Use of phosphate to avoid uranium toxicity in Arabidopsis thaliana leads to alterations of morphological and physiological responses regulated by phosphate availability

Abstract

Uranium is an ubiquitous pollutant with known chemical and radiological toxicity, which is naturally present in the plant environment. Due to its high affinity for phosphate, insoluble uranium-phosphate precipitates are formed in soils as well as in contaminated plant cells. To date, consequences of such interactions on uranium toxicity and on phosphate availability and metabolism in plants are unknown. This study aims at evaluating in which extent uranium-phosphate interactions have an effect on physiological and molecular mechanisms involved in plant responses (i) to uranium contamination and (ii) to phosphate availability in Arabidopsis thaliana. Inorganic phosphate (Pi) supply in U-contaminated medium was shown to decrease U bioaccumulation and U toxic effects on plant biomass and root cell viability. Besides, U was shown to disturb plant responses to Pi availability. Indeed, in Pi-sufficient conditions, high U concentrations promoted the induction of phosphate starvation responses in plants. However, the most drastic effects have been observed in Pi-deficient conditions as U affected the following plant responses to Pi-starvation: root architecture modulation, phosphate acquisition and optimization of phosphate allocation. Indeed, despite the low Pi status of these plants, 2 μM U inhibited the primary root growth arrest normally triggered by low Pi. Moreover, Pi uptake and translocation to shoot were reduced. The root concentration of soluble inorganic phosphate decreased in Pi-starved plantlets contaminated with U, despite the enhancement of shoot-to-root remobilization of Pi. The observations of intracellular and apoplastic deposits of U and P in roots using electron microscopy (TEM-EDX) and secondary ion mass spectroscopy (NanoSIMS) provided evidence that Pi flux disturbance is a consequence of the use of Pi to immobilize U within roots.