Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis

Abstract

Phosphate 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 ‘split‐root’ 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.