Phosphate starvation alters abiotic stress-induced cytosolic free calcium increases in roots

Phosphate (Pi) deficiency strongly limits plant growth, and plant roots foraging the soil for nutrients need to adapt to optimize Pi uptake. Ca2+ is known to signal in root development and adaptation but has to be tightly controlled as it is highly toxic to Pi metabolism. Under Pi starvation and a resulting decreased cellular Pi pool, the use of cytosolic free Ca2+ ([Ca2+]cyt) as a signal transducer may therefore have to be altered. Employing aequorin-expressing Arabidopsis, we show that Pi starvation but not nitrogen starvation strongly dampens the [Ca2+]cyt increases evoked by mechanical, salt, osmotic, and oxidative stress as well as by extracellular nucleotides. The altered root [Ca2+]cyt response to extracellular ATP manifests during seedling development under chronic Pi deprivation, but can be reversed by Pi resupply. Employing ratiometric imaging, we delineate that Pi-starved roots have a normal response to extracellular ATP at the apex, but show a strongly dampened [Ca2+]cyt response in distal parts of the root tip, correlating with high reactive oxygen species (ROS) levels induced by Pi starvation. Excluding iron, as well as Pi, rescues this altered [Ca2+]cyt response, and restores ROS levels to those under nutrient-replete conditions. These results indicate that, whilst Pi availability does not seem to be signalled through [Ca2+]cyt, Pi starvation strongly affects stress-induced [Ca2+]cyt signatures. The data reveal how plants can integrate nutritional and environmental cues, adding another layer of complexity to the use of Ca2+ as a signal transducer.