Plasticity, elasticity, and adhesion energy of plant cell walls: nanometrology of lignin loss using atomic force microscopy

Farahi, R. H.; Charrier, Anne M.; Tolbert, Allison K.; Lereu, Aude L.; Ragauskas, Arthur J.; Davison, Brian H.; Passian, Ali

doi:10.1038/s41598-017-00234-4

Title: Plasticity, elasticity, and adhesion energy of plant cell walls: nanometrology of lignin loss using atomic force microscopy

Journal Article · 09 March 2017 · Scientific Reports

DOI: https://doi.org/10.1038/s41598-017-00234-4 · OSTI ID:1346628

Farahi, R. H. ^[1];

^[2]; Tolbert, Allison K. ^[3]; Lereu, Aude L. ^[4]; Ragauskas, Arthur J. ^[5]; Davison, Brian H. ^[5]; Passian, Ali ^[6]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Quantum Information Science, Computational Sciences and Engineering Division. BioEnergy Science Center (BESC). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemical and Biomolecular Engineering
Aix Marseille Univ., Marseille (France). Interdisciplinary Center of Nanoscience at Marseille (CINaM)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC). Biosciences Division; Georgia Inst. of Technology, Atlanta, GA (United States). School of Chemistry and Biochemistry
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Quantum Information Science, Computational Sciences and Engineering Division; Aix Marseille Univ., Marseille (France). Interdisciplinary Center of Nanoscience at Marseille (CINaM)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemical and Biomolecular Engineering
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Quantum Information Science, Computational Sciences and Engineering Division. BioEnergy Science Center (BESC). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemical and Biomolecular Engineering. Dept. of Physics

The complex organic polymer, lignin, abundant in plants, prevents the efficient extraction of sugars from the cell walls that is required for large scale biofuel production. Because lignin removal is crucial in overcoming this challenge, the question of how the nanoscale properties of the plant cell ultrastructure correlate with delignification processes is important. Here, we report how distinct molecular domains can be identified and how physical quantities of adhesion energy, elasticity, and plasticity undergo changes, and whether such quantitative observations can be used to characterize delignification. By chemically processing biomass, and employing nanometrology, the various stages of lignin removal are shown to be distinguished through the observed morphochemical and nanomechanical variations. Such spatially resolved correlations between chemistry and nanomechanics during deconstruction not only provide a better understanding of the cell wall architecture but also is vital for devising optimum chemical treatments.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Contributing Organization:: Univ. of Tennessee, Knoxville, TN (United States); Aix Marseille Univ., Marseille (France); Georgia Inst. of Technology, Atlanta, GA (United States)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1346628

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Vol. 7; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Mapping nano-scale mechanical heterogeneity of primary plant cell walls Yakubov, Gleb E.; Bonilla, Mauricio R.; Chen, Huaying Journal of Experimental Botany, Vol. 67, Issue 9 https://doi.org/10.1093/jxb/erw117	journal	March 2016
Atomic Force Microscopy Stiffness Tomography on Living Arabidopsis thaliana Cells Reveals the Mechanical Properties of Surface and Deep Cell-Wall Layers during Growth Radotić, Ksenija; Roduit, Charles; Simonović, Jasna Biophysical Journal, Vol. 103, Issue 3 https://doi.org/10.1016/j.bpj.2012.06.046	journal	August 2012
Scanning below the cell surface Sahin, Ozgur Nature Nanotechnology, Vol. 3, Issue 8 https://doi.org/10.1038/nnano.2008.222	journal	August 2008
Lignin content in natural Populus variants affects sugar release Studer, M. H.; DeMartini, J. D.; Davis, M. F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305 https://doi.org/10.1073/pnas.1009252108	journal	March 2011
The Role of Mechanical Forces in Plant Morphogenesis Mirabet, Vincent; Das, Pradeep; Boudaoud, Arezki Annual Review of Plant Biology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev-arplant-042110-103852	journal	June 2011
Multivariate statistical analysis of X-ray data from cellulose: A new method to determine degree of crystallinity and predict hydrolysis rates Bansal, Prabuddha; Hall, Mélanie; Realff, Matthew J. Bioresource Technology, Vol. 101, Issue 12 https://doi.org/10.1016/j.biortech.2010.01.068	journal	June 2010
Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques Fromm, Jörg; Rockel, Beate; Lautner, Silke Journal of Structural Biology, Vol. 143, Issue 1 https://doi.org/10.1016/s1047-8477(03)00119-9	journal	July 2003
Infrared Studies of “Hard” and “Soft” Woods Owen, N. L.; Thomas, D. W. Applied Spectroscopy, Vol. 43, Issue 3 https://doi.org/10.1366/0003702894202760	journal	March 1989
Rapid determination of lignocellulose by diffuse reflectance Fourier transform infrared spectrometry Schultz, Tor P.; Templeton, M. Curry.; McGinnis, Gary D. Analytical Chemistry, Vol. 57, Issue 14 https://doi.org/10.1021/ac00291a027	journal	December 1985
Imaging nanoparticles in cells by nanomechanical holography Tetard, Laurene; Passian, Ali; Venmar, Katherine T. Nature Nanotechnology, Vol. 3, Issue 8 https://doi.org/10.1038/nnano.2008.162	journal	June 2008
Mapping nano-scale mechanical heterogeneity of primary plant cell walls Yakubov, Gleb E.; Bonilla, Mauricio R.; Chen, Huaying Journal of Experimental Botany, Vol. 67, Issue 9 https://doi.org/10.1093/jxb/erw117	journal	March 2016
In-situ Raman microprobe studies of plant cell walls: Macromolecular organization and compositional variability in the secondary wall of Picea mariana (Mill.) B.S.P. Agarwal, U. P.; Atalla, R. H. Planta, Vol. 169, Issue 3 https://doi.org/10.1007/bf00392127	journal	November 1986
Opto-nanomechanical spectroscopic material characterization Tetard, L.; Passian, A.; Farahi, R. H. Nature Nanotechnology, Vol. 10, Issue 10 https://doi.org/10.1038/nnano.2015.168	journal	August 2015
How Does Plant Cell Wall Nanoscale Architecture Correlate with Enzymatic Digestibility? Ding, S. -Y.; Liu, Y. -S.; Zeng, Y. Science, Vol. 338, Issue 6110 https://doi.org/10.1126/science.1227491	journal	November 2012
Solubility of Structurally Complicated Materials: I. Wood Horvath, Ari L. Journal of Physical and Chemical Reference Data, Vol. 35, Issue 1 https://doi.org/10.1063/1.2035708	journal	March 2006
Expanding the Library of Secondary Ions That Distinguish Lignin and Polysaccharides in Time-of-Flight Secondary Ion Mass Spectrometry Analysis of Wood Goacher, Robyn E.; Jeremic, Dragica; Master, Emma R. Analytical Chemistry, Vol. 83, Issue 3 https://doi.org/10.1021/ac1023028	journal	February 2011
Plants control the properties and actuation of their organs through the orientation of cellulose fibrils in their cell walls Burgert, I.; Fratzl, P. Integrative and Comparative Biology, Vol. 49, Issue 1 https://doi.org/10.1093/icb/icp026	journal	May 2009
Nanoindentation of wood cell walls: Continuous stiffness and hardness measurements Tze, W. T. Y.; Wang, S.; Rials, T. G. Composites Part A: Applied Science and Manufacturing, Vol. 38, Issue 3 https://doi.org/10.1016/j.compositesa.2006.06.018	journal	March 2007
Cellulose microfibril angle in the cell wall of wood fibres Barnett, J. R.; Bonham, Victoria A. Biological Reviews, Vol. 79, Issue 2 https://doi.org/10.1017/S1464793103006377	journal	January 1999
Plants control the properties and actuation of their organs through the orientation of cellulose fibrils in their cell walls Burgert, I.; Fratzl, P. Integrative and Comparative Biology, Vol. 49, Issue 1 https://doi.org/10.1093/icb/icp026	journal	May 2009
Lignin content in natural Populus variants affects sugar release Studer, Michael Hans-Peter; DeMartini, J. D.; Davis, M. F. National Academy of Sciences https://doi.org/10.24451/arbor.10127	text	January 2011
The Role of Mechanical Forces in Plant Morphogenesis Mirabet, Vincent; Das, Pradeep; Boudaoud, Arezki Annual Review of Plant Biology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev-arplant-042110-103852	journal	June 2011
Detection, Localization, and Conformational Analysis of Single Polysaccharide Molecules on Live Bacteria Francius, Grégory; Lebeer, Sarah; Alsteens, David ACS Nano, Vol. 2, Issue 9 https://doi.org/10.1021/nn800341b	journal	August 2008
Correlating confocal microscopy and atomic force indentation reveals metastatic cancer cells stiffen during invasion into collagen I matrices Staunton, Jack R.; Doss, Bryant L.; Lindsay, Stuart Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19686	journal	January 2016
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Atomic Force Microscopy Stiffness Tomography on Living Arabidopsis thaliana Cells Reveals the Mechanical Properties of Surface and Deep Cell-Wall Layers during Growth Radotić, Ksenija; Roduit, Charles; Simonović, Jasna Biophysical Society https://doi.org/10.5167/uzh-79172	text	January 2012
Effect of crystallinity and degree of polymerization of cellulose on enzymatic saccharification Puri, Vinod P. Biotechnology and Bioengineering, Vol. 26, Issue 10 https://doi.org/10.1002/bit.260261010	journal	October 1984
On the generality of the relationship among contact stiffness, contact area, and elastic modulus during indentation Pharr, G. M.; Oliver, W. C.; Brotzen, F. R. Journal of Materials Research, Vol. 7, Issue 3 https://doi.org/10.1557/jmr.1992.0613	journal	March 1992
Micromechanical understanding of the cell-wall structure Salmén, Lennart Comptes Rendus Biologies, Vol. 327, Issue 9-10 https://doi.org/10.1016/j.crvi.2004.03.010	journal	September 2004
Band assignments in the raman spectra of celluloses Wiley, James H.; Atalla, Rajai H. Carbohydrate Research, Vol. 160, p. 113-129 https://doi.org/10.1016/0008-6215(87)80306-3	journal	February 1987
Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes Cosgrove, Daniel J. Journal of Experimental Botany, Vol. 67, Issue 2 https://doi.org/10.1093/jxb/erv511	journal	November 2015
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
Biomass pretreatment: Fundamentals toward application Agbor, Valery B.; Cicek, Nazim; Sparling, Richard Biotechnology Advances, Vol. 29, Issue 6 https://doi.org/10.1016/j.biotechadv.2011.05.005	journal	November 2011
Fast nanomechanical spectroscopy of soft matter Herruzo, Elena T.; Perrino, Alma P.; Garcia, Ricardo Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4126	journal	January 2014
Progress in Green Polymer Composites from Lignin for Multifunctional Applications: A Review Thakur, Vijay Kumar; Thakur, Manju Kumari; Raghavan, Prasanth ACS Sustainable Chemistry & Engineering, Vol. 2, Issue 5 https://doi.org/10.1021/sc500087z	journal	April 2014
Secondary Cell Wall Deposition in Developing Secondary Xylem of Poplar Kaneda, Minako; Rensing, Kim; Samuels, Lacey Journal of Integrative Plant Biology, Vol. 52, Issue 2 https://doi.org/10.1111/j.1744-7909.2010.00925.x	journal	February 2010
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
Heterogeneity in the chemistry, structure and function of plant cell walls Burton, Rachel A.; Gidley, Michael J.; Fincher, Geoffrey B. Nature Chemical Biology, Vol. 6, Issue 10 https://doi.org/10.1038/nchembio.439	journal	September 2010
The emergence of multifrequency force microscopy Garcia, Ricardo; Herruzo, Elena T. Nature Nanotechnology, Vol. 7, Issue 4 https://doi.org/10.1038/nnano.2012.38	journal	April 2012
Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques Fromm, Jörg; Rockel, Beate; Lautner, Silke Journal of Structural Biology, Vol. 143, Issue 1 https://doi.org/10.1016/s1047-8477(03)00119-9	journal	July 2003
Cellulose crystallinity and ordering of hemicelluloses in pine and birch pulps as revealed by solid-state NMR spectroscopic methods Liitiä, Tiina; Maunu, Sirkka Liisa; Hortling, Bo Cellulose, Vol. 10, Issue 4, p. 307-316 https://doi.org/10.1023/a:1027302526861	journal	December 2003
In-situ Raman microprobe studies of plant cell walls: Macromolecular organization and compositional variability in the secondary wall of Picea mariana (Mill.) B.S.P. Agarwal, U. P.; Atalla, R. H. Planta, Vol. 169, Issue 3 https://doi.org/10.1007/BF00392127	journal	November 1986
Imaging nanoparticles in cells by nanomechanical holography Tetard, Laurene; Passian, Ali; Venmar, Katherine T. Nature Nanotechnology, Vol. 3, Issue 8 https://doi.org/10.1038/nnano.2008.162	journal	June 2008
Images from below the surface Garcia, Ricardo Nature Nanotechnology, Vol. 5, Issue 2 https://doi.org/10.1038/nnano.2010.14	journal	February 2010
Beating beats mixing in heterodyne detection schemes Verbiest, G. J.; Rost, M. J. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7444	journal	March 2015
Cellulose microfibril angle in the cell wall of wood fibres Barnett, J. R.; Bonham, Victoria A. Biological Reviews, Vol. 79, Issue 2 https://doi.org/10.1017/s1464793103006377	journal	January 1999
Cellulose microfibril angle in the cell wall of wood fibres Barnett, J. R.; Bonham, Victoria A. Biological Reviews, Vol. 79, Issue 2 https://doi.org/10.1017/s1464793103006377	journal	January 1999
Comparative structure and biomechanics of plant primary and secondary cell walls Cosgrove, Daniel J.; Jarvis, Michael C. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00204	journal	January 2012
Beating beats mixing in heterodyne detection schemes Verbiest, G. J.; Rost, M. J. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7444	journal	March 2015
Cellulose crystallinity and ordering of hemicelluloses in pine and birch pulps as revealed by solid-state NMR spectroscopic methods Liitiä, Tiina; Maunu, Sirkka Liisa; Hortling, Bo Cellulose, Vol. 10, Issue 4, p. 307-316 https://doi.org/10.1023/A:1027302526861	journal	December 2003
An atomic force microscope tip designed to measure time-varying nanomechanical forces Sahin, Ozgur; Magonov, Sergei; Su, Chanmin Nature Nanotechnology, Vol. 2, Issue 8 https://doi.org/10.1038/nnano.2007.226	journal	July 2007
Molecular Origin of Strength and Stiffness in Bamboo Fibrils Youssefian, Sina; Rahbar, Nima Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep11116	journal	June 2015
Atomic Force Microscopy Stiffness Tomography on Living Arabidopsis thaliana Cells Reveals the Mechanical Properties of Surface and Deep Cell-Wall Layers during Growth Radotić, Ksenija; Roduit, Charles; Simonović, Jasna Biophysical Journal, Vol. 103, Issue 3 https://doi.org/10.1016/j.bpj.2012.06.046	journal	August 2012
Identifying the Characteristic Secondary Ions of Lignin Polymer Using ToF−SIMS Saito, Kaori; Kato, Toshiyuki; Tsuji, Yukiko Biomacromolecules, Vol. 6, Issue 2 https://doi.org/10.1021/bm049521v	journal	March 2005
Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques Fromm, Jörg; Rockel, Beate; Lautner, Silke Journal of Structural Biology, Vol. 143, Issue 1 https://doi.org/10.1016/S1047-8477(03)00119-9	journal	July 2003
On the generality of the relationship among contact stiffness, contact area, and elastic modulus during indentation Pharr, G. M.; Oliver, W. C.; Brotzen, F. R. Journal of Materials Research, Vol. 7, Issue 3 https://doi.org/10.1557/JMR.1992.0613	journal	March 1992
Secondary Cell Wall Deposition in Developing Secondary Xylem of Poplar Kaneda, Minako; Rensing, Kim; Samuels, Lacey Journal of Integrative Plant Biology, Vol. 52, Issue 2 https://doi.org/10.1111/j.1744-7909.2010.00925.x	journal	February 2010

Cited By (9)

Branched Pectic Galactan in Phloem-Sieve-Element Cell Walls: Implications for Cell Mechanics Torode, Thomas A.; O’Neill, Rachel; Marcus, Susan E. Plant Physiology, Vol. 176, Issue 2 https://doi.org/10.1104/pp.17.01568	journal	November 2017
Exploring the Treasure of Plant Molecules With Integrated Biorefineries Torres, Andres F.; Xu, Xuan; Nikiforidis, Constantinos V. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00478	journal	April 2019
Nanoscale hygromechanical behavior of lignin Hess, Kristen M.; Killgore, Jason P.; Srubar, Wil V. Cellulose, Vol. 25, Issue 11 https://doi.org/10.1007/s10570-018-2045-3	journal	September 2018
Action of lytic polysaccharide monooxygenase on plant tissue is governed by cellular type Chabbert, Brigitte; Habrant, Anouck; Herbaut, Mickaël Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-17938-2	journal	December 2017
A High-Q AFM Sensor Using a Balanced Trolling Quartz Tuning Fork in the Liquid Zhang, Yingxu; Li, Yingzi; Song, Zihang Sensors, Vol. 18, Issue 5 https://doi.org/10.3390/s18051628	journal	May 2018
Investigations on the elasticity of functional gold nanoparticles using single-molecule force spectroscopy Sun, Li; Riedel, René; Stanciu, Stefan G. Journal of Materials Chemistry B, Vol. 6, Issue 19 https://doi.org/10.1039/c7tb03309e	journal	January 2018
Action of lytic polysaccharide monooxygenase on plant tissue is governed by cellular type Chabbert, Brigitte; Habrant, Anouck; Herbaut, Mickaël Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-17938-2	journal	December 2017
Nanomechanics and Raman Spectroscopy of in Situ Native Carbohydrate Storage Granules for Enhancing Starch Quality and Lignocellulosic Biomass Production Farahi, Rubye H.; Lereu, Aude L.; Charrier, Anne M. ACS Omega, Vol. 5, Issue 6 https://doi.org/10.1021/acsomega.9b02849	journal	February 2020
A High-Q AFM Sensor Using a Balanced Trolling Quartz Tuning Fork in the Liquid Zhang, Yingxu; Li, Yingzi; Song, Zihang Sensors, Vol. 18, Issue 5 https://doi.org/10.3390/s18051628	journal	May 2018

Similar Records

Breaking the Biological barriers to Cellulosic Ethanol: A Joint Research Agenda

Book · 2006 · OSTI ID:978245

Mansfield, Betty Kay; Alton, Anita Jean; Andrews, Shirley H; +6 more

Visualizing Lignin Coalescence and Migration Through Maize Cell Walls Following Thermochemical Pretreatment

Journal Article · 2008 · Biotechnology and Bioengineering · OSTI ID:947416

Donohoe, B S; Decker, S R; Tucker, M P; +2 more

Visualizing plant cell wall changes proves the superiority of hydrochloric acid over sulfuric acid catalyzed γ-valerolactone pretreatment

Journal Article · 2020 · Chemical Engineering Journal · OSTI ID:1755189

Zhang, Jian; Shen, Wei; Collings, Cynthia; +5 more

Related Subjects

09 BIOMASS FUELS
77 NANOSCIENCE AND NANOTECHNOLOGY
applications of atomic force microscopy (AFM)
nanoscale materials

Title: Plasticity, elasticity, and adhesion energy of plant cell walls: nanometrology of lignin loss using atomic force microscopy

Citation Formats

References (57)

Cited By (9)

Similar Records

Related Subjects