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Title: Rhamnogalacturonan-I is a determinant of cell–cell adhesion in poplar wood

Abstract

The molecular basis of cell–cell adhesion in woody tissues is not known. Xylem cells in wood particles of hybrid poplar (Populus tremula 9 P. alba cv. INRA 717-1B4) were separated by oxidation of lignin with acidic sodium chlorite when combined with extraction of xylan and rhamnogalacturonan-I (RG-I) using either dilute alkali or a combination of xylanase and RG-lyase. Acidic chlorite followed by dilute alkali treatment enables cell–cell separation by removing material from the compound middle lamellae between the primary walls. Although lignin is known to contribute to adhesion between wood cells, we found that removing lignin is a necessary but not sufficient condition to effect complete cell–cell separation in poplar lines with various ratios of syringyl:guaiacyl lignin. Transgenic poplar lines expressing an Arabidopsis thaliana gene encoding an RG-lyase (AtRGIL6) showed enhanced cell–cell separation, increased accessibility of cellulose and xylan to hydrolytic enzyme activities, and increased fragmentation of intact wood particles into small cell clusters and single cells under mechanical stress. Our results indicate a novel function for RG-I, and also for xylan, as determinants of cell–cell adhesion in poplar wood cell walls. Genetic control of RG-I content provides a new strategy to increase catalyst accessibility and saccharification yields from woodymore » biomass for biofuels and industrial chemicals.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]
  1. Purdue Univ., West Lafayette, IN (United States)
Publication Date:
Research Org.:
Purdue Univ., West Lafayette, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1625927
Grant/Contract Number:  
SC0000997
Resource Type:
Accepted Manuscript
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Volume: 18; Journal Issue: 4; Journal ID: ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Plant Sciences; cell–cell adhesion; rhamnogalacturonan-I; rhamnogalacturonan lyase; middle lamella; poplar; xylan; lignin; cell wall

Citation Formats

Yang, Haibing, Benatti, Matheus R., Karve, Rucha A., Fox, Arizona, Meilan, Richard, Carpita, Nicholas C., and McCann, Maureen C. Rhamnogalacturonan-I is a determinant of cell–cell adhesion in poplar wood. United States: N. p., 2019. Web. doi:10.1111/pbi.13271.
Yang, Haibing, Benatti, Matheus R., Karve, Rucha A., Fox, Arizona, Meilan, Richard, Carpita, Nicholas C., & McCann, Maureen C. Rhamnogalacturonan-I is a determinant of cell–cell adhesion in poplar wood. United States. https://doi.org/10.1111/pbi.13271
Yang, Haibing, Benatti, Matheus R., Karve, Rucha A., Fox, Arizona, Meilan, Richard, Carpita, Nicholas C., and McCann, Maureen C. Mon . "Rhamnogalacturonan-I is a determinant of cell–cell adhesion in poplar wood". United States. https://doi.org/10.1111/pbi.13271. https://www.osti.gov/servlets/purl/1625927.
@article{osti_1625927,
title = {Rhamnogalacturonan-I is a determinant of cell–cell adhesion in poplar wood},
author = {Yang, Haibing and Benatti, Matheus R. and Karve, Rucha A. and Fox, Arizona and Meilan, Richard and Carpita, Nicholas C. and McCann, Maureen C.},
abstractNote = {The molecular basis of cell–cell adhesion in woody tissues is not known. Xylem cells in wood particles of hybrid poplar (Populus tremula 9 P. alba cv. INRA 717-1B4) were separated by oxidation of lignin with acidic sodium chlorite when combined with extraction of xylan and rhamnogalacturonan-I (RG-I) using either dilute alkali or a combination of xylanase and RG-lyase. Acidic chlorite followed by dilute alkali treatment enables cell–cell separation by removing material from the compound middle lamellae between the primary walls. Although lignin is known to contribute to adhesion between wood cells, we found that removing lignin is a necessary but not sufficient condition to effect complete cell–cell separation in poplar lines with various ratios of syringyl:guaiacyl lignin. Transgenic poplar lines expressing an Arabidopsis thaliana gene encoding an RG-lyase (AtRGIL6) showed enhanced cell–cell separation, increased accessibility of cellulose and xylan to hydrolytic enzyme activities, and increased fragmentation of intact wood particles into small cell clusters and single cells under mechanical stress. Our results indicate a novel function for RG-I, and also for xylan, as determinants of cell–cell adhesion in poplar wood cell walls. Genetic control of RG-I content provides a new strategy to increase catalyst accessibility and saccharification yields from woody biomass for biofuels and industrial chemicals.},
doi = {10.1111/pbi.13271},
journal = {Plant Biotechnology Journal},
number = 4,
volume = 18,
place = {United States},
year = {2019},
month = {10}
}

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Cited by: 15 works
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Figures / Tables:

Figure 1 Figure 1: Cell–cell separation of poplar wood particles after sequential extraction with acidic chlorite and dilute alkali. (a) Bright-field micrographs of toluidine blue-stained wild-type (WT) 717-1B4 particles with acidic chlorite alone for 24 h (AC only); 0.1 M NaOH, dilute alkali, treatment alone for 24 h (NaOH only); 24 hmore » acidic chlorite followed by 24 h dilute alkali (AC→NaOH); and 24 h dilute alkali followed by 24 h acidic chlorite (NaOH→AC). Bar, 100 µm. (b) Micrographs of settled-cell volumes of wood particles in 15-mL Falcon tubes after treatments as indicated. (c) Percentages of cells released from WT and lignin genetic variants as single cells or cell clusters. Top: treatment of WT, high-S lignin (S) and high-G-lignin G, variants with acidic chlorite alone for 24 h (AC only). Middle: treatment with acidic chlorite for 3 h, followed by 0.1 M NaOH for 24 h (3h AC→NaOH). Bottom: treatment with acidic chlorite for 24 h, followed by 0.1 M NaOH. Percentages of single cells (blue) or cell clusters of 2-4 cells (red), 5-10 cells (green), and> 10 cells (purple) were determined from >1000 cells counted per genotype/treatment. Values are the means ± SD (n = 3 technical replicates); asterisks indicate significant differences based on Tukey-Kramer Post Hoc test after one-way ANOVA, P ≤ 0.05 relative to WT.« less

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