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PMID: 29683428 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

A tension-adhesion feedback loop in plant epidermis.

eLife ·Vol. 7 ·2018-00-23

Verger S, Long Y, Boudaoud A, Hamant O

Abstract

Mechanical forces have emerged as coordinating signals for most cell functions. Yet, because forces are invisible, mapping tensile stress patterns in tissues remains a major challenge in all kingdoms. Here we take advantage of the adhesion defects in the Arabidopsis mutant quasimodo1 (qua1) to deduce stress patterns in tissues. By reducing the water potential and epidermal tension in planta, we rescued the adhesion defects in qua1, formally associating gaping and tensile stress patterns in the mutant. Using suboptimal water potential conditions, we revealed the relative contributions of shape- and growth-derived stress in prescribing maximal tension directions in aerial tissues. Consistently, the tension patterns deduced from the gaping patterns in qua1 matched the pattern of cortical microtubules, which are thought to align with maximal tension, in wild-type organs. Conversely, loss of epidermis continuity in the qua1 mutant hampered supracellular microtubule alignments, revealing that coordination through tensile stress requires cell-cell adhesion.

Keywords
A. thaliana cell adhesion mechanical stress microtubules plant biology plant organs
MeSH Terms
Arabidopsis/genetics,physiology Arabidopsis Proteins Cell Adhesion Feedback Hexosyltransferases/deficiency Microtubules/metabolism Plant Epidermis/physiology Stress, Mechanical Stress, Physiological
Chemicals
Arabidopsis Proteins Hexosyltransferases QUA1 protein, Arabidopsis
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Verger Stéphane ORCID
Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, Lyon, France.
Long Yuchen
Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, Lyon, France.
Boudaoud Arezki
Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, Lyon, France.
Hamant Olivier ORCID
Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, Lyon, France.
Other Abstracts
eng

The parts of a plant that protrude from the ground are constantly shaken by the wind, applying forces to the plant that it must be able to resist. Indeed, mechanical forces are crucial for the development, growth and life of all organisms and can trigger certain behaviours or the production of particular molecules: for example, forces that bend a plant trigger gene activity that ultimately makes the stem more rigid. Mechanical forces can also originate from inside the organism. For example, the epidermal cells that cover the surface of a plant are placed under tension by the cells in the underlying layers of the plant as they grow and expand. The exact pattern of forces in the plant epidermis was not known because they cannot be directly seen, although scientists have tried to map them using theoretical and computational modeling. A mutant form of the Arabidopsis plant is unable to produce some of the molecules that allow epidermal cells to adhere to each other. Verger et al. placed the mutants in different growth conditions that lowered the pressure inside the plant, and consequently reduced the tension on the epidermal cells. This partly restored the ability of epidermal cells to adhere to each other, although gaps remained between cells in regions of the plant that have been predicted to be under high levels of tension. Verger et al. could therefore use the patterns of the gaps to map the forces across the epidermis, opening the path for the study of the role of these forces in plant development. Further experiments showed that cell adhesion defects prevent the epidermal cells from coordinating how they respond to mechanical forces. There is therefore a feedback loop in the plant epidermis: cell-cell connections transmit tension across the epidermis, and, in turn, tension is perceived by the cells to alter the strength of those connections. The results presented by Verger et al. suggest that plants use tension to monitor the adhesion in the cell layer that forms an interface with the environment. Other organisms may use similar processes

this theory is supported by the fact that sheets of animal cells use proteins that are involved in both cell-cell adhesion and the detection of tension. The next challenge is to analyse how tension in the epidermis affects developmental processes and how a plant responds to its environment.

Conflict of Interest

SV, YL, AB, OH No competing interests declared

References (67)
67 references, click to expand
  1. The OSU1/QUA2/TSD2-encoded putative methyltransferase is a critical modulator of carbon and nitrogen nutrient balance response in Arabidopsis.
    PLoS One. 2008 Jan 02;3(1):e1387 PMID: 18167546
  2. Pectin: cell biology and prospects for functional analysis.
    Plant Mol Biol. 2001 Sep;47(1-2):9-27 PMID: 11554482
  3. Quantifying forces in cell biology.
    Nat Cell Biol. 2017 Jul;19(7):742-751 PMID: 28628082
  4. Demethylesterification of cell wall pectins in Arabidopsis plays a role in seed germination.
    Plant Physiol. 2013 Jan;161(1):305-16 PMID: 23129203
  5. Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration.
    Cell. 2012 Jan 20;148(1-2):175-88 PMID: 22265410
  6. Progressive transverse microtubule array organization in hormone-induced Arabidopsis hypocotyl cells.
    Plant Cell. 2013 Feb;25(2):662-76 PMID: 23444330
  7. The conflict between cell proliferation and expansion primarily affects stem organogenesis in Arabidopsis.
    Plant Cell Physiol. 2014 Nov;55(11):1994-2007 PMID: 25246492
  8. Investigating piconewton forces in cells by FRET-based molecular force microscopy.
    J Struct Biol. 2017 Jan;197(1):37-42 PMID: 26980477
  9. Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis.
    Cell. 2012 Apr 13;149(2):439-51 PMID: 22500806
  10. Sequential activation of apical and basolateral contractility drives ascidian endoderm invagination.
    Curr Biol. 2010 Sep 14;20(17):1499-510 PMID: 20691592
  11. AtDEK1 is essential for specification of embryonic epidermal cell fate.
    Plant J. 2005 Oct;44(1):114-27 PMID: 16167900
  12. Generation of shape complexity through tissue conflict resolution.
    Elife. 2017 Feb 07;6: PMID: 28166865
  13. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells.
    Elife. 2014 Apr 16;3:e01967 PMID: 24740969
  14. The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl.
    Curr Biol. 2015 Jun 29;25(13):1746-52 PMID: 26073136
  15. Quantifying cell-generated mechanical forces within living embryonic tissues.
    Nat Methods. 2014 Feb;11(2):183-9 PMID: 24317254
  16. Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis.
    Plant Cell. 2003 Jul;15(7):1632-45 PMID: 12837952
  17. The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development.
    Plant J. 2007 May;50(4):735-50 PMID: 17461780
  18. The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues.
    PLoS Comput Biol. 2018 Feb 20;14(2):e1006011 PMID: 29462151
  19. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants.
    Nat Plants. 2016 Jun 20;2:16089 PMID: 27322096
  20. Developing a 'thick skin': a paradoxical role for mechanical tension in maintaining epidermal integrity?
    Development. 2016 Sep 15;143(18):3249-58 PMID: 27624830
  21. Tropomyosin controls sarcomere-like contractions for rigidity sensing and suppressing growth on soft matrices.
    Nat Cell Biol. 2016 Jan;18(1):33-42 PMID: 26619148
  22. A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing.
    Science. 2013 Dec 6;342(6163):1245533 PMID: 24200811
  23. How to let go: pectin and plant cell adhesion.
    Front Plant Sci. 2015 Jul 14;6:523 PMID: 26236321
  24. Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells.
    Nat Cell Biol. 2007 Feb;9(2):171-5 PMID: 17220881
  25. Differential regulation of cellulose orientation at the inner and outer face of epidermal cells in the Arabidopsis hypocotyl.
    Plant Cell. 2011 Jul;23(7):2592-605 PMID: 21742992
  26. QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis.
    Plant Cell. 2002 Oct;14(10):2577-90 PMID: 12368506
  27. Cell division plane orientation based on tensile stress in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2016 Jul 26;113(30):E4294-303 PMID: 27436908
  28. An Image Analysis Pipeline to Quantify Emerging Cracks in Materials or Adhesion Defects in Living Tissues.
    Bio Protoc. 2018 Oct 5;8(19):e3036 PMID: 30406157
  29. A mechanosensitive Ca2+ channel activity is dependent on the developmental regulator DEK1.
    Nat Commun. 2017 Oct 18;8(1):1009 PMID: 29044106
  30. FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images.
    Nat Protoc. 2014 Feb;9(2):457-63 PMID: 24481272
  31. Membrane tension regulates motility by controlling lamellipodium organization.
    Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11429-34 PMID: 21709265
  32. A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells
    Plant Cell. 1998 Nov;10(11):1927-40 PMID: 9811799
  33. Mechanical Shielding of Rapidly Growing Cells Buffers Growth Heterogeneity and Contributes to Organ Shape Reproducibility.
    Curr Biol. 2017 Nov 20;27(22):3468-3479.e4 PMID: 29129534
  34. Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling.
    Curr Biol. 2012 Sep 25;22(18):1732-7 PMID: 22885061
  35. Role of turgor pressure in endocytosis in fission yeast.
    Mol Biol Cell. 2014 Mar;25(5):679-87 PMID: 24403609
  36. The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls.
    J Cell Sci. 2010 Oct 15;123(Pt 20):3490-5 PMID: 20876662
  37. The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells.
    BMC Plant Biol. 2011 Feb 01;11:27 PMID: 21284861
  38. Cellular growth in plants requires regulation of cell wall biochemistry.
    Curr Opin Cell Biol. 2017 Feb;44:28-35 PMID: 28131101
  39. An auxin-mediated shift toward growth isotropy promotes organ formation at the shoot meristem in Arabidopsis.
    Curr Biol. 2014 Oct 6;24(19):2335-42 PMID: 25264254
  40. Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media.
    J Exp Bot. 2000 Sep;51(350):1555-62 PMID: 11006306
  41. MorphoLibJ: integrated library and plugins for mathematical morphology with ImageJ.
    Bioinformatics. 2016 Nov 15;32(22):3532-3534 PMID: 27412086
  42. Developmental patterning by mechanical signals in Arabidopsis.
    Science. 2008 Dec 12;322(5908):1650-5 PMID: 19074340
  43. DRACO-STEM: An Automatic Tool to Generate High-Quality 3D Meshes of Shoot Apical Meristem Tissue at Cell Resolution.
    Front Plant Sci. 2017 Mar 29;8:353 PMID: 28424704
  44. Cellular basis of hypocotyl growth in Arabidopsis thaliana.
    Plant Physiol. 1997 May;114(1):295-305 PMID: 9159952
  45. The mechanics behind cell polarity.
    Trends Cell Biol. 2012 Nov;22(11):584-91 PMID: 22980034
  46. On the role of stress anisotropy in the growth of stems.
    J Exp Bot. 2013 Nov;64(15):4697-707 PMID: 23913952
  47. Tensile Tissue Stress Affects the Orientation of Cortical Microtubules in the Epidermis of Sunflower Hypocotyl.
    J Plant Growth Regul. 2000 Mar;19(1):31-44 PMID: 11010990
  48. Cell adhesion in plants is under the control of putative O-fucosyltransferases.
    Development. 2016 Jul 15;143(14):2536-40 PMID: 27317803
  49. The epidermal-growth-control theory of stem elongation: an old and a new perspective.
    J Plant Physiol. 2007 Nov;164(11):1395-409 PMID: 17905474
  50. Heterogeneity and Robustness in Plant Morphogenesis: From Cells to Organs.
    Annu Rev Plant Biol. 2018 Apr 29;69:469-495 PMID: 29505739
  51. The epidermis both drives and restricts plant shoot growth.
    Nature. 2007 Mar 8;446(7132):199-202 PMID: 17344852
  52. MorphoGraphX: A platform for quantifying morphogenesis in 4D.
    Elife. 2015 May 06;4:05864 PMID: 25946108
  53. A Mechanical Feedback Restricts Sepal Growth and Shape in Arabidopsis.
    Curr Biol. 2016 Apr 12;: PMID: 27151660
  54. Mechanical stress in Arabidopsis leaves orients microtubules in a 'continuous' supracellular pattern.
    BMC Plant Biol. 2013 Oct 18;13:163 PMID: 24138025
  55. Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary.
    Curr Biol. 2009 Dec 1;19(22):1950-5 PMID: 19879142
  56. Time-lapse imaging of developing meristems using confocal laser scanning microscope.
    Methods Mol Biol. 2014;1080:111-9 PMID: 24132423
  57. Stress and strain provide positional and directional cues in development.
    PLoS Comput Biol. 2014 Jan;10(1):e1003410 PMID: 24415926
  58. Microtubules and CESA tracks at the inner epidermal wall align independently of those on the outer wall of light-grown Arabidopsis hypocotyls.
    J Cell Sci. 2011 Apr 1;124(Pt 7):1088-94 PMID: 21363888
  59. New Evidence for the Role of Mechanical Forces in the Shoot Apical Meristem.
    J Plant Growth Regul. 2000 Mar;19(1):7-18 PMID: 11010988
  60. Mechanical feedback as a possible regulator of tissue growth.
    Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3318-23 PMID: 15728365
  61. Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain.
    Plant J. 2007 May;50(4):605-14 PMID: 17425712
  62. Tissue-wide Mechanical Forces Influence the Polarity of Stomatal Stem Cells in Arabidopsis.
    Curr Biol. 2017 Mar 20;27(6):877-883 PMID: 28285992
  63. KymoRod: a method for automated kinematic analysis of rod-shaped plant organs.
    Plant J. 2016 Nov;88(3):468-475 PMID: 27354251
  64. Quantifying hydrostatic pressure in plant cells by using indentation with an atomic force microscope.
    Biophys J. 2015 May 19;108(10):2448-2456 PMID: 25992723
  65. Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements.
    Plant Physiol. 2002 May;129(1):290-9 PMID: 12011359
  66. Altered middle lamella homogalacturonan and disrupted deposition of (1-->5)-alpha-L-arabinan in the pericarp of Cnr, a ripening mutant of tomato.
    Plant Physiol. 2001 May;126(1):210-21 PMID: 11351084
  67. Matching Patterns of Gene Expression to Mechanical Stiffness at Cell Resolution through Quantitative Tandem Epifluorescence and Nanoindentation.
    Plant Physiol. 2014 Jun 12;165(4):1399-1408 PMID: 24924426
Article Info
Journal
eLife
Abbr.
Elife
ISSN
2050-084X
Published
2018-00-23
Epub
2018-00-23
Language
English
Region
England
NLM ID
101579614
PMCID
PMC5963923
Subset
IM
Grants
European Research Council · 615739 · International
European Research Council · ERC-2013-CoG-615739 · International
European Research Council · ERC-2012-StG-307387 · International
Corrections
ErratumIn
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