Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells

• DOI: 10.7554/elife.01967
• Publication Date: 2014-04-16T15:28:03Z
• Authors: Arun Sampathkumar; Pawel Krupinski; Raymond Wightman; Pascale Milani; Alexandre Berquand; Arezki Boudaoud; Olivier Hamant; Henrik Jönsson; Elliot M Meyerowitz
• Keywords: computational modeling; 0301 basic medicine; 570; Time Factors; QH301-705.5; [SDV]Life Sciences [q-bio]; Science; GROWTH ANISOTROPY; FUNCTIONAL ASSOCIATION; Arabidopsis; KATANIN; Microscopy, Atomic Force; Mechanotransduction, Cellular; Microtubules; Models, Biological; biomechanics; FORCE; 03 medical and health sciences; [SDV.BV]Life Sciences [q-bio]/Vegetal Biology; Computer Simulation; Biology (General); Cell Shape; Cytoskeleton; Feedback, Physiological; 0303 health sciences; ORGANOGENESIS; CORTICAL MICROTUBULES; Microscopy, Video; SHOOT APICAL MERISTEM;CORTICAL MICROTUBULES;CELLULOSE SYNTHASE;FUNCTIONAL ASSOCIATION;POSITIONAL INFORMATION;GROWTH ANISOTROPY;FORCE;ORIENTATION;KATANIN;ORGANOGENESIS; Q; R; cytoskeleton; POSITIONAL INFORMATION; Cell Biology; Medicine; cell wall; biomechanic; Stress, Mechanical; SHOOT APICAL MERISTEM; ORIENTATION; Cotyledon; CELLULOSE SYNTHASE; microtubule

Although it is a central question in biology, how cell shape controls intracellular dynamics largely remains an open question. Here, we show that the shape of Arabidopsis pavement cells creates a stress pattern that controls microtubule orientation, which then guides cell wall reinforcement. Live-imaging, combined with modeling of cell mechanics, shows that microtubules align along the maximal tensile stress direction within the cells, and atomic force microscopy demonstrates that this leads to reinforcement of the cell wall parallel to the microtubules. This feedback loop is regulated: cell-shape derived stresses could be overridden by imposed tissue level stresses, showing how competition between subcellular and supracellular cues control microtubule behavior. Furthermore, at the microtubule level, we identified an amplification mechanism in which mechanical stress promotes the microtubule response to stress by increasing severing activity. These multiscale feedbacks likely contribute to the robustness of microtubule behavior in plant epidermis.