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Title: Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy

Abstract

Cellulose in plant cell walls are synthesized as crystalline microfibrils with diameters of 3–4 nm and lengths of around 1–10 μm. These microfibrils are known to be the backbone of cell walls, and their multiscale three-dimensional organization plays a critical role in cell wall functions including plant growth and recalcitrance to degradation. The mesoscale organization of microfibrils over a 1–100 nm range in cell walls is challenging to resolve because most characterization techniques investigating this length scale suffer from low spatial resolution, sample preparation artifacts, or inaccessibility of specific cell types. Here, we report a sum frequency generation (SFG) study determining the mesoscale polarity of cellulose microfibrils in intact plant cell walls. SFG is a nonlinear optical spectroscopy technique sensitive to the molecular-to-mesoscale order of noncentrosymmetric domains in amorphous matrices. However, the quantitative theoretical model to unravel the effect of polarity in packing of noncentrosymmetric domains on SFG spectral features has remained unresolved. In this work, we show how the phase synchronization principle of the SFG process is used to predict the relative intensities of vibrational modes with different polar angles from the noncentrosymmetric domain axis. Applying this model calculation for the first time and employing SFG microscopy, we foundmore » that cellulose microfibrils in certain xylem cell walls are deposited unidirectionally (or biased in one direction) instead of the bidirectional polarity which was believed to be dominant in plant cell walls from volume-averaged characterizations of macroscopic samples. Here, with this advancement in SFG analysis, one can now determine the relative polarity of noncentrosymmetric domains such as crystalline biopolymers interspersed in amorphous polymer matrices, which will open opportunities to study new questions that have not been conceived in the past.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [1]
+ Show Author Affiliations
  1. Pennsylvania State Univ., University Park, PA (United States)
  2. Univ. Grenoble Alpes (France)
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
OSTI Identifier:
1873670
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: 124; Journal Issue: 37; Journal ID: ISSN 1520-6106
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 36 MATERIALS SCIENCE; Cells; Cellulose; Crystals; Nonlinear optics; Polarity

Citation Formats

Makarem, Mohamadamin, Nishiyama, Yoshiharu, Xin, Xiaoran, Durachko, Daniel M., Gu, Ying, Cosgrove, Daniel J., and Kim, Seong H. Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy. United States: N. p., 2020. Web. doi:10.1021/acs.jpcb.0c07076.
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Makarem, Mohamadamin, Nishiyama, Yoshiharu, Xin, Xiaoran, Durachko, Daniel M., Gu, Ying, Cosgrove, Daniel J., & Kim, Seong H. Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy. United States. https://doi.org/10.1021/acs.jpcb.0c07076
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Makarem, Mohamadamin, Nishiyama, Yoshiharu, Xin, Xiaoran, Durachko, Daniel M., Gu, Ying, Cosgrove, Daniel J., and Kim, Seong H. Mon . "Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy". United States. https://doi.org/10.1021/acs.jpcb.0c07076. https://www.osti.gov/servlets/purl/1873670.
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@article{osti_1873670,
title = {Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy},
author = {Makarem, Mohamadamin and Nishiyama, Yoshiharu and Xin, Xiaoran and Durachko, Daniel M. and Gu, Ying and Cosgrove, Daniel J. and Kim, Seong H.},
abstractNote = {Cellulose in plant cell walls are synthesized as crystalline microfibrils with diameters of 3–4 nm and lengths of around 1–10 μm. These microfibrils are known to be the backbone of cell walls, and their multiscale three-dimensional organization plays a critical role in cell wall functions including plant growth and recalcitrance to degradation. The mesoscale organization of microfibrils over a 1–100 nm range in cell walls is challenging to resolve because most characterization techniques investigating this length scale suffer from low spatial resolution, sample preparation artifacts, or inaccessibility of specific cell types. Here, we report a sum frequency generation (SFG) study determining the mesoscale polarity of cellulose microfibrils in intact plant cell walls. SFG is a nonlinear optical spectroscopy technique sensitive to the molecular-to-mesoscale order of noncentrosymmetric domains in amorphous matrices. However, the quantitative theoretical model to unravel the effect of polarity in packing of noncentrosymmetric domains on SFG spectral features has remained unresolved. In this work, we show how the phase synchronization principle of the SFG process is used to predict the relative intensities of vibrational modes with different polar angles from the noncentrosymmetric domain axis. Applying this model calculation for the first time and employing SFG microscopy, we found that cellulose microfibrils in certain xylem cell walls are deposited unidirectionally (or biased in one direction) instead of the bidirectional polarity which was believed to be dominant in plant cell walls from volume-averaged characterizations of macroscopic samples. Here, with this advancement in SFG analysis, one can now determine the relative polarity of noncentrosymmetric domains such as crystalline biopolymers interspersed in amorphous polymer matrices, which will open opportunities to study new questions that have not been conceived in the past.},
doi = {10.1021/acs.jpcb.0c07076},
journal = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},
number = 37,
volume = 124,
place = {United States},
year = {Mon Aug 17 00:00:00 EDT 2020},
month = {Mon Aug 17 00:00:00 EDT 2020}
}
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