TY - JOUR
T1 - Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy
AU - Makarem, Mohamadamin
AU - Nishiyama, Yoshiharu
AU - Xin, Xiaoran
AU - Durachko, Daniel M.
AU - Gu, Ying
AU - Cosgrove, Daniel J.
AU - Kim, Seong H.
N1 - Funding Information:
The theoretical calculations and verification with uniaxially aligned CNC suspensions were conducted with the support by the Center for Lignocellulose Structure and Formation, Energy Frontier Research Center, funded by the U.S. Department of Energy, Office of Science, Basic Energy Sciences, under Award Number DE-SC0001090. The study on the transdifferentiated xylem cells of Arabidopsis and tracheary cellulose coils of celery was carried out as part of the iSuperSEED program of the Penn State MRSEC funded by the National Science Foundation (grant no. DMR-1420620). We are also thankful to the ESRF for allocating us beamtime at D2AM.
PY - 2020/9/17
Y1 - 2020/9/17
N2 - 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. 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.
AB - 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. 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.
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U2 - 10.1021/acs.jpcb.0c07076
DO - 10.1021/acs.jpcb.0c07076
M3 - Article
C2 - 32805111
AN - SCOPUS:85091191715
VL - 124
SP - 8071
EP - 8081
JO - Journal of Physical Chemistry B
JF - Journal of Physical Chemistry B
SN - 1520-6106
IS - 37
ER -