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

Elife. 2014 Apr 16:3:e01967. doi: 10.7554/eLife.01967.

Abstract

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. DOI: http://dx.doi.org/10.7554/eLife.01967.001.

Keywords: biomechanics; cell wall; computational modeling; cytoskeleton; microtubule.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Video-Audio Media

MeSH terms

  • Arabidopsis / cytology
  • Arabidopsis / embryology
  • Arabidopsis / physiology*
  • Cell Shape*
  • Computer Simulation
  • Cotyledon / cytology
  • Cotyledon / physiology*
  • Cytoskeleton / physiology*
  • Feedback, Physiological
  • Mechanotransduction, Cellular*
  • Microscopy, Atomic Force
  • Microscopy, Video
  • Microtubules / physiology
  • Models, Biological
  • Stress, Mechanical
  • Time Factors

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.