Raphael Tiziani, Fabio Trevisan, Ondřej Hodek, Sandra Jämtgård, T. Moritz, Oussama Bouaicha, M. Chibesa, Ilaria Fracasso, Tanja Mimmo
Root-exuded organic acids are crucial in mitigating iron (Fe) and phosphorus (P) deficiencies, and 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 tomato plants grown hydroponically using 13C-labelling with 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 contents, reduced photosynthesis, altered root morphology, and an altered citric acid uptake that 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, enhancing resource use efficiency. Unexpectedly, citric acid uptake increased with plant development. In Fe deficiency, citric acid-derived carbon was allocated to secondary metabolites, while in P deficiency it supported the tricarboxylic acid and GS-GOGAT cycles. This study is the first to demonstrate that citric acid uptake is a multifunctional process, underscoring its critical role in plant responses to nutrient starvation, especially under P deficiency.