title: Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells.
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.
authors.affiliation: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States.
authors.forename: Arun
authors.initials: A
authors.lastname: Sampathkumar
authors.forename: Pawel
authors.initials: P
authors.lastname: Krupinski
authors.forename: Raymond
authors.initials: R
authors.lastname: Wightman
authors.forename: Pascale
authors.initials: P
authors.lastname: Milani
authors.forename: Alexandre
authors.initials: A
authors.lastname: Berquand
authors.forename: Arezki
authors.initials: A
authors.lastname: Boudaoud
authors.forename: Olivier
authors.initials: O
authors.lastname: Hamant
authors.forename: Henrik
authors.initials: H
authors.lastname: Jönsson
authors.forename: Elliot M
authors.initials: EM
authors.lastname: Meyerowitz
mesh_terms: D017360:Arabidopsis / Q000166:cytology / Q000196:embryology / Q000502:physiology*; D048430:Cell Shape; D003198:Computer Simulation; D018548:Cotyledon / Q000166:cytology / Q000502:physiology*; D003599:Cytoskeleton / Q000502:physiology*; D025461:Feedback, Physiological; D040542:Mechanotransduction, Cellular; D018625:Microscopy, Atomic Force; D018715:Microscopy, Video; D008870:Microtubules / Q000502:physiology; D008954:Models, Biological; D013314:Stress, Mechanical; D013997:Time Factors
keywords: biomechanics; cell wall; computational modeling; cytoskeleton; microtubule
references.citation: Cell. 2005 Mar 11;120(5):687-700
references.pmid: 15766531
references.citation: Plant Physiol. 1999 Feb;119(2):681-92
references.pmid: 9952465
references.citation: Nat Protoc. 2014 Feb;9(2):457-63
references.pmid: 24481272
references.citation: Sci Signal. 2009 Apr 14;2(66):ra16
references.pmid: 19366994
references.citation: PLoS Biol. 2010 Oct 19;8(10):e1000516
references.pmid: 20976043
references.citation: J Exp Bot. 2009;60(14):4175-87
references.pmid: 19684107
references.citation: Plant J. 2011 Sep;67(6):1116-23
references.pmid: 21605208
references.citation: Am J Bot. 2006 Oct;93(10):1415-25
references.pmid: 21642088
references.citation: Biophys J. 2011 May 18;100(10):2440-9
references.pmid: 21575578
references.citation: Cell. 2010 Oct 1;143(1):99-110
references.pmid: 20887895
references.citation: Biophys J. 2002 Jun;82(6):2916-27
references.pmid: 12023214
references.citation: Cell. 2009 Jun 26;137(7):1331-42
references.pmid: 19563762
references.citation: Plant Cell. 2012 Jan;24(1):163-77
references.pmid: 22294619
references.citation: Cell. 2012 Apr 13;149(2):439-51
references.pmid: 22500806
references.citation: Curr Biol. 2010 Sep 14;20(17):1499-510
references.pmid: 20691592
references.citation: Lab Chip. 2013 Jul 7;13(13):2599-608
references.pmid: 23571308
references.citation: Proc Natl Acad Sci U S A. 2013 Sep 3;110(36):14670-5
references.pmid: 23964126
references.citation: Plant J. 2011 Jun;66(6):915-28
references.pmid: 21535258
references.citation: Proc Natl Acad Sci U S A. 2012 Sep 18;109(38):15101-8
references.pmid: 22932871
references.citation: Nat Rev Mol Cell Biol. 2007 Aug;8(8):633-44
references.pmid: 17643125
references.citation: J Cell Biol. 1993 Aug;122(4):859-75
references.pmid: 8349735
references.citation: Science. 2013 Dec 6;342(6163):1245533
references.pmid: 24200811
references.citation: Plant Cell. 2011 Jul;23(7):2592-605
references.pmid: 21742992
references.citation: Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1633-8
references.pmid: 16415160
references.citation: Mol Biol Cell. 2005 Aug;16(8):3764-75
references.pmid: 15930123
references.citation: Nat Cell Biol. 2007 Jul;9(7):832-7
references.pmid: 17572669
references.citation: Plant J. 2001 Jan;25(2):137-48
references.pmid: 11169190
references.citation: J Theor Biol. 1969 Oct;25(1):1-47
references.pmid: 4390734
references.citation: Plant J. 2007 Nov;52(4):742-51
references.pmid: 17877711
references.citation: Ann Bot. 2004 Jul;94(1):9-32
references.pmid: 15155376
references.citation: Development. 2012 Dec 1;139(23):4416-27
references.pmid: 23095885
references.citation: J Cell Sci. 2010 Oct 15;123(Pt 20):3490-5
references.pmid: 20876662
references.citation: BMC Plant Biol. 2011 Feb 01;11:27
references.pmid: 21284861
references.citation: Nature. 2009 Jan 22;457(7228):495-9
references.pmid: 19029882
references.citation: Science. 2008 Dec 12;322(5908):1650-5
references.pmid: 19074340
references.citation: Science. 2006 Jun 9;312(5779):1491-5
references.pmid: 16627697
references.citation: Cold Spring Harb Perspect Biol. 2009 Sep;1(3):a001255
references.pmid: 20066104
references.citation: Cell. 2006 Aug 25;126(4):677-89
references.pmid: 16923388
references.citation: Development. 2008 Oct;135(19):3175-83
references.pmid: 18776142
references.citation: Annu Rev Cell Dev Biol. 2008;24:551-75
references.pmid: 18837672
references.citation: Science. 2012 Mar 2;335(6072):1096-9
references.pmid: 22383847
references.citation: Curr Biol. 2013 Feb 18;23(4):290-7
references.pmid: 23394835
references.citation: Trends Cell Biol. 2012 Nov;22(11):584-91
references.pmid: 22980034
references.citation: Curr Biol. 2013 Oct 7;23(19):1902-7
references.pmid: 24055158
references.citation: Curr Biol. 2013 Nov 4;23(21):2191-5
references.pmid: 24206847
references.citation: J Exp Bot. 2012 Apr;63(7):2525-40
references.pmid: 22291130
references.citation: J Plant Physiol. 2007 Nov;164(11):1395-409
references.pmid: 17905474
references.citation: Nature. 2007 May 24;447(7143):493-6
references.pmid: 17495931
references.citation: BMC Plant Biol. 2013 Oct 18;13:163
references.pmid: 24138025
references.citation: J Plant Growth Regul. 2000 Mar;19(1):7-18
references.pmid: 11010988
references.citation: Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3318-23
references.pmid: 15728365
references.citation: Planta. 2002 Oct;215(6):989-96
references.pmid: 12355159
references.citation: Plant Physiol. 2001 Jan;125(1):387-95
references.pmid: 11154346
references.citation: PLoS Biol. 2010 May 11;8(5):e1000367
references.pmid: 20485493
references.citation: Annu Rev Biophys Biophys Chem. 1988;17:431-49
references.pmid: 3293594