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The mechanical properties of plant cell walls soft material at the subcellular scale: the implications of water and of the intercellular boundaries

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Abstract

Subcellular mechanical characterization of the cell wall can provide important insights into the cell wall’s functional organization, especially if the characterization is not confounded by extracellular factors and intercellular boundaries. However, due to the technical challenges associated with the microscale mechanical characterization of soft biological materials, subcellular investigations of the plant cell wall under tensile loading have yet to be properly performed. This study reports the mechanical characterization of primary onion epidermal cell wall profiles using a novel cryosection-based sample preparation method and a microelectromechanical system-based tensile testing protocol. At the subcellular scale, the cell wall showed biphasic behavior similar to tissue samples. However, instead of a transition zone between the linear elastic or viscoelastic and linear plastic zones, the subcellular-scale samples showed a plateau-like trend with a sharp drop in the modulus value. The critical ranges of stress (20–40 MPa) and strain (5–12 %) of the plateau zone were identified. A strain energy of 1.3 MJ m−3 was calculated at the midpoint of the critical stress–strain range; this value was in accordance with the previously estimated hydrogen bond energy of the cell wall. Subcellular-scale samples showed very large lateral/axial deformations (0.8 ± 0.13) at fracturing. In addition, investigating the cell wall’s mechanical properties at three different water states showed that water is critical for the flow-like behavior of cell wall matrix polymers. These results at subcellular scale provide new insights into biological materials that possess a structural hierarchy at different length scales; which cannot be obtained from tissue-scale experiments.

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References

  1. Keegstra K (2010) Plant cell walls. Plant Physiol 154:483–486. doi:10.1104/pp.110.161240

  2. Park YB, Cosgrove DJ (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158:1933–1943

    Article  Google Scholar 

  3. Harris PJ, Stone BA (2008) Chemistry and molecular organization of plant cell walls. Biomass Recalcitrance. Blackwell Publishing Ltd., pp 61–93

  4. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900. doi:10.1016/j.carres.2009.05.021

    Article  Google Scholar 

  5. Burton RA, Gidley MJ, Fincher GB (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 6:724–732

    Article  Google Scholar 

  6. Albersheim P, Darvill A, Roberts K (2010) Plant cell walls: from chemistry to biology. Garland Science, Garland.

  7. McCann M, Rose J (2010) Blueprints for building plant cell walls. Plant Physiol 153:365. doi:10.1104/pp.110.900324

    Article  Google Scholar 

  8. Hepworth DG, Bruce DM (2004) Relationships between primary plant cell wall architecture and mechanical properties for onion bulb scale epidermal cells. J Texture Stud 35:586–602

    Article  Google Scholar 

  9. Park YB, Cosgrove DJ (2012) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of arabidopsis. Plant Physiol 158:465–475. doi:10.1104/pp.111.189779

    Article  Google Scholar 

  10. Cosgrove D, Jarvis M (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3:6

    Article  Google Scholar 

  11. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev cell Biol 6:850–861

    Article  Google Scholar 

  12. Burgert I, Keplinger T (2013) Plant micro- and nanomechanics: experimental techniques for plant cell-wall analysis. J Exp Bot 64:4635–4649. doi:10.1093/jxb/ert255

    Article  Google Scholar 

  13. Liepman AH, Wightman R, Geshi N et al (2010) Arabidopsis—a powerful model system for plant cell wall research. Plant J 61:1107–1121

    Article  Google Scholar 

  14. Somerville C, Bauer S, Brininstool G et al (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211

    Article  Google Scholar 

  15. McCann MC, Carpita NC (2008) Designing the deconstruction of plant cell walls. Curr Opin Plant Biol 11:314–320. doi:10.1016/j.pbi.2008.04.001

    Article  Google Scholar 

  16. Ryden P, Sugimoto-Shirasu K, Smith AC et al (2003) Tensile properties of arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132:1033–1040

    Article  Google Scholar 

  17. Suslov D, Verbelen J-P, Vissenberg K (2009) Onion epidermis as a new model to study the control of growth anisotropy in higher plants. J Exp Bot 60:4175–4187

    Article  Google Scholar 

  18. Keckes J, Burgert I, Fruhmann K et al (2003) Cell-wall recovery after irreversible deformation of wood. Nat Mater 2:810–813

    Article  Google Scholar 

  19. Zabler S, Paris O, Burgert I, Fratzl P (2010) Moisture changes in the plant cell wall force cellulose crystallites to deform. J Struct Biol 171:133–141. doi:10.1016/j.jsb.2010.04.013

    Article  Google Scholar 

  20. Zdunek A, Umeda M (2005) Influence of cell size and cell wall volume fraction on failure properties of potato and carrot tissue. J Texture Stud 36:25–43

    Article  Google Scholar 

  21. 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. doi:10.1016/j.jfoodeng.2013.09.012

    Article  Google Scholar 

  22. Konstankiewicz K, Pawlak K, Zdunek A (2001) Influence of structural parameters of potato tuber cells on their mechanical properties. Int Agrophys 15:243–246

    Google Scholar 

  23. Waldron KW, Brett CT (2007) The role of polymer cross-linking in intercellular adhesion. In: Roberts JA, Gonzalez-Carranza Z (eds) Plant cell separation and adhesion. Blackwell Publishing Ltd, Ames, pp 183–204

  24. Faisal T, Rey A, Pasini D (2013) A multiscale mechanical model for plant tissue stiffness. Polymers (Basel) 5:730–750. doi:10.3390/polym5020730

    Article  Google Scholar 

  25. Höfte H, Peaucelle A, Braybrook S (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3:6

    Google Scholar 

  26. Dick-Pérez M, Zhang Y, Hayes J et al (2011) Structure and Interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50:989–1000. doi:10.1021/bi101795q

    Article  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. Jarvis MC, Briggs SPH, Knox JP (2003) Intercellular adhesion and cell separation in plants. Plant Cell Environ 26:977–989

    Article  Google Scholar 

  29. Gibson LJ (2012) The hierarchical structure and mechanics of plant materials. J R Soc Interface 9:2749–2766. doi:10.1098/rsif.2012.0341

    Article  Google Scholar 

  30. Métraux J-P, Taiz L (1978) Transverse viscoelastic extension in Nitella I. Relationship to growth rate. Plant Physiol 61:135–138

    Article  Google Scholar 

  31. Toole GGA, Gunning PA, Parker MML et al (2001) Fracture mechanics of the cell wall of Chara corallina. Planta 212:606–611. doi:10.1007/s004250000425

    Article  Google Scholar 

  32. Sedighi-Gilani M, Sunderland H, Navi P (2005) Microfibril angle non-uniformities within normal and compression wood tracheids. Wood Sci Technol 39:419–430. doi:10.1007/s00226-005-0022-0

    Article  Google Scholar 

  33. Geitmann A (2006) Experimental approaches used to quantify physical parameters at cellular and subcellular levels. Am J Bot 93:1380–1390. doi:10.3732/ajb.93.10.1380

    Article  Google Scholar 

  34. Peaucelle A (2014) AFM-based Mapping of the elastic properties of cell walls: at tissue, cellular, and subcellular resolutions. e51317. doi:10.3791/51317

  35. Peaucelle A, Braybrook S, Le Guillou L et al (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in arabidopsis. Curr Biol 21:1720–1726

    Article  Google Scholar 

  36. Kasas S, Longo G, Dietler G (2013) Mechanical properties of biological specimens explored by atomic force microscopy. J Phys D Appl Phys 46:133001

    Article  Google Scholar 

  37. Kasas S, Gmur T, Dietler G (2008) The world of nano-biomechanics. 221–243. doi:10.1016/B978-044452777-6.50014-0

  38. Notbohm J, Poon B, Ravichandran G (2012) Analysis of nanoindentation of soft materials with an atomic force microscope. J Mater Res 27:229–237

    Article  Google Scholar 

  39. Zamil MS, Yi H, Haque A, Virendra MP (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

    Article  Google Scholar 

  40. Zamil MS, Yi H, Puri VM (2014) Mechanical characterization of outer epidermal middle lamella of onion under tensile loading. Am J Bot 101:778–787. doi:10.3732/ajb.1300416

    Article  Google Scholar 

  41. Kha H, Tuble SC, Kalyanasundaram S, Williamson RE (2010) WallGen, software to construct layered cellulose-hemicellulose networks and predict their small deformation mechanics. Plant Physiol 152:774–786

    Article  Google Scholar 

  42. Yi H, Puri VM (2012) Architecture-based multiscale computational modeling of plant cell wall mechanics to examine the hydrogen-bonding hypothesis of cell wall network structure model. Plant Physiol 160:1281–1292. doi:10.1104/pp.112.201228

    Article  Google Scholar 

  43. Blewett J, Burrows K, Thomas C (2000) A micromanipulation method to measure the mechanical properties of single tomato suspension cells. Biotechnol Lett 22:1877–1883

    Article  Google Scholar 

  44. Saito T, Soga K, Hoson T, Terashima I (2006) The bulk elastic modulus and the reversible properties of cell walls in developing quercus leaves. Plant Cell Physiol 47:715–725

    Article  Google Scholar 

  45. Evered C, Majevadia B, Thompson DS (2007) Cell wall water content has a direct effect on extensibility in growing hypocotyls of sunflower (Helianthus annuus L.). J Exp Bot 58:3361–3371

    Article  Google Scholar 

  46. Moore JP, Farrant JM, Driouich A (2008) A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal Behav 3:102–104

  47. Hansen SL, Ray PM, Karlsson AO et al (2011) Mechanical properties of plant cell walls probed by relaxation spectra. Plant Physiol 155:246–258. doi:10.1104/pp.110.166629

    Article  Google Scholar 

  48. Ulvskov P, Wium H, Bruce D et al (2005) Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta 220:609–620. doi:10.1007/s00425-004-1373-8

    Article  Google Scholar 

  49. Dick-Perez M, Wang T, Salazar A et al (2012) Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly 13C-labeled Arabidopsis primary cell walls. Magn Reson Chem 50:539–550. doi:10.1002/mrc.3836

    Article  Google Scholar 

  50. Wilson RH, Smith AC, Kačuráková M et al (2000) The mechanical properties and molecular dynamics of plant cell wall polysaccharides studied by fourier-transform infrared spectroscopy. Plant Physiol 124:397–406. doi:10.1104/pp.124.1.397

    Article  Google Scholar 

  51. White PB, Wang T, Park YB et al (2014) Water-polysaccharide interactions in the primary cell wall of arabidopsis thaliana from polarization transfer solid-state NMR. J Am Chem Soc 136:10399–10409. doi:10.1021/ja504108h

    Article  Google Scholar 

  52. Zhang T, Mahgsoudy-Louyeh S, Tittmann B, Cosgrove D (2014) Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis. Cellulose 21:853–862. doi:10.1007/s10570-013-9996-1

    Article  Google Scholar 

  53. Kafle K, Xi X, Lee CM et al (2014) Cellulose microfibril orientation in onion (Allium cepa L.) epidermis studied by atomic force microscopy (AFM) and vibrational sum frequency generation (SFG) spectroscopy. Cellulose 21:1075–1086. doi:10.1007/s10570-013-0121-2

    Article  Google Scholar 

  54. Engqvist C, Forsberg S, Norgren M et al (2007) Interactions between single latex particles and silica surfaces studied with AFM. Colloids Surf A 302:197–203. doi:10.1016/j.colsurfa.2007.02.032

    Article  Google Scholar 

  55. Tas N, Sonnenberg T, Jansen H, Legtenberg R, Elwenspoek M (1996) Stiction in surface micromachining. J Micromech Microeng 6:385

    Article  Google Scholar 

  56. Evert RF (2006) Esau’s pant anatomy, 3rd edn. Wiley, New York, p 601

  57. Hayles MF, Stokes DJ, Phifer D, Findlay KC (2007) A technique for improved focused ion beam milling of cryo-prepared life science specimens. J Microsc 226:263–269. doi:10.1111/j.1365-2818.2007.01775.x

    Article  Google Scholar 

  58. Vanstreels E, Alamar MC, Verlinden BE et al (2005) Micromechanical behaviour of onion epidermal tissue. Postharvest Biol Technol 37:163–173

    Article  Google Scholar 

  59. Sokolov I, Dokukin ME, Guz NV (2013) Method for quantitative measurements of the elastic modulus of biological cells in AFM indentation experiments. Methods 60:202–213. doi:10.1016/j.ymeth.2013.03.037

    Article  Google Scholar 

  60. Zdunek A, Pieczywek PM (2013) Study on model development of plant tissue using the finite element method. Inside Food Symposium, Leuven, Belgium, pp 9–12

  61. Lee T, Lakes RS (1997) Anisotropic polyurethane foam with Poisson’sratio greater than 1. J Mater Sci 32:2397–2401. doi:10.1023/A:1018557107786

    Article  Google Scholar 

  62. Peel LD (2007) Exploration of high and negative Poisson’s ratio elastomer-matrix laminates. Phys status solidi 244:988–1003. doi:10.1002/pssb.200572717

    Article  Google Scholar 

  63. Greaves GN, Greer AL, Lakes RS, Rouxel T (2011) Poisson’s ratio and modern materials. Nat Mater 10:823–837

    Article  Google Scholar 

  64. Köhler L, Spatz H-C (2002) Micromechanics of plant tissues beyond the linear-elastic range. Planta 215:33–40. doi:10.1007/s00425-001-0718-9

    Article  Google Scholar 

  65. Spatz H, Kohler L, Niklas KJ (1999) Mechanical behaviour of plant tissues: composite materials or structures? J Exp Biol 202:3269–3272

    Google Scholar 

  66. Dintwa E, Jancsók P, Mebatsion HK et al (2011) A finite element model for mechanical deformation of single tomato suspension cells. J Food Eng 103:265–272. doi:10.1016/j.jfoodeng.2010.10.023

    Article  Google Scholar 

  67. Donaldson L (2007) Cellulose microfibril aggregates and their size variation with cell wall type. Wood Sci Technol 41:443–460. doi:10.1007/s00226-006-0121-6

    Article  Google Scholar 

  68. Thompson DS (2005) How do cell walls regulate plant growth? J Exp Bot 56:2275–2285

    Article  Google Scholar 

  69. Timoshenko S, Goodier JN (1984) Theory of elasticity, 3rd edn. Singapore, McGraw-Hill, Auckland

    Google Scholar 

  70. Cosgrove D (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Bi 13:171–201

    Article  Google Scholar 

  71. Alamar MC, Vanstreels E, Oey ML et al (2008) Micromechanical behaviour of apple tissue in tensile and compression tests: storage conditions and cultivar effect. J Food Eng 86:324–333

    Article  Google Scholar 

  72. Oey ML, Vanstreels E, De Baerdemaeker J et al (2007) Effect of turgor on micromechanical and structural properties of apple tissue: a quantitative analysis. Postharvest Biol Technol 44:240–247. doi:10.1016/j.postharvbio.2006.12.015

    Article  Google Scholar 

  73. Decraemer WF, Maes MA, Vanhuyse VJ (1980) An elastic stress-strain relation for soft biological tissues based on a structural model. J Biomech 13:463–468. doi:10.1016/0021-9290(80)90338-3

    Article  Google Scholar 

  74. Davies LM, Harris PJ (2003) Atomic force microscopy of microfibrils in primary cell walls. Planta 217:283–289. doi:10.1007/s00425-003-0979-6

    Google Scholar 

  75. Keegstra K, Albersheim P, Darvill A et al (2010) Plant Cell Walls. Plant Physiol 154:483–486. doi:10.1104/pp.110.161240

    Article  Google Scholar 

  76. Hayashi T, Marsden MP, Delmer DP (1987) Pea xyloglucan and cellulose: V. Xyloglucan-cellulose interactions in vitro and in vivo. Plant Physiol 83:384–389

    Article  Google Scholar 

  77. McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. 96:323–334

    Google Scholar 

  78. Ha MA, Apperley DC, Jarvis MC (1997) Molecular rigidity in dry and hydrated onion cell walls. Plant Physiol 115:593–598

    Google Scholar 

  79. Vicré M, Sherwin HW, Driouich A et al (1999) Cell wall characteristics and structure of hydrated and dry leaves of the resurrection plant craterostigma wilmsii, a microscopical study. J Plant Physiol 155:719–726. doi:10.1016/S0176-1617(99)80088-1

    Article  Google Scholar 

  80. Kačuráková M, Smith AC, Gidley MJ, Wilson RH (2002) Molecular interactions in bacterial cellulose composites studied by 1D FT-IR and dynamic 2D FT-IR spectroscopy. Carbohydr Res 337:1145–1153. doi:10.1016/S0008-6215(02)00102-7

    Article  Google Scholar 

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Acknowledgements

This study was funded by the Center for Lignocellulose Structure and Formation, an Energy Frontier Research Center funded by the U. S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC0001090.

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  1. M. Shafayet Zamil

    Present address: IRBV, University de Montreal, Montreal, QC, H1X 2B2, Canada

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  1. Department of Agricultural and Biological Engineering, Pennsylvania State University, University Park, PA, 16802, USA

    M. Shafayet Zamil, Hojae Yi & Virendra M. Puri

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Zamil, M.S., Yi, H. & Puri, V.M. The mechanical properties of plant cell walls soft material at the subcellular scale: the implications of water and of the intercellular boundaries. J Mater Sci 50, 6608–6623 (2015). https://doi.org/10.1007/s10853-015-9204-9

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