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.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152:787–796
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 45:2481–2482
Argatov I, Mishuris G (2015) Contact mechanics of articular cartilage layers. In: Asymptotic models. Springer
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 27:2484–2500
Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222
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 56:3371
Bidhendi AJ, Geitmann A (2016) Relating the mechanics of the primary plant cell wall to morphogenesis. J Exp Bot 67:449–461
Bidhendi AJ, Geitmann A (2018) Finite element modeling of shape changes in plant cells. Plant Physiol 176:41–56
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 289:265–275
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 5:227–236
Braybrook SA, Peaucelle A (2013) Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS ONE 8:e57813
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 31:526–535
Chanliaud E, Burrows KM, Jeronimidis G, Gidley MJ (2002) Mechanical properties of primary plant cell wall analogues. Planta 215:989–996
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 160:1940–1955
Cheng S, Clarke EC, Bilston LE (2009) The effects of preconditioning strain on measured tissue properties. J Biomech 42:1360–1362
Chimungu JG, Loades KW, Lynch JP (2015) Root anatomical phenes predict root penetration ability and biomechanical properties in maize (Zea Mays). J Exp Bot 66:3151–3162
Cooke JR, De Baerdemaeker JG, Rand RH, Mang HA (1976) A finite element shell analysis of guard cell deformations. Trans ASAE 19:1107–1121
Cosgrove DJ (1998) Cell wall loosening by expansins. Plant Physiol 118:333–339
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
Derbyshire P, Findlay K, McCann MC, Roberts K (2007) Cell elongation in Arabidopsis hypocotyls involves dynamic changes in cell wall thickness. J Exp Bot 58:2079–2089
Durachko DM, Cosgrove DJ (2009) Measuring plant cell wall extension (creep) induced by acidic pH and by alpha-expansin. J Vis Exp JoVE
Eder M, Arnould O, Dunlop JW, Hornatowska J, Salmén L (2013) Experimental micromechanical characterisation of wood cell walls. Wood Sci Technol 47:163–182
Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Fredberg JJ (2001) Scaling the microrheology of living cells. Phys Rev Lett 87:148102
Forterre Y, Skotheim JM, Dumais J, Mahadevan L (2005) How the Venus flytrap snaps. Nature 433:421–425
Freundthal AM (1968) Statistical approach to brittle fracture. In: Lievowitz H (ed) Fracture: an advanced treatise, vol 2. Academic Press, New York, pp 591–619
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 239:1129–1137
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:e0143850
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 39:2691–2705
Green PB (1960) Multinet growth in the cell wall of Nitella. J Cell Biol 7:289–296
Guilak F, Butler DL, Goldstein SA, Baaijens FP (2014) Biomechanics and mechanobiology in functional tissue engineering. J Biomech 47:1933–1940
Hall SA, Muir Wood D, Ibraim E, Viggiani G (2010) Localised deformation patterning in 2D granular materials revealed by digital image correlation. Granul Matter 12:1–14
Hannon A, Tiernan P (2008) A review of planar biaxial tensile test systems for sheet metal. J Mater Process Technol 198:1–13
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 121:421–429
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 26:513–518
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 1–10
Kalidindi S, Abusafieh A, El-Danaf E (1997) Accurate characterization of machine compliance for simple compression testing. Exp Mech 37:210–215
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 53:46–61
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 2:810–813
Kerstens S, Decraemer WF, Verbelen J-P (2001) Cell walls at the plant surface behave mechanically like fiber-reinforced composite materials. Plant Physiol 127:381–385
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 4
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 102:12–20
Kollmannsberger P, Fabry B (2011) Linear and nonlinear rheology of living cells. Annu Rev Mater Res 41:75–97
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 335:1092–1096
Lally C, Reid A, Prendergast P (2004) Elastic behavior of porcine coronary artery tissue under uniaxial and equibiaxial tension. Ann Biomed Eng 32:1355–1364
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 47:747–753
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 18:61–77
Lynch TM, Lintilhac PM (1997) Mechanical signals in plant development: a new method for single cell studies. Dev Biol 181:246–256
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 52:865–880
Maier-Schneider D, Maibach J, Obermeier E (1995) A new analytical solution for the load-deflection of square membranes. J Microelectromech Syst 4:238–241
Milani P, Braybrook SA, Boudaoud A (2013) Shrinking the hammer: micromechanical approaches to morphogenesis. J Exp Bot 64:4651–4662
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 134:031007
Mir M, Ali MN, Sami J, Ansari U (2014) Review of mechanics and applications of auxetic structures. Adv Mate Sci Eng
Mofrad MR (2009) Rheology of the cytoskeleton. Annu Rev Fluid Mech 41:433–453
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 17:260–269
Neggers J, Hoefnagels J, Hild F, Roux S, Geers M (2014) Direct stress-strain measurements from bulged membranes using topography image correlation. Exp Mech 54:717–727
Norris A (2006) Extreme values of Poisson’s ratio and other engineering moduli in anisotropic materials. J Mech Mater Struct 1:793–812
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 25:044016
Orthner M, Rieth L, Solzbacher F (2010) High speed wafer scale bulge testing for the determination of thin film mechanical properties. Rev Sci Instrum 81:055111
Palin R, Geitmann A (2012) The role of pectin in plant morphogenesis. Biosystems 109:397–402
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 20:062001
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 11:795–801
Peaucelle A, Wightman R, Höfte H (2015) The control of growth symmetry breaking in the Arabidopsis hypocotyl. Curr Biol 25:1746–1752
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 175:1593–1607
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 123:50–59
Prasanna V, Prabha T, Tharanathan R (2007) Fruit ripening phenomena–an overview. Crit Rev Food Sci Nutr 47:1–19
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 46:698–715
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 158:1514–1522
Sanders PG, Eastman J, Weertman J (1997) Elastic and tensile behavior of nanocrystalline copper and palladium. Acta Mater 45:4019–4025
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:e0167808
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–S61
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 33:1494–1504
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 47:649–658
Silva S, Sabino M, Fernandes E, Correlo V, Boesel L, Reis R (2005) Cork: properties, capabilities and applications. Int Mater Rev 50:345–365
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 9:25–30
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 14:186–191
Spatz H, Kohler L, Niklas K (1999) Mechanical behaviour of plant tissues: composite materials or structures? J Exp Biol 202:3269–3272
Srikar V, Spearing S (2003) A critical review of microscale mechanical testing methods used in the design of microelectromechanical systems. Exp Mech 43:238–247
Sutton M, Reu PL (eds) (2017) international digital imaging correlation society. In: Proceedings of the first annual conference 2016. Springer International Publishing
Ting T (2004) Very large Poisson’s ratio with a bounded transverse strain in anisotropic elastic materials. J Elast 77:163–176
Ting T, Chen T (2005) Poisson’s ratio for anisotropic elastic materials can have no bounds. Q J Mech Appl Math 58:73–82
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 7:106–113
Turek DE (1993) On the tensile testing of high modulus polymers and the compliance correction. Polym Eng Sci 33:328–333
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 37:163–173
Wei C, Lintilhac LS, Lintilhac PM (2006) Loss of stability, pH, and the anisotropic extensibility of Chara cell walls. Planta 223:1058–1067
Wei C, Lintilhac PM, Tanguay JJ (2001) An insight into cell elasticity and load-bearing ability. Measurement and theory. Plant Physiol 126:1129–1138
Yamaguchi I (1981) A laser-speckle strain gauge. J Phys E Sci Instrum 14:1270
Yang L, Ettemeyer A (2003) Strain measurement by three-dimensional electronic speckle pattern interferometry: potentials, limitations, and applications. Opt Eng 42:1257–1266
Yu Z, Xu H, Chen H, Pei Y, Fang D (2016) characterization method of thick films using the bulge test technique. Exp Mech 56
Zamil M, Geitmann A (2017) The middle lamella—more than a glue. Phys Biol 14:015004
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 100:1105–1115
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 13:7947–7968
Zemánek M, Burša J, Děták M (2009) Biaxial tension tests with soft tissues of arterial wall. Eng Mech 16:3–11
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 334:437–446
Zhang T, Vavylonis D, Durachko DM, Cosgrove DJ (2017) Nanoscale movements of cellulose microfibrils in primary cell walls. Nat Plants 3:17056
Zhou P, Goodson KE (2001) Subpixel displacement and deformation gradient measurement using digital image/speckle correlation (DISC). Opt Eng 40:1613–1620
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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Bidhendi, A.J., Geitmann, A. (2018). Tensile Testing of Primary Plant Cells and Tissues. In: Geitmann, A., Gril, J. (eds) Plant Biomechanics. Springer, Cham. https://doi.org/10.1007/978-3-319-79099-2_15
Download citation
DOI: https://doi.org/10.1007/978-3-319-79099-2_15
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-79098-5
Online ISBN: 978-3-319-79099-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)