Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis

Phosphate (P-i) is a major limiting factor for plant growth. Plants respond to limiting P-i supplies by inducing a suite of adaptive responses comprising altered growth behaviour, enhanced P-i acquisition and reduced P-i demand that together define a distinct physiological state. In P-i-starved plants, continued root growth is required for P-i acquisition from new sources, yet meristem activity consumes P-i. Therefore, we analysed the relationship between organ growth, phosphate starvation-responsive (PSR) gene expression and P-i content in Arabidopsis thaliana under growth-promoting or inhibitory conditions. Induction of PSR gene expression after transfer of plants to P-i-depleted conditions quantitatively reflects prior levels of P-i acquisition, and hence is sensitive to the balance of P-i supply and demand. When plants are P-i-starved, enhanced root or shoot growth exacerbates, whereas growth inhibition suppresses, P-i starvation responses, suggesting that the magnitude of organ growth activity specifies the level of P-i demand. Inhibition of cell-cycle activity, but not of cell expansion or cell growth, reduces P-i starvation-responsive gene expression. Thus, the level of cell-cycle activity specifies the magnitude of P-i demand in P-i-starved plants. We propose that cell-cycle activity is the ultimate arbiter for P-i demand in growing organs, and that other factors that influence levels of PSR gene expression do so by affecting growth through modulation of meristem activity.