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Phosphate transport and signaling in Arabidopsis

Final Report Summary - PHOSTASIA (Phosphate transport and signaling in Arabidopsis)

In modern agriculture, the use of phosphate (Pi)-based fertilizers is essential to maximize yields and ensure an adequate food supply to a growing world population. Yet, Pi is a non-renewable resource, just like mineral oil, that will be exhausted one day and needs to be used with caution. On the other hand, a significant portion of Pi applied to agricultural fields reaches rivers and lakes, representing a major cause of water pollution that leads to eutrophication. Despite the importance of Pi management, we know little about how plants sense and adapt to fluctuation in soil Pi content, in particular to Pi deficiency. Understanding how plants sense and adapt to Pi deficiency is key to attain sustainable agriculture. Plants take up Pi via their roots from where it is transported to the green parts of the plants, the shoot. Nutrient transfer to the shoot requires the export of Pi into the xylem vessel, which is essentially a tube enabling the movement of water and nutrients from the roots to the shoots. Contrary to Pi import from the soil into root cells, mechanisms regulating Pi export into the root xylem vessel largely unknown despite being essential for Pi homeostasis in plants. The only protein known to mediate Pi efflux is the thale cress (Arabidopsis thaliana) PHO1. PHO1 mediates Pi loading into the root xylem, and plants without a functional PHO1 protein (pho1 knock-out mutants) show severe Pi starvation in the shoots. PHO1 is also involved in the sensing the Pi deficiency and mediating adaptation of plants to this deficiency (so called signaling role), linking low Pi content to reduced growth and gene activation. PHO1 has thus a dual function in transport of Pi and in signaling to Pi deficiency, a feature typical of “transceptors” (combination of transporter and sensor activities). The PHO1 proteins can be divided into three distinctive subdomains, which functions were not known at the beginning of this project.

During our IEF project “PHOSTASIA”, we could successfully determine the structure of the Pi exporter PHO1 of Arabidopsis thaliana. With this knowledge, we constructed several different truncations of PHO1, all composed of distinct domains, to analyse their role in the activity of PHO1 either as a Pi exporter or a component of the Pi-deficiency signaling cascade, and determine their role on PHO1 localization within the cell. After an initial study in tobacco regarding Pi transport activity and membrane localisation, we were able to construct transgenic Arabidopsis plants that grow like wild-type plants and show the same seed yield despite containing low Pi content in both shoots and roots. These plants constitute the first step towards optimising crop plants to meet the demand for future plants that use less Pi but maintain optimal field yield.

Additionally to the PHO1 protein in plants, a mammalian homologue of PHO1, called XPR1, was also functionally investigated during this project, to determine if PHO1-like proteins in other organisms, such as humans, also play a role in mediating Pi export. No Pi-export protein had been previously been identified in humans or other animals, despite the importance of Pi export in ensuring proper functioning of kidney and intestine. By expressing the mouse (Mus musculus) XPR1 in tobacco cells, we were able to show that also XPR1 functions as a Pi-exporter, making it the first Pi-exporter identified in animals.