Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport

Roots of phosphorus (P)-deficient white lupin exhibit striking changes in morphology and gene expression. In this report we provide further insight into genetic elements affecting transcription of P-deficiency-induced genes. Moreover, we also show that sugars and photosynthates are integrally related to P-deficiency-induced gene expression. White lupin phosphate transporter (LaPT1) and secreted acid phosphatase (LaSAP1) promoter-reporter genes when transformed into alfalfa, a heterologous legume, showed significant induction in roots specifically in response to P-deficiency. In addition, both promoters were active in nitrogen-fixing root nodules but not in ineffective nodules indicating a link between P-deficiency and factors related to nitrogen fixation/metabolism. As sugars play a role in signal transduction during nitrogen assimilation and are required for effective nitrogen fixation, we tested the relationship of sugars to P-deficiency-induced gene expression. Exogenous sucrose, glucose, and fructose stimulated LaPT1 and LaSAP1 transcript accumulation in dark-grown P-sufficient white lupin seedlings. Furthermore, in intact P-deficient white lupin plants, LaPT1 and LaSAP1 expression in cluster roots was strikingly reduced in dark-adapted plants with expression rapidly restored upon reexposure to light. Likewise, interruption of phloem supply to P-deficient roots resulted in a rapid decline in LaPT1 and LaSAP1 transcript accumulation. Similar results were also obtained with a third lupin P-deficiency-induced gene encoding a putative multidrug and toxin efflux protein (LaMATE). Taken together, our data show that the regulation of P-deficiency-induced genes is conserved across plant species and sugars/photosynthates are crucial for P-deficiency signal transduction.