Exploring the micromechanical design of plant cell walls.

Plants are hierarchically organized in a way that their macroscopic properties emerge from their micro- and nanostructural level. Hence, micromechanical investigations, which focus on the mechanical design of plant cell walls, are well suited for elucidating the details of the relationship between plant form and function. However, due to the complex nature of primary and secondary cell walls, micromechanical tests on the entire structure cannot provide exact values for polymer properties but must be targeted at the general mechanisms of cell wall deformation and polymer interaction. The success of micromechanical examinations depends on well-considered specimen selection and/or sample pretreatment as well as appropriate experimental setups. Making use of structural differences by taking advantage of the natural variability in plant tissue and cell structure, adaptation strategies can be analyzed at the micro- and nanoscale. Targeted genetic and enzymatic treatments can be utilized to specifically modify individual polymers without degrading the structural integrity of the cell wall. The mechanical properties of such artificial systems reveal the functional roles of individual polymers for a better understanding of the mechanical interactions within the cell wall assembly. In terms of testing methodology, in situ methods that combine micromechanical testing with structural and chemical analyses are particularly well suited for the study of the basic structure-property relationships in plant design. The micromechanical approaches reviewed here are not exhaustive, but they do provide a reasonably comprehensive overview of the methodology with which the general mechanisms underlying the functionality of plant micro- and nanostructure can be explored without destroying the entire cell wall.

[1]  D J Cosgrove,et al.  Wall extensibility: its nature, measurement and relationship to plant cell growth. , 1993, The New phytologist.

[2]  C. Neinhuis,et al.  Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. , 2005, Journal of experimental botany.

[3]  Gidley,et al.  In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites , 1999, The Plant Journal.

[4]  W. Gindl,et al.  The significance of the elastic modulus of wood cell walls obtained from nanoindentation measurements , 2004 .

[5]  A. Geitmann,et al.  Cytomechanical properties of papaver pollen tubes are altered after self-incompatibility challenge. , 2004, Biophysical journal.

[6]  S. Shaler,et al.  The tensile testing of individual wood fibers using environmental scanning electron microscopy and video image analysis , 1995 .

[7]  C. Riekel,et al.  Characterisation of the microstructure and deformation of high modulus cellulose fibres , 2003 .

[8]  A. Geitmann,et al.  Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense , 2005, Planta.

[9]  Peter Fratzl,et al.  Cellulose and collagen: from fibres to tissues , 2003 .

[10]  Thomas Speck,et al.  Mechanical, chemical and X-ray analysis of wood in the two tropical lianas Bauhinia guianensis and Condylocarpon guianense: variations during ontogeny , 2003, Planta.

[11]  R. Wimmer,et al.  Longitudinal hardness and Young's modulus of spruce tracheid secondary walls using nanoindentation technique , 1997, Wood Science and Technology.

[12]  D. Goring,et al.  ultrastructural arrangement of the wood cell wall , 1975 .

[13]  Maureen C. McCann,et al.  Complexity in the spatial localization and length distribution of plant cell‐wall matrix polysaccharides , 1992 .

[14]  Leslie H. Groom,et al.  Mechanical properties of individual southern pine fibers. Part III. Global relationships between fiber properties and fiber location within an individual tree. , 2002 .

[15]  P. Schopfer,et al.  In-vivo measurement of cell-wall extensibility in maize coleoptiles: Effects of auxin and abscisic acid , 1986, Planta.

[16]  S. Stanzl-Tschegg,et al.  Microtensile Testing of Wood Fibers Combined with Video Extensometry for Efficient Strain Detection , 2003 .

[17]  D. Fengel,et al.  Wood: Chemistry, Ultrastructure, Reactions , 1983 .

[18]  Leslie H. Groom,et al.  A technique to measure strain distributions in single wood pulp fibers , 1996 .

[19]  P. Fratzl,et al.  Determination of spiral angles of elementary fibrils in the wood cell wall: comparison of small-angle X-ray scattering and wide-angle X-ray diffraction. , 1998 .

[20]  Jozsef Bodig,et al.  Mechanics of Wood and Wood Composites , 1982 .

[21]  Takahisa Hayashi,et al.  Xyloglucans in the Primary Cell Wall , 1989 .

[22]  S. Fry,et al.  A simple apparatus for measuring long-term extension of plant cell walls subjected to tensile stress , 2005 .

[23]  A. Geitmann,et al.  More Than a Leak Sealant. The Mechanical Properties of Callose in Pollen Tubes1 , 2005, Plant Physiology.

[24]  Keiko Sugimoto-Shirasu,et al.  Tensile Properties of Arabidopsis Cell Walls Depend on Both a Xyloglucan Cross-Linked Microfibrillar Network and Rhamnogalacturonan II-Borate Complexes1 , 2003, Plant Physiology.

[25]  David Stuart Thompson,et al.  How do cell walls regulate plant growth? , 2005, Journal of experimental botany.

[26]  D. Cosgrove Wall structure and wall loosening. A look backwards and forwards. , 2001, Plant physiology.

[27]  M. Ha,et al.  Molecular Rigidity in Dry and Hydrated Onion Cell Walls , 1997, Plant physiology.

[28]  P. Fratzl,et al.  Mechanical properties of spruce wood cell walls by nanoindentation , 2004 .

[29]  R. Cleland Cell Wall Extension , 1971 .

[30]  I. Burgert,et al.  Mechanical model for the deformation of the wood cell wall , 2004, International Journal of Materials Research.

[31]  Hanns-Christof Spatz,et al.  Micromechanics of plant tissues beyond the linear-elastic range , 2002, Planta.

[32]  D. Cosgrove Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls , 2004, Planta.

[33]  I. Burgert,et al.  Adaptive Growth of Gymnosperm Branches-Ultrastructural and Micromechanical Examinations , 2004, Journal of Plant Growth Regulation.

[34]  Manuel Elices,et al.  Structural biological materials : design and structure-property relationships , 2000 .

[35]  J. Verbelen,et al.  Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls. , 2006, Journal of experimental botany.

[36]  L. Salmén,et al.  Interaction between hemicelluloses, lignin and cellulose : Structure-property relationships , 1998 .

[37]  L. Salmén,et al.  Pore and matrix distribution in the fiber wall revealed by atomic force microscopy and image analysis. , 2005, Biomacromolecules.

[38]  Jozef Keckes,et al.  Cell-wall recovery after irreversible deformation of wood , 2003, Nature materials.

[39]  I. Burgert,et al.  Mechanics of the Wood Cell Wall , 2006 .

[40]  D. Cosgrove Growth of the plant cell wall , 2005, Nature Reviews Molecular Cell Biology.

[41]  B. Meyer,et al.  Simulations of the static and dynamic molecular conformations of xyloglucan. The role of the fucosylated sidechain in surface-specific sidechain folding. , 1991, The Plant journal : for cell and molecular biology.

[42]  W. Diepenbrock,et al.  Determination of Mechanical Strength Properties of Hemp Fibers Using Near-Infrared Fourier Transform Raman Microspectroscopy , 2006, Applied spectroscopy.

[43]  S. Eichhorn,et al.  Elastic modulus and stress-transfer properties of tunicate cellulose whiskers. , 2005, Biomacromolecules.

[44]  D. Fengel Ultrastructural behaviour of cell wall polysaccharides. , 1970 .

[45]  S. Stanzl-Tschegg,et al.  Variation of cellulose microfibril angles in softwoods and hardwoods-a possible strategy of mechanical optimization. , 1999, Journal of structural biology.

[46]  W F Decraemer,et al.  Cell walls at the plant surface behave mechanically like fiber-reinforced composite materials. , 2001, Plant physiology.

[47]  A. Darke,et al.  In vitro assembly of cellulose/xyloglucan networks: ultrastructural and molecular aspects , 1995 .

[48]  G. Pezzotti Raman piezo-spectroscopic analysis of natural and synthetic biomaterials , 2005, Analytical and bioanalytical chemistry.

[49]  L. Staehelin,et al.  Xyloglucan sidechains modulate binding to cellulose during in vitro binding assays as predicted by conformational dynamics simulations. , 1997, The Plant journal : for cell and molecular biology.

[50]  H. Zhu,et al.  A mechanics model for the compression of plant and vegetative tissues. , 2003, Journal of theoretical biology.

[51]  J. Vincent,et al.  The Mechanical Properties of Xylem Tissue from Tobacco Plants (Nicotiana tabacum‘Samsun’)☆ , 1998 .

[52]  James W. Evans,et al.  Influence of Cambial Age and Growth Conditions on Microfibril Angle in Young Norway Spruce (Picea abies [L.] Karst.) , 1998 .

[53]  M. Burghammer,et al.  Mechanical properties of cellulose fibres and wood. Orientational aspects in situ investigated with synchrotron radiation. , 2005, Journal of synchrotron radiation.

[54]  Mitchell,et al.  Roles of cellulose and xyloglucan in determining the mechanical properties of primary plant cell walls , 1999, Plant physiology.

[55]  P. K. Rastogi,et al.  Micromechanics of wood subjected to axial tension , 1995, Wood Science and Technology.

[56]  Antony Bacic,et al.  8 – Structure and Function of Plant Cell Walls , 1988 .

[57]  K Niklas,et al.  The role of the epidermis as a stiffening agent in Tulipa (Liliaceae) stems. , 1997, American journal of botany.

[58]  D. M. Bruce,et al.  RELATIONSHIPS BETWEEN PRIMARY PLANT CELL WALL ARCHITECTURE AND MECHANICAL PROPERTIES FOR ONION BULB SCALE EPIDERMAL CELLS , 2004 .

[59]  J. Vincent,et al.  Survival of the cheapest , 2002 .

[60]  N. Carpita,et al.  Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. , 1993, The Plant journal : for cell and molecular biology.

[61]  C. Chapple,et al.  Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. , 1997, The Plant journal : for cell and molecular biology.

[62]  P. Albersheim,et al.  Structure and function of the primary cell walls of plants. , 1984, Annual review of biochemistry.

[63]  S. Fry Polysaccharide-Modifying Enzymes in the Plant Cell Wall , 1995 .

[64]  N. Carpita,et al.  The Galactose Residues of Xyloglucan Are Essential to Maintain Mechanical Strength of the Primary Cell Walls in Arabidopsis during Growth1 , 2004, Plant Physiology.

[65]  F. El-Hosseiny,et al.  mechanical properties of single wood pulp fibres. VI. Fibril angle and the shape of the stress-strain curve , 1983 .

[66]  A. Reiterer,et al.  Cellulose microfibril angles in a spruce branch and mechanical implications , 2001 .

[67]  T. Schindler The new view of the primary cell wall , 1998 .

[68]  L. Taiz,et al.  Plant Cell Expansion: Regulation of Cell Wall Mechanical Properties , 1984 .

[69]  J. Aizenberg,et al.  Skeleton of Euplectella sp.: Structural Hierarchy from the Nanoscale to the Macroscale , 2005, Science.

[70]  C. Dunand,et al.  The MUR3 Gene of Arabidopsis Encodes a Xyloglucan Galactosyltransferase That Is Evolutionarily Related to Animal Exostosins Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009837. , 2003, The Plant Cell Online.

[71]  C. Neinhuis,et al.  Two-dimensional tension tests in plant biomechanics--sweet cherry fruit skin as a model system. , 2004, Plant biology.

[72]  A MICRO‐PENETRATION TECHNIQUE FOR MECHANICAL TESTING OF PLANT CELL WALLS , 1996 .

[73]  Christopher J. Hogan,et al.  Temperature and water content effects on the viscoelastic behavior of Tilia americana (Tiliaceae) sapwood , 2004, Trees.

[74]  Ingo Burgert,et al.  Molecular changes during tensile deformation of single wood fibers followed by Raman microscopy. , 2006, Biomacromolecules.

[75]  G. Grüll,et al.  In-situ Fracturing of Wood in the Scanning Electron Microscope , 1996 .

[76]  S. Stanzl-Tschegg,et al.  Detection of the Fracture Path under Tensile Loads through in situ Tests in an ESEM Chamber , 2003 .

[77]  L. Salmén,et al.  Interactions between wood polymers studied by dynamic FT-IR spectroscopy , 2001 .

[78]  J. Brändström MICRO- AND ULTRASTRUCTURAL ASPECTS OF NORWAY SPRUCE TRACHEIDS: A REVIEW , 2001 .

[79]  S. Eichhorn,et al.  Crystalline and amorphous deformation of process-controlled cellulose-II fibres , 2005 .

[80]  M. McCann,et al.  Macromolecular biophysics of the plant cell wall: Concepts and methodology , 2000 .

[81]  K. Keegstra,et al.  The Structure of Plant Cell Walls: III. A Model of the Walls of Suspension-cultured Sycamore Cells Based on the Interconnections of the Macromolecular Components. , 1973, Plant physiology.

[82]  Stephen M. Shaler,et al.  Mechanical Properties Of Individual Southern Pine Fibers. Part II. Comparison Of Earlywood And Latewood Fibers With Respect To Tree Height And Juvenility , 2002 .

[83]  T. Baskin Anisotropic expansion of the plant cell wall. , 2005, Annual review of cell and developmental biology.

[84]  A. Reiterer,et al.  Experimental evidence for a mechanical function of the cellulose microfibril angle in wood cell walls , 1999 .

[85]  T. Speck,et al.  Micromechanics and anatomical changes during early ontogeny of two lianescent Aristolochia species , 2000, Planta.

[86]  George Jeronimidis,et al.  Mechanical properties of primary plant cell wall analogues , 2002, Planta.

[87]  J. Vincken,et al.  Two General Branching Patterns of Xyloglucan, XXXG and XXGG , 1997, Plant physiology.

[88]  P. Schopfer,et al.  Viscoelastic versus plastic cell wall extensibility in growing seedling organs: a contribution to avoid some misconceptions , 1997 .

[89]  Lennart Salmén,et al.  Micromechanical understanding of the cell-wall structure. , 2004, Comptes rendus biologies.

[90]  R. D. Preston,et al.  The physical biology of plant cell walls , 1975 .

[91]  N. Raikhel,et al.  The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[92]  H. Mang,et al.  Rate-independent mechanical behavior of biaxially stressed wood: Experimental observations and constitutive modeling as an orthotropic two-surface elasto-plastic material , 2005 .

[93]  J. Sugiyama,et al.  Studies of the structural change during deformation in Cryptomeria japonica by time-resolved synchrotron small-angle X-ray scattering. , 2005, Journal of structural biology.

[94]  P. Schopfer,et al.  Effect of auxin and abscisic acid on cell wall extensibility in maize coleoptiles , 1986, Planta.

[95]  Himadri S. Gupta,et al.  On the role of interface polymers for the mechanics of natural polymeric composites , 2004 .

[96]  S. Shaler,et al.  Mechanical properties of individual southern pine fibers. Part I. Determination and variability of stress-strain curves with respect to tree height and juvenility , 2002 .

[97]  George Jeronimidis,et al.  Chapter 1 - Structure-Property Relationships in Biological Materials , 2000 .

[98]  K J Niklas,et al.  Mechanical behaviour of plant tissues: composite materials or structures? , 1999, The Journal of experimental biology.

[99]  Thomas Speck,et al.  Biomimetics and technical textiles: solving engineering problems with the help of nature's wisdom. , 2006, American journal of botany.

[100]  D. Page,et al.  Behaviour of Single Wood Fibres under Axial Tensile Strain , 1971, Nature.