Many signaling proteins permanently or transiently localize to specific organelles for function. It is well established that certain lipids act as biochemical landmarks to specify compartment identity. However, they also influence membrane biophysical properties, which emerge as important features in specifying cellular territories. Such parameters include the membrane inner surface potential, which varies according to the lipid composition of each organelle. Here, we found that the plant plasma membrane (PM) and the cell plate of dividing cells have a unique electrostatic signature controlled by phosphatidylinositol-4-phosphate (PI4P). Our results further reveal that, contrarily to other eukaryotes, PI4P massively accumulates at the PM, establishing it as a critical hallmark of this membrane in plants. Membrane surface charges control the PM localization and function of the polar auxin transport regulator PINOID, as well as proteins from the BRI1 KINASE INHIBITOR1 (BKI1)/MEMBRANE ASSOCIATED KINASE REGULATORs (MAKRs) family, which are involved in brassinosteroid and receptor-like kinase signaling. We anticipate that this PI4P-driven physical membrane property will control the localization and function of many proteins involved in development, reproduction, immunity and nutrition.

SUMMARYPhosphate is a crucial and often limiting nutrient for plant growth. To obtain inorganic phosphate (P i ), which is very insoluble, and is heterogeneously distributed in the soil, plants have evolved a complex network of morphological and biochemical processes. These processes are controlled by a regulatory system triggered by P i concentration, not only present in the medium (external P i ), but also inside plant cells (internal P i ). A 'splitroot' assay was performed to mimic a heterogeneous environment, after which a transcriptomic analysis identified groups of genes either locally or systemically regulated by P i starvation at the transcriptional level. These groups revealed coordinated regulations for various functions associated with P i starvation (including P i uptake, P i recovery, lipid metabolism, and metal uptake), and distinct roles for members in gene families. Genetic tools and physiological analyses revealed that genes that are locally regulated appear to be modulated mostly by root development independently of the internal P i content. By contrast, internal P i was essential to promote the activation of systemic regulation. Reducing the flow of P i had no effect on the systemic response, suggesting that a secondary signal, independent of P i , could be involved in the response. Furthermore, our results display a direct role for the transcription factor PHR1, as genes systemically controlled by low P i have promoters enriched with P1BS motif (PHR1-binding sequences). These data detail various regulatory systems regarding P i starvation responses (systemic versus local, and internal versus external P i ), and provide tools to analyze and classify the effects of P i starvation on plant physiology.