The response of shoots to phosphate (Pi) deficiency implicates long-distance communication between roots and shoots, but the participating components are poorly understood. We have studied the topology of the Arabidopsis thaliana PHO1 Pi exporter and defined the functions of its different domains in Pi homeostasis and signaling. Results indicate that the N- and C-termini of PHO1 are both oriented towards the cytosol and that the protein is spanning the membrane twice in the EXS domain, resulting in a total of 6 transmembrane α-helices. Using transient expression in tobacco leaf, we demonstrated that the EXS domain of PHO1 is essential for Pi export activity and proper localization to the Golgi and trans Golgi network, although the EXS domain by itself cannot mediate Pi export. In contrast, removal of the N-terminal hydrophilic SPX domain does not affect the Pi export capacity of the truncated PHO1 in tobacco. While the Arabidopsis pho1 mutant has low shoot Pi and shows all the hallmarks associated with Pi deficiency, including poor shoot growth and overexpression of numerous Pi-deficiency responsive genes, expression of only the EXS domain of PHO1 in the roots of the pho1 mutant results in a remarkable improvement of shoot growth despite low shoot Pi. Transcriptomic analysis of pho1 expressing the EXS domain indicates an attenuation of the Pi signaling cascade and the up-regulation of genes involved in cell wall synthesis and the synthesis or response to several phytohormones in leaves as well as an altered expression of genes responsive to ABA in roots.

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