Display options
Share it on

Front Plant Sci. 2016 Sep 07;7:1351. doi: 10.3389/fpls.2016.01351. eCollection 2016.

A Mechanical Model to Interpret Cell-Scale Indentation Experiments on Plant Tissues in Terms of Cell Wall Elasticity and Turgor Pressure.

Frontiers in plant science

Richard Malgat, François Faure, Arezki Boudaoud

Affiliations

  1. Institut National de Recherche en Informatique et en AutomatiqueGrenoble, France; Laboratoire Jean Kuntzmann, Centre National de la Recherche ScientifiqueGrenoble, France; Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, Institut National de la Recherche Agronomique, Centre National de la Recherche ScientifiqueLyon, France.
  2. Institut National de Recherche en Informatique et en AutomatiqueGrenoble, France; Laboratoire Jean Kuntzmann, Centre National de la Recherche ScientifiqueGrenoble, France.
  3. Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique Lyon, France.

PMID: 27656191 PMCID: PMC5013127 DOI: 10.3389/fpls.2016.01351

Abstract

Morphogenesis in plants is directly linked to the mechanical elements of growing tissues, namely cell wall and inner cell pressure. Studies of these structural elements are now often performed using indentation methods such as atomic force microscopy. In these methods, a probe applies a force to the tissue surface at a subcellular scale and its displacement is monitored, yielding force-displacement curves that reflect tissue mechanics. However, the interpretation of these curves is challenging as they may depend not only on the cell probed, but also on neighboring cells, or even on the whole tissue. Here, we build a realistic three-dimensional model of the indentation of a flower bud using SOFA (Simulation Open Framework Architecture), in order to provide a framework for the analysis of force-displacement curves obtained experimentally. We find that the shape of indentation curves mostly depends on the ratio between cell pressure and wall modulus. Hysteresis in force-displacement curves can be accounted for by a viscoelastic behavior of the cell wall. We consider differences in elastic modulus between cell layers and we show that, according to the location of indentation and to the size of the probe, force-displacement curves are sensitive with different weights to the mechanical components of the two most external cell layers. Our results confirm most of the interpretations of previous experiments and provide a guide to future experimental work.

Keywords: atomic force microscope; cell wall; floral meristem; indentation; mechanical model; physically-based simulation; shoot apical meristem; turgor

References

  1. Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:447-472 - PubMed
  2. Science. 2008 Dec 12;322(5908):1650-5 - PubMed
  3. Curr Biol. 2011 Oct 25;21(20):1720-6 - PubMed
  4. Trends Plant Sci. 2010 Jun;15(6):353-60 - PubMed
  5. Soft Matter. 2015 Feb 4;11(7):1281-92 - PubMed
  6. Elife. 2014 Apr 16;3:e01967 - PubMed
  7. Front Plant Sci. 2015 Nov 26;6:1038 - PubMed
  8. Plant Physiol. 2010 Feb;152(2):420-7 - PubMed
  9. Plant J. 2013 Feb;73(3):509-20 - PubMed
  10. Plants (Basel). 2015 Mar 25;4(2):167-82 - PubMed
  11. J Exp Bot. 2013 Nov;64(15):4729-44 - PubMed
  12. Biophys J. 2009 Jul 22;97(2):674-7 - PubMed
  13. Curr Biol. 2008 Dec 23;18(24):1943-8 - PubMed
  14. Proc Natl Acad Sci U S A. 2004 Apr 6;101(14):4728-35 - PubMed
  15. Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9783-8 - PubMed
  16. Plant J. 2013 Feb;73(4):617-27 - PubMed
  17. PLoS One. 2013;8(3):e57813 - PubMed
  18. Nat Methods. 2010 Jul;7(7):547-53 - PubMed
  19. Science. 2012 Mar 2;335(6072):1096-9 - PubMed
  20. Plant J. 2011 Sep;67(6):1116-23 - PubMed
  21. J Plant Growth Regul. 2000 Mar;19(1):90-7 - PubMed
  22. J Exp Bot. 2016 Jan;67(2):463-76 - PubMed
  23. Ann Bot. 2014 Nov;114(7):1517-33 - PubMed
  24. Int J Eng Sci. 2009 Nov 1;47(11):1274-1283 - PubMed
  25. Annu Rev Cell Dev Biol. 2014;30:59-78 - PubMed
  26. Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11812-7 - PubMed
  27. Biophys J. 2012 Aug 8;103(3):386-94 - PubMed
  28. Am J Bot. 2006 Oct;93(10):1380-90 - PubMed
  29. Phys Rev Lett. 2012 Oct 5;109(14):144302 - PubMed
  30. Curr Biol. 2015 Jun 29;25(13):1746-52 - PubMed
  31. J Exp Bot. 2013 Nov;64(15):4651-62 - PubMed
  32. PLoS Comput Biol. 2015 Jan 08;11(1):e1003950 - PubMed
  33. Annu Rev Plant Biol. 2011;62:365-85 - PubMed
  34. Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Feb;85(2 Pt 1):021916 - PubMed
  35. Curr Opin Plant Biol. 2013 Feb;16(1):25-32 - PubMed
  36. J R Soc Interface. 2012 Mar 7;9(68):448-55 - PubMed
  37. Biophys J. 2015 May 19;108(10):2448-56 - PubMed
  38. J Mech Behav Biomed Mater. 2016 Sep;62:222-35 - PubMed
  39. J Exp Bot. 2012 Apr;63(7):2525-40 - PubMed
  40. J Exp Bot. 2013 Nov;64(15):4617-33 - PubMed
  41. Plant Physiol. 2001 Oct;127(2):381-5 - PubMed
  42. J Exp Bot. 2015 Jun;66(11):3229-41 - PubMed
  43. Plant Physiol. 2014 Jun 12;165(4):1399-1408 - PubMed
  44. Plant Physiol. 2012 Apr;158(4):1514-22 - PubMed
  45. Am J Bot. 2006 Oct;93(10):1415-25 - PubMed
  46. Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8685-90 - PubMed

Publication Types