SPX4 interacts with both PHR1 and PAP1 to regulate critical steps in phosphorus-status-dependent anthocyanin biosynthesis

Phosphate (Pi) is the plant-accessible form of phosphorus, and its insufficiency limits plant growth. The over-accumulation of anthocyanins in plants is often an indication of Pi starvation. However, whether the two pathways are directly linked and which components are involved in this process await identification. Here, we demonstrate that SPX4, a conserved regulator of the Pi response, transduces the Pi starvation signal to anthocyanin biosynthesis in Arabidopsis. When phr1spx4 plants were grown under low Pi conditions, DFR expression and anthocyanin biosynthesis were induced, which distinguished the plant from the behavior reported in the phr1 mutant. We also provide evidence that SPX4 interacts with PAP1, an MYB transcription factor that controls the anthocyanin biosynthetic pathway, in an inositol polyphosphate-dependent manner. Through a physical interaction, SPX4 prevented PAP1 from binding to its target gene promoter; by contrast, during Pi-deficient conditions, in the absence of inositol polyphosphates, PAP1 was released from SPX to activate anthocyanin biosynthesis. Our results reveal a direct link between Pi deficiency and flavonoid metabolism. This new regulatory module, at least partially independent from PHR1, may contribute to developing a strategy for plants to adapt to Pi starvation.