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Title: Regiospecific Cellulose Orientation and Anisotropic Mechanical Property in Plant Cell Walls

Journal Article · · Biomacromolecules

Cellulose microfibrils (CMFs) are a major load-bearing component in plant cell walls. Thus, their structures have been studied extensively with spectroscopic and microscopic characterization methods; but the findings from these two approaches were inconsistent, which hampers mechanistic understanding of cell wall mechanics. Here, we report the regiospecific assembly of CMFs in the periclinal wall of plant epidermal cells. Using sum frequency generation spectroscopic imaging, we found that CMFs are highly aligned in the cell edge region where two cells form a junction, whereas they are mostly isotropic on average throughout the wall thickness in the flat face region of the epidermal cell. This subcellular-level heterogeneity in CMF alignment provided insights into tissue-level anisotropy in tensile modulus of cell wall materials. Furthermore, this finding also has resolved a previous contradiction between the spectroscopic and microscopic imaging studies, which paves a foundation for better understanding of cell wall artichecture, especially structure-geometry relationships.

Research Organization:
Pennsylvania State University, University Park, PA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0001090
OSTI ID:
2349339
Journal Information:
Biomacromolecules, Journal Name: Biomacromolecules Journal Issue: 11 Vol. 24; ISSN 1525-7797
Publisher:
American Chemical SocietyCopyright Statement
Country of Publication:
United States
Language:
English

References (60)

Preparation of Onion Epidermal Cell Walls for Imaging by Atomic Force Microscopy (AFM) journal January 2017
Transforms and Operators for Directional Bioimage Analysis: A Survey book May 2016
High-Resolution Field Emission Scanning Electron Microscopy (FESEM) Imaging of Cellulose Microfibril Organization in Plant Primary Cell Walls journal August 2017
Are microtubules tension sensors? journal May 2019
Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction journal August 2002
Dehydration-induced physical strains of cellulose microfibrils in plant cell walls journal October 2018
Multimodal Broadband Vibrational Sum Frequency Generation (MM-BB-V-SFG) Spectrometer and Microscope journal December 2015
Wall extensibility: its nature, measurement and relationship to plant cell growth journal May 1993
Modeling the nonlinear elastic behavior of plant epidermis journal January 2020
Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls journal May 2006
Preferred crystallographic orientation of cellulose in plant primary cell walls journal September 2020
Heterogeneity in the chemistry, structure and function of plant cell walls journal September 2010
Cryo-electron tomography of the onion cell wall shows bimodally oriented cellulose fibers and reticulated homogalacturonan networks journal June 2022
Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis journal July 2013
Resonant soft X-ray scattering reveals cellulose microfibril spacing in plant primary cell walls journal August 2018
Quantification of crystalline cellulose in lignocellulosic biomass using sum frequency generation (SFG) vibration spectroscopy and comparison with other analytical methods journal July 2012
Sum-Frequency-Generation Vibration Spectroscopy and Density Functional Theory Calculations with Dispersion Corrections (DFT-D2) for Cellulose Iα and Iβ journal May 2013
Nanoscale structure, mechanics and growth of epidermal cell walls journal December 2018
A multiscale FEA framework for bridging cell-wall to tissue-scale mechanical properties: the contributions of middle lamella interface and cell shape journal March 2017
Development of an ABAQUS plugin tool for periodic RVE homogenisation journal May 2018
Nanoscale movements of cellulose microfibrils in primary cell walls journal April 2017
Biomechanical Characterization of Onion Epidermal Cell Walls journal January 2017
Toward a Systems Approach to Understanding Plant Cell Walls journal December 2004
Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy journal January 2016
The Mechanical Properties and Molecular Dynamics of Plant Cell Wall Polysaccharides Studied by Fourier-Transform Infrared Spectroscopy journal September 2000
Onion epidermis as a new model to study the control of growth anisotropy in higher plants journal August 2009
Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy journal August 2020
Probing crystal structure and mesoscale assembly of cellulose microfibrils in plant cell walls, tunicate tests, and bacterial films using vibrational Sum Frequency Generation (SFG) spectroscopy journal January 2014
Re-constructing our models of cellulose and primary cell wall assembly journal December 2014
Experimental and Theoretical Study of Azimuth Angle and Polarization Dependences of Sum-Frequency-Generation Vibrational Spectral Features of Uniaxially Aligned Cellulose Crystals journal August 2017
Moisture uptake in native cellulose – the roles of different hydrogen bonds: a dynamic FT-IR study using Deuterium exchange journal March 2006
Quantifying Hydrostatic Pressure in Plant Cells by Using Indentation with an Atomic Force Microscope journal May 2015
Developmental Patterning by Mechanical Signals in Arabidopsis journal December 2008
Relating the mechanics of the primary plant cell wall to morphogenesis journal December 2015
Vibrational sum-frequency-generation (SFG) spectroscopy study of the structural assembly of cellulose microfibrils in reaction woods journal June 2014
Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis journal August 2004
Intercellular adhesion and cell separation in plants journal July 2003
Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes journal November 2015
Growth of the plant cell wall journal November 2005
Microtubule-Mediated Wall Anisotropy Contributes to Leaf Blade Flattening journal October 2020
Finite element modelling of the mechanical behaviour of onion epidermis with incorporation of nonlinear properties of cell walls and real tissue geometry journal February 2014
Micromechanical behaviour of onion epidermal tissue journal August 2005
Molecular insights into the complex mechanics of plant epidermal cell walls journal May 2021
Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy journal April 2018
Correlation between crystalline cellulose structure and cellulose synthase complex shape: a spectroscopic study with unicellular freshwater alga Micrasterias journal October 2019
Architecture of a catalytically active homotrimeric plant cellulose synthase complex journal July 2020
CSI1, PATROL1, and exocyst complex cooperate in delivery of cellulose synthase complexes to the plasma membrane journal March 2018
Sum frequency generation (SFG) microscopy analysis of cellulose microfibrils in Physcomitrium patens gametophore leaf journal July 2023
The Shape of Native Plant Cellulose Microfibrils journal September 2018
Comparative structure and biomechanics of plant primary and secondary cell walls journal January 2012
Anisotropic Expansion of the Plant cell wall journal November 2005
Numerical Simulation of Vibrational Sum Frequency Generation Intensity for Non-Centrosymmetric Domains Interspersed in an Amorphous Matrix: A Case Study for Cellulose in Plant Cell Wall journal August 2022
How Cell Geometry and Cellular Patterning Influence Tissue Stiffness journal May 2022
The importance of being edgy: cell geometric edges as an emerging polar domain in plant cells journal November 2019
On the Orientation-Induced Crystallization of Polymers journal June 2016
Effects of mechanical stretching on average orientation of cellulose and pectin in onion epidermis cell wall: A polarized FT-IR study journal May 2017
Atomic force microscopy based nanoindentation study of onion abaxial epidermis walls in aqueous environment journal January 2015
Cellulose microfibril orientation in onion (Allium cepa L.) epidermis studied by atomic force microscopy (AFM) and vibrational sum frequency generation (SFG) spectroscopy journal December 2013
Probing cellulose structures with vibrational spectroscopy journal January 2019
Mechanical Stress Acts via Katanin to Amplify Differences in Growth Rate between Adjacent Cells in Arabidopsis journal April 2012