A tale of two players: the role of phosphate in iron and zinc homeostatic interactions.

MAIN CONCLUSION: This minireview details the impact of iron-phosphate and zinc-phosphate interactions in plants and provides perspectives for further areas of research regarding nutrient homeostasis. Iron (Fe) and zinc (Zn) are among the most important micronutrients for plant growth and have numerous implications for human health and agriculture. While plants have developed efficient uptake and transport mechanisms for Fe and Zn, emerging research has shown that the availability of other nutrients in the environment influences the homeostasis of Fe and Zn within plants. In this minireview, we present the current knowledge regarding homeostatic interactions of Fe and Zn with the macronutrient phosphorous (P) and the resulting physiological responses to combined deficiencies of these nutrients. Fe and P interactions have been shown to influence root development, photosynthesis, and biological processes aiding Fe uptake. Zn and P interactions also influence root growth, and coordination of Zn-dependent transcriptional regulation contributes to phosphate (Pi) transport in the plant. Understanding homeostatic interactions among these different nutrients is of critical importance to obtain a more complete understanding of plant nutrition in complex soil environments.

Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling.

Iron deficiency hampers photosynthesis and is associated with chlorosis. We recently showed that iron deficiency-induced chlorosis depends on phosphorus availability. How plants integrate these cues to control chlorophyll accumulation is unknown. Here, we show that iron limitation downregulates photosynthesis genes in a phosphorus-dependent manner. Using transcriptomics and genome-wide association analysis, we identify two genes, PHT4;4 encoding a chloroplastic ascorbate transporter and bZIP58, encoding a nuclear transcription factor, which prevent the downregulation of photosynthesis genes leading to the stay-green phenotype under iron-phosphorus deficiency. Joint limitation of these nutrients induces ascorbate accumulation by activating expression of an ascorbate biosynthesis gene, VTC4, which requires bZIP58. Furthermore, we demonstrate that chloroplastic ascorbate transport prevents the downregulation of photosynthesis genes under iron-phosphorus combined deficiency through modulation of ROS homeostasis. Our study uncovers a ROS-mediated chloroplastic retrograde signaling pathway to adapt photosynthesis to nutrient availability.

Auxin-mediated root branching is determined by the form of available nitrogen.

To improve water and nutrient acquisition from the soil, plants can modulate their root system architecture. Despite the importance of changes in root architecture to exploit local nutrient patches occurring in heterogenous soils or after placed fertilization, mechanisms integrating external nutrient signals into the root developmental programme remain poorly understood. Here, we show that local ammonium supply stimulates the accumulation of shoot-derived auxin in the root vasculature and promotes lateral root emergence to build a highly branched root system. Activities of pH and auxin reporters indicate that ammonium uptake mediated by ammonium transporters acidifies the root apoplast, which increases pH-dependent import of protonated auxin into cortical and epidermal cells overlaying lateral root primordia, and subsequently promotes their emergence from the parental root. Thereby, ammonium-induced and H+-ATPase-mediated acidification of the apoplast allows auxin to bypass the auxin importers AUX1 and LAX3. In nitrogen-deficient plants, auxin also accumulates in the root vasculature but a more alkaline apoplast leads to retention of auxin in these tissues and prevents lateral root formation. Our study highlights the impact of externally available nitrogen forms on pH-dependent radial auxin mobility and its regulatory function in organ development.