Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis

SUMMARYInorganic phosphate (Pi) is one of the most limiting nutrients for plant growth in both natural and agriculturalcontexts. Pi-deficiency leads to a strong decrease in shoot growth, and triggers extensive changes at thedevelopmental, biochemical and gene expression levels that are presumably aimed at improving theacquisition of this nutrient and sustaining growth. The Arabidopsis thaliana PHO1 gene has previously beenshown toparticipatein the transportof Pi fromroots toshoots, andthe null pho1 mutant hasall the hallmarksassociated with shoot Pi deficiency. We show here that A. thaliana plants with a reduced expression of PHO1in roots have shoot growth similar to Pi-sufficient plants, despite leaves being strongly Pi deficient.Furthermore, the gene expression profile normally triggered by Pi deficiency is suppressed in plants with lowPHO1 expression. At comparable levels of shoot Pi supply, the wild type reduces shoot growth but maintainsadequate shoot vacuolar Pi content, whereas the PHO1 underexpressor maintains maximal growth withstrongly depleted Pi reserves. Expression of the Oryza sativa (rice) PHO1 ortholog in the pho1 null mutant alsoleads to plants that maintain normal growth and suppression of the Pi-deficiency response, despite the lowshoot Pi. These data show that it is possible to unlink low shoot Pi content with the responses normallyassociated with Pi deficiency through the modulation of PHO1 expression or activity. These data also showthat reduced shoot growth is not a direct consequence of Pi deficiency, but is more likely to be a result ofextensive gene expression reprogramming triggered by Pi deficiency.Keywords: phosphate, PHO1, nutrient deficiency, signal transduction.INTRODUCTIONOf the macronutrients required for plant growth, phospho-rus is the least mobile in soil. Plants absorb phosphorusfrom the roots as orthophosphate (inorganic phosphate, Pi).Pi concentration in most soils is in the low micromolarrange, and may even drop to submicromolar levels at theroot/soil interface. Plants respond to growth in Pi-deficientenvironments with numerous changes at the biochemical,morphological, developmental and gene expression levels.For example, vacuolar Pi reserves are mobilized, phospha-tases are secreted to scavenge Pi from organic sources,phospholipids are replaced by sulfolipids and galactolipids,root hair density and length are increased, and growth ofsecondary roots is promoted (Poirier and Bucher, 2002).Microarray studies revealed that several hundreds of genesare either induced or repressed following Pi starvation(Misson et al., 2004; Morcuende et al., 2007; Mu¨ller et al.,2007). Collectively, all these changes are thought to help theplant improve the acquisition of this vital nutrient, therebysustaining growth and improving plant survival. From anagronomical point of view, the main deleterious effects ofPi deficiency is a strong reduction in shoot growth. The wideuse of Pi-containing fertilizers is aimed at compensating thislimitation, andthusassuringmaximumcrop yield.However,this agricultural practice is costly, non-sustainable and