Randuch, M.; Kulich, I.; Vladimirtsev, D.; Huang, S.; Hedrich, R.; Friml, J.

Roots must continuously adapt their growth and have evolved the ability to rapidly respond to diverse environmental and hormonal cues, including the phytohormone auxin. Auxin-induced cellular responses involve membrane depolarization, cytosolic calcium (Ca2+) elevation, and extracellular pH increase, but how these processes lead to rapid growth regulation remains unclear. Here, we show that cytosolic Ca2+ acts as a universal signal integrating diverse cues for the rapid regulation of root growth. Using live imaging, microfluidics, and optogenetics in Arabidopsis, we demonstrate that a swift rise in cytosolic Ca2+ is the primary target of auxin signaling affecting growth inhibition. Disruption of Ca2+ influx abolishes these responses, whereas light-gated Ca2+ influx from the apoplast or endoplasmic reticulum stores inhibits growth. Multiple unrelated stimuli-including auxin, extracellular ATP, RALF peptides, and hydrogen peroxide - converge on this Ca2+-dependent mechanism. Cytosolic Ca2+; elevation thus represents a necessary and sufficient step for rapid growth inhibition, revealing a unifying principle of root signaling.