Advertisement

Tensile Testing of Primary Plant Cells and Tissues

  • Amir J. Bidhendi
  • Anja Geitmann
Chapter

Abstract

The primary cell wall controls plant growth and morphogenesis but also determines the structural resilience of nonwoody plant organs. The predominant mechanical role of the primary cell wall lies in its ability to resist or conform to tensile forces. Assessing the tensile properties of the cell wall, therefore, is fundamental for both biomechanics and mechanobiology. Tensile testing is a classic approach used for the mechanical characterization of materials. Various loading strategies such as monotonic or cyclic loading or creep or relaxation allow for analysis of the material response in terms of elastic, viscoelastic, and failure properties. Here, we discuss tensile testing strategies for plant samples with primary cell walls with the aim to provide a practical guide that highlights challenges and offers solutions for the design, execution, and interpretation of such tests.

Keywords

Mechanical characterization Micromechanics Cell wall mechanics Tension test Uniaxial tensile test Biaxial testing Young’s modulus Cellulose Primary cell wall Anisotropy Inverse finite element analysis Multiscale Arabidopsis 

Notes

Acknowledgements

Research in the Geitmann lab is funded by Discovery and Accelerator Grants from the National Science and Engineering Research Council of Canada and by the Canada Research Chair Program.

References

  1. Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152:787–796CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anssari-Benam A, Legerlotz K, Bader DL, Screen HR (2012) On the specimen length dependency of tensile mechanical properties in soft tissues: gripping effects and the characteristic decay length. J Biomech 45:2481–2482CrossRefPubMedGoogle Scholar
  3. Argatov I, Mishuris G (2015) Contact mechanics of articular cartilage layers. In: Asymptotic models. SpringerGoogle Scholar
  4. Armour WJ, Barton DA, Law AM, Overall RL (2015) Differential growth in periclinal and anticlinal walls during lobe formation in Arabidopsis cotyledon pavement cells. Plant Cell 27:2484–2500CrossRefPubMedPubMedCentralGoogle Scholar
  5. Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222CrossRefPubMedGoogle Scholar
  6. Bernal M, Urban MW, Rosario D, Aquino W, Greenleaf JF (2011) Measurement of biaxial mechanical properties of soft tubes and arteries using piezoelectric elements and sonometry. Phys Med Biol 56:3371CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bidhendi AJ, Geitmann A (2016) Relating the mechanics of the primary plant cell wall to morphogenesis. J Exp Bot 67:449–461CrossRefPubMedGoogle Scholar
  8. Bidhendi AJ, Geitmann A (2018) Finite element modeling of shape changes in plant cells. Plant Physiol 176:41–56CrossRefPubMedGoogle Scholar
  9. Boitier G, Chermant J, Vicens J (2000) Understanding the creep behavior of a 2.5 DC f–SiC composite: II. Experimental specifications and macroscopic mechanical creep responses. Mater Sci Eng, A 289:265–275CrossRefGoogle Scholar
  10. Bolduc J-F, Lewis LJ, Aubin C-É, Geitmann A (2006) Finite-element analysis of geometrical factors in micro-indentation of pollen tubes. Biomech Model Mechanobiol 5:227–236CrossRefPubMedGoogle Scholar
  11. Braybrook SA, Peaucelle A (2013) Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS ONE 8:e57813CrossRefPubMedPubMedCentralGoogle Scholar
  12. Carew E, Patel J, Garg A, Houghtaling P, Blackstone E, Vesely I (2003) Effect of specimen size and aspect ratio on the tensile properties of porcine aortic valve tissues. Ann Biomed Eng 31:526–535CrossRefPubMedGoogle Scholar
  13. Chanliaud E, Burrows KM, Jeronimidis G, Gidley MJ (2002) Mechanical properties of primary plant cell wall analogues. Planta 215:989–996CrossRefPubMedGoogle Scholar
  14. Chebli Y, Kaneda M, Zerzour R, Geitmann A (2012) The cell wall of the Arabidopsis pollen tube—spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160:1940–1955CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cheng S, Clarke EC, Bilston LE (2009) The effects of preconditioning strain on measured tissue properties. J Biomech 42:1360–1362CrossRefPubMedGoogle Scholar
  16. Chimungu JG, Loades KW, Lynch JP (2015) Root anatomical phenes predict root penetration ability and biomechanical properties in maize (Zea Mays). J Exp Bot 66:3151–3162CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cooke JR, De Baerdemaeker JG, Rand RH, Mang HA (1976) A finite element shell analysis of guard cell deformations. Trans ASAE 19:1107–1121CrossRefGoogle Scholar
  18. Cosgrove DJ (1998) Cell wall loosening by expansins. Plant Physiol 118:333–339CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861CrossRefPubMedGoogle Scholar
  20. Derbyshire P, Findlay K, McCann MC, Roberts K (2007) Cell elongation in Arabidopsis hypocotyls involves dynamic changes in cell wall thickness. J Exp Bot 58:2079–2089CrossRefPubMedGoogle Scholar
  21. Durachko DM, Cosgrove DJ (2009) Measuring plant cell wall extension (creep) induced by acidic pH and by alpha-expansin. J Vis Exp JoVEGoogle Scholar
  22. Eder M, Arnould O, Dunlop JW, Hornatowska J, Salmén L (2013) Experimental micromechanical characterisation of wood cell walls. Wood Sci Technol 47:163–182CrossRefGoogle Scholar
  23. Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Fredberg JJ (2001) Scaling the microrheology of living cells. Phys Rev Lett 87:148102CrossRefPubMedGoogle Scholar
  24. Forterre Y, Skotheim JM, Dumais J, Mahadevan L (2005) How the Venus flytrap snaps. Nature 433:421–425CrossRefPubMedGoogle Scholar
  25. Freundthal AM (1968) Statistical approach to brittle fracture. In: Lievowitz H (ed) Fracture: an advanced treatise, vol 2. Academic Press, New York, pp 591–619Google Scholar
  26. Gadalla A, Dehoux T, Audoin B (2014) Transverse mechanical properties of cell walls of single living plant cells probed by laser-generated acoustic waves. Planta 239:1129–1137CrossRefPubMedGoogle Scholar
  27. Gallenmüller F, Feus A, Fiedler K, Speck T (2015) Rose prickles and Asparagus spines–different hook structures as attachment devices in climbing plants. PLoS ONE 10:e0143850CrossRefPubMedPubMedCentralGoogle Scholar
  28. Grédiac M, Toussaint E, Pierron F (2002) Special virtual fields for the direct determination of material parameters with the virtual fields method. 1—Principle and definition. Int J Solids Struct 39:2691–2705CrossRefGoogle Scholar
  29. Green PB (1960) Multinet growth in the cell wall of Nitella. J Cell Biol 7:289–296CrossRefGoogle Scholar
  30. Guilak F, Butler DL, Goldstein SA, Baaijens FP (2014) Biomechanics and mechanobiology in functional tissue engineering. J Biomech 47:1933–1940CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hall SA, Muir Wood D, Ibraim E, Viggiani G (2010) Localised deformation patterning in 2D granular materials revealed by digital image correlation. Granul Matter 12:1–14CrossRefGoogle Scholar
  32. Hannon A, Tiernan P (2008) A review of planar biaxial tensile test systems for sheet metal. J Mater Process Technol 198:1–13CrossRefGoogle Scholar
  33. Hervy M, Santmarti A, Lahtinen P, Tammelin T, Lee K-Y (2017) Sample geometry dependency on the measured tensile properties of cellulose nanopapers. Mater Des 121:421–429CrossRefGoogle Scholar
  34. Hua T, Xie H, Pan B, Qing X, Dai F, Feng X (2007) A new micro-tensile system for measuring the mechanical properties of low-dimensional materials—Fibers and films. Polym Test 26:513–518CrossRefGoogle Scholar
  35. Kafle K, Park YB, Lee CM, Stapleton JJ, Kiemle SN, Cosgrove DJ, Kim SH (2017) Effects of mechanical stretching on average orientation of cellulose and pectin in onion epidermis cell wall: a polarized FT-IR study. Cellulose 1–10Google Scholar
  36. Kalidindi S, Abusafieh A, El-Danaf E (1997) Accurate characterization of machine compliance for simple compression testing. Exp Mech 37:210–215CrossRefGoogle Scholar
  37. Kashfuddoja M, Ramji M (2013) Whole-field strain analysis and damage assessment of adhesively bonded patch repair of CFRP laminates using 3D-DIC and FEA. Compos B Eng 53:46–61CrossRefGoogle Scholar
  38. Keckes J, Burgert I, Frühmann K, Müller M, Kölln K, Hamilton M, Burghammer M, Roth SV, Stanzl-Tschegg S, Fratzl P (2003) Cell-wall recovery after irreversible deformation of wood. Nat Mater 2:810–813CrossRefPubMedGoogle Scholar
  39. Kerstens S, Decraemer WF, Verbelen J-P (2001) Cell walls at the plant surface behave mechanically like fiber-reinforced composite materials. Plant Physiol 127:381–385CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kim J-H, Nizami A, Hwangbo Y, Jang B, Lee H-J, Woo C-S, Hyun S, Kim T-S (2013) Tensile testing of ultra-thin films on water surface. Nat Commun 4Google Scholar
  41. Kim K, Yi H, Zamil MS, Haque MA, Puri VM (2015) Multiscale stress–strain characterization of onion outer epidermal tissue in wet and dry states. Am J Bot 102:12–20CrossRefPubMedGoogle Scholar
  42. Kollmannsberger P, Fabry B (2011) Linear and nonlinear rheology of living cells. Annu Rev Mater Res 41:75–97CrossRefGoogle Scholar
  43. Kuchen EE, Fox S, de Reuille PB, Kennaway R, Bensmihen S, Avondo J, Calder GM, Southam P, Robinson S, Bangham A (2012) Generation of leaf shape through early patterns of growth and tissue polarity. Science 335:1092–1096CrossRefPubMedGoogle Scholar
  44. Lally C, Reid A, Prendergast P (2004) Elastic behavior of porcine coronary artery tissue under uniaxial and equibiaxial tension. Ann Biomed Eng 32:1355–1364CrossRefPubMedGoogle Scholar
  45. Lava P, Cooreman S, Coppieters S, De Strycker M, Debruyne D (2009) Assessment of measuring errors in DIC using deformation fields generated by plastic FEA. Opt Lasers Eng 47:747–753CrossRefGoogle Scholar
  46. Lee JM, Courtman DW, Boughner DR (1984) The glutaraldehyde-stabilized porcine aortic valve xenograft. I. Tensile viscoelastic properties of the fresh leaflet material. J Biomed Mater Res Part A 18:61–77CrossRefGoogle Scholar
  47. Lynch TM, Lintilhac PM (1997) Mechanical signals in plant development: a new method for single cell studies. Dev Biol 181:246–256CrossRefPubMedGoogle Scholar
  48. Machado G, Favier D, Chagnon G (2012) Membrane curvatures and stress-strain full fields of axisymmetric bulge tests from 3D-DIC measurements. Theory and validation on virtual and experimental results. Exp Mech 52:865–880CrossRefGoogle Scholar
  49. Maier-Schneider D, Maibach J, Obermeier E (1995) A new analytical solution for the load-deflection of square membranes. J Microelectromech Syst 4:238–241CrossRefGoogle Scholar
  50. Milani P, Braybrook SA, Boudaoud A (2013) Shrinking the hammer: micromechanical approaches to morphogenesis. J Exp Bot 64:4651–4662CrossRefPubMedGoogle Scholar
  51. Miller KS, Edelstein L, Connizzo BK, Soslowsky LJ (2012) Effect of preconditioning and stress relaxation on local collagen fiber re-alignment: inhomogeneous properties of rat supraspinatus tendon. J Biomech Eng 134:031007CrossRefPubMedGoogle Scholar
  52. Mir M, Ali MN, Sami J, Ansari U (2014) Review of mechanics and applications of auxetic structures. Adv Mate Sci EngCrossRefGoogle Scholar
  53. Mofrad MR (2009) Rheology of the cytoskeleton. Annu Rev Fluid Mech 41:433–453CrossRefGoogle Scholar
  54. Motra H, Hildebrand J, Dimmig-Osburg A (2014) Assessment of strain measurement techniques to characterise mechanical properties of structural steel. Eng Sci Technol Int J 17:260–269CrossRefGoogle Scholar
  55. Neggers J, Hoefnagels J, Hild F, Roux S, Geers M (2014) Direct stress-strain measurements from bulged membranes using topography image correlation. Exp Mech 54:717–727CrossRefGoogle Scholar
  56. Norris A (2006) Extreme values of Poisson’s ratio and other engineering moduli in anisotropic materials. J Mech Mater Struct 1:793–812CrossRefGoogle Scholar
  57. Nouira H, Salgado J, El-Hayek N, Ducourtieux S, Delvallée A, Anwer N (2014) Setup of a high-precision profilometer and comparison of tactile and optical measurements of standards. Meas Sci Technol 25:044016CrossRefGoogle Scholar
  58. Orthner M, Rieth L, Solzbacher F (2010) High speed wafer scale bulge testing for the determination of thin film mechanical properties. Rev Sci Instrum 81:055111CrossRefPubMedPubMedCentralGoogle Scholar
  59. Palin R, Geitmann A (2012) The role of pectin in plant morphogenesis. Biosystems 109:397–402CrossRefPubMedGoogle Scholar
  60. Pan B, Qian K, Xie H, Asundi A (2009) Two-dimensional digital image correlation for in-plane displacement and strain measurement: a review. Meas Sci Technol 20:062001CrossRefGoogle Scholar
  61. Pang C, Lee G-Y, T-i Kim, Kim SM, Kim HN, Ahn S-H, Suh K-Y (2012) A flexible and highly sensitive strain-gauge sensor using reversible interlocking of nanofibres. Nat Mater 11:795–801CrossRefPubMedGoogle Scholar
  62. Peaucelle A, Wightman R, Höfte H (2015) The control of growth symmetry breaking in the Arabidopsis hypocotyl. Curr Biol 25:1746–1752CrossRefPubMedGoogle Scholar
  63. Phyo P, Wang T, Kiemle SN, O’Neill H, Pingali SV, Hong M, Cosgrove DJ (2017) Gradients in wall mechanics and polysaccharides along growing inflorescence stems. Plant Physiol 175:1593–1607CrossRefPubMedPubMedCentralGoogle Scholar
  64. Pieczywek PM, Zdunek A (2014) Finite element modelling of the mechanical behaviour of onion epidermis with incorporation of nonlinear properties of cell walls and real tissue geometry. J Food Eng 123:50–59CrossRefGoogle Scholar
  65. Prasanna V, Prabha T, Tharanathan R (2007) Fruit ripening phenomena–an overview. Crit Rev Food Sci Nutr 47:1–19CrossRefPubMedGoogle Scholar
  66. Promma N, Raka B, Grediac M, Toussaint E, Le Cam J-B, Balandraud X, Hild F (2009) Application of the virtual fields method to mechanical characterization of elastomeric materials. Int J Solids Struct 46:698–715CrossRefGoogle Scholar
  67. Routier-Kierzkowska A-L, Weber A, Kochova P, Felekis D, Nelson BJ, Kuhlemeier C, Smith RS (2012) Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiol 158:1514–1522CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sanders PG, Eastman J, Weertman J (1997) Elastic and tensile behavior of nanocrystalline copper and palladium. Acta Mater 45:4019–4025CrossRefGoogle Scholar
  69. Saxe F, Weichold S, Reinecke A, Lisec J, Döring A, Neumetzler L, Burgert I, Eder M (2016) Age effects on hypocotyl mechanics. PLoS ONE 11:e0167808CrossRefPubMedPubMedCentralGoogle Scholar
  70. Schatzmann L, Brunner P, Stäubli H (1998) Effect of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg Sports Traumatol Arthrosc 6:S56–S61CrossRefPubMedGoogle Scholar
  71. Shah DU, Schubel PJ, Clifford MJ, Licence P (2012) The tensile behavior of off-axis loaded plant fiber composites: An insight on the nonlinear stress–strain response. Polym Compos 33:1494–1504CrossRefGoogle Scholar
  72. Sharpe W, Pulskamp J, Gianola D, Eberl C, Polcawich R, Thompson R (2007) Strain measurements of silicon dioxide microspecimens by digital imaging processing. Exp Mech 47:649–658CrossRefGoogle Scholar
  73. Silva S, Sabino M, Fernandes E, Correlo V, Boesel L, Reis R (2005) Cork: properties, capabilities and applications. Int Mater Rev 50:345–365CrossRefGoogle Scholar
  74. Small MK, Daniels BJ, Clemens BM, Nix WD (1994) The elastic biaxial modulus of Ag–Pd multilayered thin films measured using the bulge test. J Mater Res 9:25–30CrossRefGoogle Scholar
  75. Soons J, Lava P, Debruyne D, Dirckx J (2012) Full-field optical deformation measurement in biomechanics: digital speckle pattern interferometry and 3D digital image correlation applied to bird beaks. J Mech Behav Biomed Mater 14:186–191CrossRefPubMedGoogle Scholar
  76. Spatz H, Kohler L, Niklas K (1999) Mechanical behaviour of plant tissues: composite materials or structures? J Exp Biol 202:3269–3272PubMedGoogle Scholar
  77. Srikar V, Spearing S (2003) A critical review of microscale mechanical testing methods used in the design of microelectromechanical systems. Exp Mech 43:238–247CrossRefGoogle Scholar
  78. Sutton M, Reu PL (eds) (2017) international digital imaging correlation society. In: Proceedings of the first annual conference 2016. Springer International PublishingGoogle Scholar
  79. Ting T (2004) Very large Poisson’s ratio with a bounded transverse strain in anisotropic elastic materials. J Elast 77:163–176CrossRefGoogle Scholar
  80. Ting T, Chen T (2005) Poisson’s ratio for anisotropic elastic materials can have no bounds. Q J Mech Appl Math 58:73–82CrossRefGoogle Scholar
  81. Tsuchiya T, Tabata O, Sakata J, Taga Y (1998) Specimen size effect on tensile strength of surface-micromachined polycrystalline silicon thin films. J Microelectromech Syst 7:106–113CrossRefGoogle Scholar
  82. Turek DE (1993) On the tensile testing of high modulus polymers and the compliance correction. Polym Eng Sci 33:328–333CrossRefGoogle Scholar
  83. Vanstreels E, Alamar M, Verlinden B, Enninghorst A, Loodts J, Tijskens E, Ramon H, Nicolaï B (2005) Micromechanical behaviour of onion epidermal tissue. Postharvest Biol Technol 37:163–173CrossRefGoogle Scholar
  84. Wei C, Lintilhac LS, Lintilhac PM (2006) Loss of stability, pH, and the anisotropic extensibility of Chara cell walls. Planta 223:1058–1067CrossRefPubMedGoogle Scholar
  85. Wei C, Lintilhac PM, Tanguay JJ (2001) An insight into cell elasticity and load-bearing ability. Measurement and theory. Plant Physiol 126:1129–1138CrossRefPubMedPubMedCentralGoogle Scholar
  86. Yamaguchi I (1981) A laser-speckle strain gauge. J Phys E Sci Instrum 14:1270CrossRefGoogle Scholar
  87. Yang L, Ettemeyer A (2003) Strain measurement by three-dimensional electronic speckle pattern interferometry: potentials, limitations, and applications. Opt Eng 42:1257–1266CrossRefGoogle Scholar
  88. Yu Z, Xu H, Chen H, Pei Y, Fang D (2016) characterization method of thick films using the bulge test technique. Exp Mech 56Google Scholar
  89. Zamil M, Geitmann A (2017) The middle lamella—more than a glue. Phys Biol 14:015004CrossRefPubMedGoogle Scholar
  90. Zamil MS, Yi H, Haque M, Puri VM (2013) Characterizing microscale biological samples under tensile loading: Stress–strain behavior of cell wall fragment of onion outer epidermis. Am J Bot 100:1105–1115CrossRefPubMedGoogle Scholar
  91. Zamil MS, Yi H, Puri VM (2017) A multiscale FEA framework for bridging cell-wall to tissue-scale mechanical properties: the contributions of middle lamella interface and cell shape. J Mater Sci 13:7947–7968CrossRefGoogle Scholar
  92. Zemánek M, Burša J, Děták M (2009) Biaxial tension tests with soft tissues of arterial wall. Eng Mech 16:3–11Google Scholar
  93. Zerzour R, Kroeger J, Geitmann A (2009) Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev Biol 334:437–446CrossRefPubMedGoogle Scholar
  94. Zhang T, Vavylonis D, Durachko DM, Cosgrove DJ (2017) Nanoscale movements of cellulose microfibrils in primary cell walls. Nat Plants 3:17056CrossRefPubMedPubMedCentralGoogle Scholar
  95. Zhou P, Goodson KE (2001) Subpixel displacement and deformation gradient measurement using digital image/speckle correlation (DISC). Opt Eng 40:1613–1620CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Département de sciences biologiquesInstitut de recherche en biologie végétale, Université de MontréalMontrealCanada
  2. 2.Department of Plant ScienceMcGill UniversitySte-Anne-de-BellevueCanada

Personalised recommendations