A fibre-reinforced fluid model of anisotropic plant cell growth

Many growing plant cells undergo rapid axial elongation with negligible radial expansion. Growth is driven by high internal turgor pressure causing viscous stretching of the cell wall, with embedded cellulose microfibrils providing the wall with strongly anisotropic properties. We present a theoretical model of a growing cell, representing the primary cell wall as a thin axisymmetric fibre-reinforced viscous sheet supported between rigid end plates. Asymptotic reduction of the governing equations, under simple sets of assumptions about the fibre and wall properties, yields variants of the traditional Lockhart equation, which relates the axial cell growth rate to the internal pressure. The model provides insights into the geometric and biomechanical parameters underlying bulk quantities such as wall extensibility, and shows how either dynamical changes in wall material properties or passive fibre reorientation may suppress cell elongation.

[1]  Clive Lloyd,et al.  Faculty Opinions recommendation of Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. , 2009 .

[2]  Y. Couder,et al.  Developmental Patterning by Mechanical Signals in Arabidopsis , 2009 .

[3]  U. Kutschera The growing outer epidermal wall: design and physiological role of a composite structure. , 2008, Annals of botany.

[4]  J. Verbelen,et al.  Xyloglucan endotransglucosylase activity loosens a plant cell wall. , 2007, Annals of botany.

[5]  Rishikesh Bhalerao,et al.  Ethylene Upregulates Auxin Biosynthesis in Arabidopsis Seedlings to Enhance Inhibition of Root Cell Elongation[W] , 2007, The Plant Cell Online.

[6]  M. McCann,et al.  Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level , 2007, BMC Plant Biology.

[7]  M. McCann,et al.  Cell elongation in Arabidopsis hypocotyls involves dynamic changes in cell wall thickness. , 2007, Journal of experimental botany.

[8]  P. Schopfer,et al.  Biomechanics of plant growth. , 2006, American journal of botany.

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

[10]  A. Geitmann Plant and fungal cytomechanics: quantifying and modeling cellular architecture 1 , 2006 .

[11]  Gerrit T. S. Beemster,et al.  Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal , 2005, Nature Cell Biology.

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

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

[14]  Laurie G. Smith,et al.  Spatial control of cell expansion by the plant cytoskeleton. , 2005, Annual review of cell and developmental biology.

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

[16]  Ulrich Schurr,et al.  Primary root growth: a biophysical model of auxin-related control. , 2005, Functional plant biology : FPB.

[17]  T. Baskin,et al.  Cell wall extension results in the coordinate separation of parallel microfibrils: evidence from scanning electron microscopy and atomic force microscopy. , 2005, The Plant journal : for cell and molecular biology.

[18]  H. Ockendon,et al.  A continuum model for entangled fibres , 2005, European Journal of Applied Mathematics.

[19]  A. Paredez,et al.  Toward a Systems Approach to Understanding Plant Cell Walls , 2004 .

[20]  L. Dolan,et al.  Cell expansion in roots. , 2004, Current opinion in plant biology.

[21]  J. Verbelen,et al.  Cellulose orientation at the surface of the Arabidopsis seedling. Implications for the biomechanics in plant development. , 2003, Journal of structural biology.

[22]  D. M. Bruce,et al.  Mathematical modelling of the cellular mechanics of plants. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  D. S. Thompson Extensiometric determination of the rheological properties of the epidermis of growing tomato fruit. , 2001, Journal of experimental botany.

[24]  L. Cummings,et al.  Fingering instabilities in driven thin nematic films , 2001 .

[25]  R. Yamamoto,et al.  Measurement of viscoelastic properties of root cell walls affected by low pH in lateral roots of Pisum sativum L. , 2000, Plant and Soil.

[26]  J. Boyer,et al.  Turgor, temperature and the growth of plant cells: using Chara corallina as a model system. , 2000, Journal of experimental botany.

[27]  R. Ogden,et al.  A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models , 2000 .

[28]  D. Tomos The plant cell pressure probe , 2000, Biotechnology Letters.

[29]  J. Boyer,et al.  Separating growth from elastic deformation during cell enlargement , 1999, Plant physiology.

[30]  S. Hiller,et al.  A membrane model for elastic deflection of individual plant cell walls , 1998 .

[31]  D J Cosgrove,et al.  A model of cell wall expansion based on thermodynamics of polymer networks. , 1998, Biophysical journal.

[32]  P. D. Howell,et al.  Models for thin viscous sheets , 1996, European Journal of Applied Mathematics.

[33]  B. W. van de Fliert,et al.  Pressure-driven flow of a thin viscous sheet , 1995, Journal of Fluid Mechanics.

[34]  S. McQueen-Mason,et al.  Expansin Mode of Action on Cell Walls (Analysis of Wall Hydrolysis, Stress Relaxation, and Binding) , 1995, Plant physiology.

[35]  Mark A. J. Chaplain,et al.  The Strain Energy Function of an Ideal Plant Cell Wall , 1993 .

[36]  J. Ortega Augmented growth equation for cell wall expansion. , 1985, Plant physiology.

[37]  M. Jarvis Structure and properties of pectin gels in plant cell walls , 1984 .

[38]  D. B. Sellen,et al.  The Response of Mechanically Anisotropic Cylindrical Cells to Multiaxial Stress , 1983 .

[39]  J. Metraux,et al.  Cell expansion patterns and directionality of wall mechanical properties in nitella. , 1980, Plant physiology.

[40]  J. R. O'callaghan,et al.  Structural mechanics of plant cells. , 1978, Journal of theoretical biology.

[41]  P B Green,et al.  Cell growth pattern and wall microfibrillar arrangement: experiments with nitella. , 1977, Plant physiology.

[42]  G. Batchelor,et al.  The stress generated in a non-dilute suspension of elongated particles by pure straining motion , 1971, Journal of Fluid Mechanics.

[43]  G. Batchelor,et al.  The stress system in a suspension of force-free particles , 1970, Journal of Fluid Mechanics.

[44]  P B Green,et al.  Growth Physics in Nitella: a Method for Continuous in Vivo Analysis of Extensibility Based on a Micro-manometer Technique for Turgor Pressure. , 1968, Plant physiology.

[45]  D. R. Cowdrey,et al.  Elasticity and microfibrillar angle in the wood of Sitka spruce , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[46]  J. Lockhart An analysis of irreversible plant cell elongation. , 1965, Journal of theoretical biology.

[47]  M. Probine Cell Growth and the Structure and Mechanical Properties of the Wall in Internodal Cells of Nitella opaca: III. SPIRAL GROWTH AND CELL WALL STRUCTURE , 1963 .

[48]  M. C. Probine,et al.  Cell Growth and the Structure and Mechanical Properties of the Wall in Internodal Cells of Nitella opaca: II. MECHANICAL PROPERTIES OF THE WALLS , 1962 .

[49]  M. Probine,et al.  Cell Growth and the Structure and Mechanical Properties of the Wall in Internodal Cells of Nitella opacaI. WALL STRUCTURE AND GROWTH , 1961 .

[50]  J. Ericksen Transversely isotropic fluids , 1960 .

[51]  Paul B. Green,et al.  Multinet Growth in the Cell Wall of Nitella , 1960, The Journal of biophysical and biochemical cytology.

[52]  J. Ericksen,et al.  Theory of Anisotropic Fluids , 1960 .

[53]  G. B. Jeffery The motion of ellipsoidal particles immersed in a viscous fluid , 1922 .

[54]  F. T. Trouton,et al.  On the coefficient of viscous traction and its relation to that of viscosity , 1906 .

[55]  Alain Goriely,et al.  Elastic Growth Models , 2008 .

[56]  Panos M. Pardalos,et al.  Mathematical modelling of biosystems , 2008 .

[57]  Charles R Steele,et al.  An anisotropic-viscoplastic model of plant cell morphogenesis by tip growth. , 2006, The International journal of developmental biology.

[58]  Tobias I. Baskin,et al.  On the alignment of cellulose microfibrils by cortical microtubules: A review and a model , 2005, Protoplasma.

[59]  J. Chan,et al.  Microtubules and the shape of plants to come , 2004, Nature Reviews Molecular Cell Biology.

[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]  Stephen C. Fry,et al.  Turgor and Cell Expansion: Beyond the Lockhart Equation , 1992 .

[62]  E. Steudle,et al.  Water Transport across Maize Roots : Simultaneous Measurement of Flows at the Cell and Root Level by Double Pressure Probe Technique. , 1991, Plant physiology.

[63]  Przemyslaw Prusinkiewicz,et al.  The Algorithmic Beauty of Plants , 1990, The Virtual Laboratory.

[64]  David V. Boger,et al.  The flow of fiber suspensions in complex geometries , 1988 .

[65]  D. C. Davis,et al.  Finite Element Analysis of Fluid-Filled Cell Response to External Loading , 1984 .

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

[67]  A. Spencer,et al.  Deformations of fibre-reinforced materials, , 1972 .

[68]  R. Aris Vectors, Tensors and the Basic Equations of Fluid Mechanics , 1962 .

[69]  A. Friedman,et al.  The extensional flow of a thin sheet of incompressible, transversely isotropic fluid , 2008, European Journal of Applied Mathematics.