Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy

Huang, Shixin; Makarem, Mohamadamin; Kiemle, Sarah N.; Hamedi, Hossein; Sau, Moujhuri; Cosgrove, Daniel J.; Kim, Seong H.

doi:10.1021/acs.jpcb.8b01537

Title: Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy

Abstract

Sum frequency generation (SFG) vibrational spectroscopy can selectively detect and analyze noncentrosymmetric components interspersed in amorphous matrices; this principle has been used for studies of nanoscale structure and mesoscale assembly of cellulose in plant cell walls. However, the spectral information averaged over a large area or volume cannot provide regiospecific or tissue-specific information of different cells in plants. Here, we demonstrate spatially resolved SFG analysis and imaging by combining a broad-band SFG spectroscopy system with an optical microscope. The system was designed to irradiate both narrow-band 800 nm and broad-band tunable IR beams through a single reflective objective lens, but from opposite sides of the surface normal direction of the sample. The developed technique was used to reveal inhomogeneous distributions of cellulose microfibrils within single cell walls, such as cotton fibers and onion epidermis as well as among different tissues in Arabidopsis inflorescence stems and bamboo culms. SFG microscopy can be used for vibrational spectroscopic imaging of other biological systems in complement to conventional Fourier transform infrared spectroscopy and confocal Raman microscopy.

Authors:

Huang, Shixin ^[1]; Makarem, Mohamadamin ^[1]; Kiemle, Sarah N. ^[2]; Hamedi, Hossein ^[1]; Sau, Moujhuri ^[1]; Cosgrove, Daniel J. ^[2];

^[1]

Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemical Engineering
Pennsylvania State Univ., University Park, PA (United States). Dept. of Biology

Publication Date:: 2018-04-26

Research Org.:: Energy Frontier Research Centers (EFRC), Washington D.C. (United States). Center for Lignocellulose Structure and Formation (CLSF)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1470553

Grant/Contract Number:: SC0001090

Resource Type:: Accepted Manuscript

Journal Name:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

Additional Journal Information:: Journal Volume: 122; Journal Issue: 19; Related Information: CLSF partners with Pennsylvania State University (lead); North Carolina State University; University of Rhode Island; Virginia Tech University; Journal ID: ISSN 1520-6106

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; biofuels (including algae and biomass); bio-inspired; membrane; carbon sequestration; materials and chemistry by design; synthesis (self-assembly)

Citation Formats


                    Huang, Shixin, Makarem, Mohamadamin, Kiemle, Sarah N., Hamedi, Hossein, Sau, Moujhuri, Cosgrove, Daniel J., and Kim, Seong H. Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy.  United States: N. p., 2018. 
        Web.  doi:10.1021/acs.jpcb.8b01537.

Copy to clipboard


                    Huang, Shixin, Makarem, Mohamadamin, Kiemle, Sarah N., Hamedi, Hossein, Sau, Moujhuri, Cosgrove, Daniel J., & Kim, Seong H. Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy.  United States.  doi:https://doi.org/10.1021/acs.jpcb.8b01537

Copy to clipboard


                    Huang, Shixin, Makarem, Mohamadamin, Kiemle, Sarah N., Hamedi, Hossein, Sau, Moujhuri, Cosgrove, Daniel J., and Kim, Seong H. Thu .  
        "Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy".  United States.  doi:https://doi.org/10.1021/acs.jpcb.8b01537.  https://www.osti.gov/servlets/purl/1470553.

Copy to clipboard


                    
@article{osti_1470553,

  title        = {Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy},

  author       = {Huang, Shixin and Makarem, Mohamadamin and Kiemle, Sarah N. and Hamedi, Hossein and Sau, Moujhuri and Cosgrove, Daniel J. and Kim, Seong H.},

  abstractNote = {Sum frequency generation (SFG) vibrational spectroscopy can selectively detect and analyze noncentrosymmetric components interspersed in amorphous matrices; this principle has been used for studies of nanoscale structure and mesoscale assembly of cellulose in plant cell walls. However, the spectral information averaged over a large area or volume cannot provide regiospecific or tissue-specific information of different cells in plants. Here, we demonstrate spatially resolved SFG analysis and imaging by combining a broad-band SFG spectroscopy system with an optical microscope. The system was designed to irradiate both narrow-band 800 nm and broad-band tunable IR beams through a single reflective objective lens, but from opposite sides of the surface normal direction of the sample. The developed technique was used to reveal inhomogeneous distributions of cellulose microfibrils within single cell walls, such as cotton fibers and onion epidermis as well as among different tissues in Arabidopsis inflorescence stems and bamboo culms. SFG microscopy can be used for vibrational spectroscopic imaging of other biological systems in complement to conventional Fourier transform infrared spectroscopy and confocal Raman microscopy.},

  doi          = {10.1021/acs.jpcb.8b01537},

  journal      = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},

  number       = 19,

  volume       = 122,

  place        = {United States},

  year         = {2018},

  month        = {4}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

DOI: https://doi.org/10.1021/acs.jpcb.8b01537

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 6 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Works referencing / citing this record:

Effects of ball milling on the structure of cotton cellulose
journal, January 2019

Ling, Zhe; Wang, Tuo; Makarem, Mohamadamin
Cellulose, Vol. 26, Issue 1
DOI: 10.1007/s10570-018-02230-x

Probing cellulose structures with vibrational spectroscopy
journal, January 2019

Makarem, Mohamadamin; Lee, Christopher M.; Kafle, Kabindra
Cellulose, Vol. 26, Issue 1
DOI: 10.1007/s10570-018-2199-z

High-resolution infrared imaging of biological samples with third-order sum-frequency generation microscopy
journal, January 2018

Hanninen, Adam M.; Prince, Richard C.; Ramos, Raul
Biomedical Optics Express, Vol. 9, Issue 10
DOI: 10.1364/boe.9.004807

Similar Records in DOE PAGES and OSTI.GOV collections:

Dependence of Sum Frequency Generation (SFG) Spectral Features on the Mesoscale Arrangement of SFG-Active Crystalline Domains Interspersed in SFG-Inactive Matrix: A Case Study with Cellulose in Uniaxially Aligned Control Samples and Alkali-Treated Secondary Cell Walls of Plants

Journal Article Makarem, Mohamadamin ; Sawada, Daisuke ; O'Neill, Hugh M. ; ... - Journal of Physical Chemistry. C

Vibrational sum frequency generation (SFG) spectroscopy can selectively detect not only molecules at two-dimensional (2D) interfaces but also noncentrosymmetric domains interspersed in amorphous three-dimensional (3D) matrixes. However, the SFG analysis of 3D systems is more complicated than 2D systems because more variables are involved. One such variable is the distance between SFG-active domains in SFG-inactive matrixes. In this study, we fabricated control samples in which SFG-active cellulose crystals were uniaxially aligned in an amorphous matrix. Assuming uniform separation distances between cellulose crystals, the relative intensities of alkyl (CH) and hydroxyl (OH) SFG peaks of cellulose could be related to themore »« less
Cited by 3
DOI: https://doi.org/10.1021/acs.jpcc.7b02770

Full Text Available
Imaging and quantitative data acquisition of biological cell walls with Atomic Force Microscopy and Scanning Acoustic Microscopy

Book Tittmann, B. R. ; Xi, X.

This chapter demonstrates the feasibility of Atomic Force Microscopy (AFM) and High Frequency Scanning Acoustic Microscopy (HF-SAM) as tools to characterize biological tissues. Both the AFM and the SAM have shown to provide imaging (with different resolution) and quantitative elasticity measuring abilities. Plant cell walls with minimal disturbance and under conditions of their native state have been examined with these two kinds of microscopy. After descriptions of both the SAM and AFM, their special features and the typical sample preparation is discussed. The sample preparation is focused here on epidermal peels of onion scales and celery epidermis cells which weremore »« less
Full Text Available
Multimodal Broadband Vibrational Sum Frequency Generation (MM-BB-V-SFG) Spectrometer and Microscope

Journal Article Lee, Christopher M. ; Kafle, Kabindra ; Huang, Shixin ; ... - Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

A broadband sum frequency generation (BB-SFG) spectrometer with multimodal (MM) capabilities was constructed, which could be routinely reconfigured for tabletop experiments in reflection, transmission, and total internal reflection (TIR) geometries, as well as microscopic imaging. The system was constructed using a Ti:sapphire amplifier (800 nm, pulse width = 85 fs, repetition rate = 2 kHz), an optical parameter amplification (OPA) system for production of broadband IR pulses tunable between 1000 and 4000 cm^–1, and two Fabry–Pérot etalons arranged in series for production of narrowband 800 nm pulses. The key feature allowing the MM operation was the nearly collinear alignment ofmore »« less
Cited by 27
DOI: https://doi.org/10.1021/acs.jpcb.5b10290

Full Text Available
Defining Determinants and Dynamics and Cellulose Microfibril Biosynthesis, Assembly and Degredation OSP Number: 63079/A001

Technical Report

The central paradigm for converting plant biomass into soluble sugars for subsequent conversion to transportation fuels involves the enzymatic depolymerization of lignocellulosic plant cell walls by microbial enzymes. Despite decades of intensive research, this is still a relatively inefficient process, due largely to the recalcitrance and enormous complexity of the substrate. A major obstacle is still insufficient understanding of the detailed structure and biosynthesis of major wall components, including cellulose. For example, although cellulose is generally depicted as rigid, insoluble, uniformly crystalline microfibrils that are resistant to enzymatic degradation, the in vivo structures of plant cellulose microfibrils are surprisingly complex.more »« less
DOI: https://doi.org/10.2172/1361024

Full Text Available
Resonant soft X-ray scattering reveals cellulose microfibril spacing in plant primary cell walls

Journal Article Ye, Dan ; Kiemle, Sarah N. ; Rongpipi, Sintu ; ... - Scientific Reports

Cellulose microfibrils are crucial for many of the remarkable mechanical properties of primary cell walls. Nevertheless, many structural features of cellulose microfibril organization in cell walls are not yet fully described. Microscopy techniques provide direct visualization of cell wall organization, and quantification of some aspects of wall microstructure is possible through image processing. Complementary to microscopy techniques, scattering yields structural information in reciprocal space over large sample areas. Using the onion epidermal wall as a model system, we introduce resonant soft X-ray scattering (RSoXS) to directly quantify the average interfibril spacing. Tuning the X-ray energy to the calcium L-edge enhancesmore »« less
Cited by 4
DOI: https://doi.org/10.1038/s41598-018-31024-1

Similar Records

Title: Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy

Abstract

Citation Formats

Effects of ball milling on the structure of cotton cellulose journal, January 2019

Probing cellulose structures with vibrational spectroscopy journal, January 2019

High-resolution infrared imaging of biological samples with third-order sum-frequency generation microscopy journal, January 2018

Effects of ball milling on the structure of cotton cellulose
journal, January 2019

Probing cellulose structures with vibrational spectroscopy
journal, January 2019

High-resolution infrared imaging of biological samples with third-order sum-frequency generation microscopy
journal, January 2018