Mechanical forces instruct division plane orientation of cambium stem cells during radial growth inArabidopsis thaliana

Abstract

AbstractPrecise regulation of cell division is central for the formation of complex multicellular organisms and a hallmark of stem cell activity. In plants, due to the absence of cell migration, correct placement of newly produced cell walls during cell division is of eminent importance for generating functional tissues and organs. In particular, during radial growth of plant shoots and roots, concerted cell divisions in the cambium are essential to produce adjacent xylem and phloem tissues in a strictly bidirectional manner. While several intercellular signaling cascades have been identified to instruct tissue organization during radial growth, a role of mechanical forces in guiding cambium stem cell activity has been frequently proposed but, so far, not been functionally investigated on the cellular level. Here, we coupled anatomical analyses with a cell-based vertex model to analyze the role of mechanical stress in radial plant growth at the cell and tissue scale. Simulations based on segmented cellular outlines of radially growingArabidopsishypocotyls revealed a distinct stress pattern with circumferential stresses in cambium stem cells which coincided with the orientation of cortical microtubules. Integrating stress patterns as a cue instructing cell division orientation was sufficient for the emergence of typical cambium-derived cell files and agreed with experimental results for stress-related tissue organization in confining mechanical environments. Our work thus underlines the significance of mechanical forces in tissue organization through self-emerging stress patterns during the growth of plant organs.