The epidermis coordinates multi-scale symmetry breaking in chiral root growth

Twisted growth serves myriad adaptive functions in plants. Unlike animal motions, plant motions require symmetry breaking during growth and typically involve microtubule-related genes. But how macroscopic twisting emerges from molecular-level perturbations remains unclear. Here, we show that microtubule-based symmetry breaking propagates across multiple organizational scales via the epidermis to produce handed root skewing. At the nanoscale, aberrant patterning of cellulose microfibrils is associated with microscale skewed cell expansion, both of which precede the millimeter scale emergence of helical epidermal cell files. The resulting chiral torsion of the epidermis mediates organ level symmetry breaking in the form of whole-root skewing through macroscale interactions between the root and its surrounding environment. We demonstrate the dominant role of the epidermis by complementation of microtubule activity in the epidermis alone, which is sufficient to restore transverse cortical microtubule orientation, wild-type-like morphology in cortical cells, and straight root growth.