Arabidopsis PIEZO regulates magnetic field-mediated root growth under blue light

The mechanosensitive ion channel PIEZO is known to play a role in root growth. However, whether the PIEZO gene responds to magnetic fields and the mechanisms underlying its regulation of root growth remain unclear. Here, we demonstrate that Arabidopsis PIEZO regulates root growth in response to both MF and blue light. Mutation of PIEZO led to a significantly shorter roots under MF exposure and blue light illumination. We further identified that PIEZO expression in root tips was up-regulated by a blue light-induced signal, which is transmitted from leaves to roots in the presence of a MF. PIEZO modulated calcium ion efflux and disturbed auxin transport, specifically through interactions with PIN-FORMED (PIN) 3, 6 and 7 under combined MF and blue light conditions. Notably, the blue light receptors CRYPTOCHROME 1 (CRY1) and CRY2 were essential for both MF perception and the regulation of root growth. Transcriptome analysis of the piezo-cl mutant under MF and blue light revealed that the PIEZO integrates multiple signaling pathways, including those involved in gibberellin 4 (GA4), ethylene, calcium ion-related genes, mechanosensors, and microRNAs. Specifically, miR5648-5p expression conferred MF sensitivity and provided a mechanism for the negative regulation of PIEZO under these conditions. Our findings elucidate a multifactorial mechanism by which PIEZO coordinates root growth responses to MF and blue light, integrating phytohormone signaling, mechanosensation, calcium ion dynamics, and light perception. This study highlights PIEZO as a central node in a complex network that converges diverse environmental cues to regulate root growth. One-Sentence Summary: PIEZO integrates magnetic fields and blue light signaling to regulate root growth in Arabidopsis through coordinated phytohormone, calcium, and mechanosensory pathways.