Deciphering underexplored rhizosphere processes: root acquisition of citric acid and its metabolic journey in tomato

Root-exuded organic acids are crucial in mitigating iron (Fe) and phosphorus (P) deficiencies. Their biosynthesis and secretion require significant metabolic investment. Recent studies have shown that roots can also uptake exudates. We hypothesized that citric acid uptake increases under Fe and P deficiencies, declines over time, and contributes to primary metabolism. We investigated citric acid uptake, translocation, and metabolization in Fe- and P-deficient in hydroponically-grown tomato plants. We applied 13C-labeled citric acid analysed through bulk stable isotope and compound-specific stable isotope analysis. Physiological parameters, root morphology, and elemental composition were also assessed. Deficient plants showed reduced P and Fe content, reduced photosynthesis, altered root morphology and an altered citric acid uptake, which could not be attributed to morphological differences. Iron deficiency reduced citric acid uptake, indicating its role in rhizospheric Fe mobilization, while P deficiency increased the uptake emphasizing resource use efficiency. Unexpectedly, citric acid uptake increased with plant development. In Fe deficiency, citric acid-derived carbon is allocated to secondary metabolites, while in P deficiency, it supports the TCA and GS-GOGAT cycles. This study is the first to demonstrate citric acid uptake as a multifunctional process, underscoring its critical role in plant responses to nutrient starvation, especially under P deficiency.