Environmental cues profoundly modulate cell proliferation and cell elongation to inform and direct plant growth and development. External phosphate (Pi) limitation inhibits primary root growth in many plant species. However, the underlying Pi sensory mechanisms are unknown. Here we genetically uncouple two Pi sensing pathways in the root apex of Arabidopsis thaliana. First, the rapid inhibition of cell elongation in the transition zone is controlled by transcription factor STOP1, by its direct target, ALMT1, encoding a malate channel, and by ferroxidase LPR1, which together mediate Fe and peroxidase-dependent cell wall stiffening. Second, during the subsequent slow inhibition of cell proliferation in the apical meristem, which is mediated by LPR1-dependent, but largely STOP1–ALMT1-independent, Fe and callose accumulate in the stem cell niche, leading to meristem reduction. Our work uncovers STOP1 and ALMT1 as a signalling pathway of low Pi availability and exuded malate as an unexpected apoplastic inhibitor of root cell wall expansion.

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.