between water deficit and reduced photosynthesis, which compromises carbon availability within the plant, the activation of a complete set of sucrose- and starch-degrading and -synthesising enzymes was detected. These enzymes act in concert with hexose and sucrose transporters to remobilise carbon throughout the plant system. In addition to enhanced carbon remobilisation, a notable root-specific downregulation of ethylene synthesis was observed, shedding light on the mechanism regulating plant growth under drought stress. In conclusion, our findings reveal a strong organ-specific and coordinated molecular response across progressive drought stress levels. • Medicago truncatula prioritizes water supply to aboveground organs during drought stress, leading to a significant reduction in root water content. • Drought stress triggers the activation of sucrose and starch-degrading enzymes, ensuring carbon remobilization throughout the plant via SWEET transporters. • Carbon is redirected into distinct metabolic pathways: raffinose and myo-inositol synthesis in leaves, and malate pathway activation in roots to relieve the carbon flux in glycolysis under drought conditions. • The downregulation of ethylene synthesis in fibrous roots suggests a strategy to mitigate growth inhibition during water deficit stress.