DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability

Abstract

The composition, integrity, and architecture of the macromolecular matrix of cell walls, collectively referred to as cell wall ultrastructure, exhibits variation across species and organs and among cell types within organs. Indirect approaches have suggested that modifications to cell wall ultrastructure occur in response to abiotic stress; however, modifications have not been directly observed. Glycome profiling was used to study cell wall ultrastructure by examining variation in composition and extractability of non-cellulosic glycans in cell walls of stem wood, roots, and needles of loblolly pine saplings exposed to high and low soil moisture. Soil moisture influenced physiological processes and the overall composition and extractability of cell wall components differed as a function of soil moisture treatments. The strongest response of cell wall ultrastructure to soil moisture was increased extractability of pectic backbone epitopes in the low soil moisture treatment. The higher abundance of these pectic backbone epitopes in the oxalate extract indicate that the loosening of cell wall pectic components could be associated with the release of pectic signals as a stress response. The increased extractability of pectic backbone epitopes in response to low soil moisture availability was more pronounced in stem wood than in roots or needles. Additional responsesmore » to low soil moisture availability were observed in lignin associated carbohydrates released in chlorite extracts of stem wood, including an increased abundance of pectic arabinogalactan epitopes. Overall, these results indicate that cell walls of loblolly pine organs undergo changes in their ultrastructural composition and extractability as a response to soil moisture availability and that cell walls of the stem wood are more responsive to low soil moisture availability compared to cell walls of roots and needles. In conclusion, to our knowledge, this is the first direct evidence, delineated by glycomic analyses, that abiotic stress affects cell wall ultrastructure. This study is also unique in that glycome profiling of pine needles has never before been reported.« less

Authors:
 [1];  [2];  [1];  [1];  [2];  [2];  [3]
  1. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  2. Univ. of Georgia, Athens, GA (United States). Daniel B. Warnell School of Forestry and Natural Resources
  3. Univ. of Georgia, Athens, GA (United States). Daniel B. Warnell School of Forestry and Natural Resources;Univ. of Georgia, Aiken, SC (United States). Savannah River Ecology Laboratory
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1285865
Grant/Contract Number:  
AC05-00OR22725; 2011-67009-30065; 2013-67009-21405
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; cell walls; glycome profiling; moisture stress; monoclonal antibodies; pectin; Pinus taeda; xylan; pine pinus-taeda; carbon-isotope discrimination; loblolly-pine; arabidopsis-thaliana; extracellular-matrix; vascular tissues; elastic-modulus; drought stress; abiotic stress; water-deficit

Citation Formats

Pattathil, Sivakumar, Ingwers, Miles W., Victoriano, Olivia L., Kandemkavil, Sindhu, McGuire, Mary Anne, Teskey, Robert O., and Aubrey, Doug P.. Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability. United States: N. p., 2016. Web. doi:10.3389/fpls.2016.00882.
Pattathil, Sivakumar, Ingwers, Miles W., Victoriano, Olivia L., Kandemkavil, Sindhu, McGuire, Mary Anne, Teskey, Robert O., & Aubrey, Doug P.. Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability. United States. https://doi.org/10.3389/fpls.2016.00882
Pattathil, Sivakumar, Ingwers, Miles W., Victoriano, Olivia L., Kandemkavil, Sindhu, McGuire, Mary Anne, Teskey, Robert O., and Aubrey, Doug P.. Fri . "Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability". United States. https://doi.org/10.3389/fpls.2016.00882. https://www.osti.gov/servlets/purl/1285865.
@article{osti_1285865,
title = {Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability},
author = {Pattathil, Sivakumar and Ingwers, Miles W. and Victoriano, Olivia L. and Kandemkavil, Sindhu and McGuire, Mary Anne and Teskey, Robert O. and Aubrey, Doug P.},
abstractNote = {The composition, integrity, and architecture of the macromolecular matrix of cell walls, collectively referred to as cell wall ultrastructure, exhibits variation across species and organs and among cell types within organs. Indirect approaches have suggested that modifications to cell wall ultrastructure occur in response to abiotic stress; however, modifications have not been directly observed. Glycome profiling was used to study cell wall ultrastructure by examining variation in composition and extractability of non-cellulosic glycans in cell walls of stem wood, roots, and needles of loblolly pine saplings exposed to high and low soil moisture. Soil moisture influenced physiological processes and the overall composition and extractability of cell wall components differed as a function of soil moisture treatments. The strongest response of cell wall ultrastructure to soil moisture was increased extractability of pectic backbone epitopes in the low soil moisture treatment. The higher abundance of these pectic backbone epitopes in the oxalate extract indicate that the loosening of cell wall pectic components could be associated with the release of pectic signals as a stress response. The increased extractability of pectic backbone epitopes in response to low soil moisture availability was more pronounced in stem wood than in roots or needles. Additional responses to low soil moisture availability were observed in lignin associated carbohydrates released in chlorite extracts of stem wood, including an increased abundance of pectic arabinogalactan epitopes. Overall, these results indicate that cell walls of loblolly pine organs undergo changes in their ultrastructural composition and extractability as a response to soil moisture availability and that cell walls of the stem wood are more responsive to low soil moisture availability compared to cell walls of roots and needles. In conclusion, to our knowledge, this is the first direct evidence, delineated by glycomic analyses, that abiotic stress affects cell wall ultrastructure. This study is also unique in that glycome profiling of pine needles has never before been reported.},
doi = {10.3389/fpls.2016.00882},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Fri Jun 24 00:00:00 EDT 2016},
month = {Fri Jun 24 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Distribution of (1->4)- -galactans, arabinogalactan proteins, xylans and (1->3)- -glucans in tracheid cell walls of softwoods
journal, April 2010


Functional groups show distinct differences in nitrogen cycling during early stand development: implications for forest management
journal, August 2011


Wood contains a cell-wall structural protein.
journal, July 1992

  • Bao, W.; O'Malley, D. M.; Sederoff, R. R.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 14
  • DOI: 10.1073/pnas.89.14.6604

Genes commonly regulated by water-deficit stress in Arabidopsis thaliana
journal, September 2004


Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivars
journal, August 2002


Assembly and Enlargement of the Primary cell wall in Plants
journal, November 1997


Changes in the tobacco leaf apoplast proteome in response to salt stress
journal, January 2005


Solute accumulation and elastic modulus changes in six radiata pine breeds exposed to drought
journal, January 2013


Application of monoclonal antibodies to investigate plant cell wall deconstruction for biofuels production
journal, January 2011

  • DeMartini, Jaclyn D.; Pattathil, Sivakumar; Avci, Utku
  • Energy & Environmental Science, Vol. 4, Issue 10
  • DOI: 10.1039/c1ee02112e

"Contrasting Patterns of Selection at Pinus pinaster Ait. Drought Stress Candidate Genes as Revealed by Genetic Differentiation Analyses"
journal, January 2008

  • Eveno, E.; Collada, C.; Guevara, M. A.
  • Molecular Biology and Evolution, Vol. 25, Issue 2
  • DOI: 10.1093/molbev/msm272

Cell wall evolution and diversity
journal, January 2012


Carbon Isotope Discrimination and Photosynthesis
journal, June 1989

  • Farquhar, G. D.; Ehleringer, J. R.; Hubick, K. T.
  • Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 40, Issue 1, p. 503-537
  • DOI: 10.1146/annurev.pp.40.060189.002443

Developmental and Tissue-Specific Structural Alterations of the Cell-Wall Polysaccharides of Arabidopsis thaliana Roots
journal, April 1996

  • Freshour, G.; Clay, R. P.; Fuller, M. S.
  • Plant Physiology, Vol. 110, Issue 4
  • DOI: 10.1104/pp.110.4.1413

Plant cell walls: supramolecular assembly, signalling and stress
journal, February 2009


Apparent homology of expressed genes from wood-forming tissues of loblolly pine (Pinus taeda L.) with Arabidopsis thaliana
journal, May 2003

  • Kirst, M.; Johnson, A. F.; Baucom, C.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 12
  • DOI: 10.1073/pnas.1132171100

Revealing the structural and functional diversity of plant cell walls
journal, June 2008


Cell wall proteome of wheat roots under flooding stress using gel-based and LC MS/MS-based proteomics approaches
journal, January 2010

  • Kong, Fan-Jiang; Oyanagi, Atsushi; Komatsu, Setsuko
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 1
  • DOI: 10.1016/j.bbapap.2009.09.023

Cell Wall Metabolism in Response to Abiotic Stress
journal, February 2015

  • Le Gall, Hyacinthe; Philippe, Florian; Domon, Jean-Marc
  • Plants, Vol. 4, Issue 1
  • DOI: 10.3390/plants4010112

Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis
journal, October 2013

  • Liang, Yan; Basu, Debarati; Pattathil, Sivakumar
  • Journal of Experimental Botany, Vol. 64, Issue 18
  • DOI: 10.1093/jxb/ert321

Water stress-responsive genes in loblolly pine (Pinus taeda) roots identified by analyses of expressed sequence tag libraries
journal, January 2006


Chemical Linkage of Pine Polysaccharides to Lignin
journal, January 1982


Carbohydrate-related genes and cell wall biosynthesis in vascular tissues of loblolly pine (Pinus taeda)
journal, July 2008


An automated system for controlling drought stress and irrigation in potted plants
journal, November 2006


Identification of Extracellular Matrix Proteins of Rice ( Oryza sativa L.) Involved in Dehydration-Responsive Network: A Proteomic Approach
journal, July 2010

  • Pandey, Aarti; Rajamani, Uma; Verma, Jitendra
  • Journal of Proteome Research, Vol. 9, Issue 7
  • DOI: 10.1021/pr901098p

Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense
journal, September 2004


Immunological Approaches to Plant Cell Wall and Biomass Characterization: Glycome Profiling
book, January 2012


Insights into plant cell wall structure, architecture, and integrity using glycome profiling of native and AFEX TM -pre-treated biomass
journal, April 2015

  • Pattathil, Sivakumar; Hahn, Michael G.; Dale, Bruce E.
  • Journal of Experimental Botany, Vol. 66, Issue 14
  • DOI: 10.1093/jxb/erv107

Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants
journal, June 2011


Abnormal Lignin in a Loblolly Pine Mutant
journal, July 1997


Automated Synthesis of Arabinoxylan-Oligosaccharides Enables Characterization of Antibodies that Recognize Plant Cell Wall Glycans
journal, February 2015

  • Schmidt, Deborah; Schuhmacher, Frank; Geissner, Andreas
  • Chemistry - A European Journal, Vol. 21, Issue 15
  • DOI: 10.1002/chem.201500065

Irritable Walls: The Plant Extracellular Matrix and Signaling
journal, February 2010


Cell wall remodeling under abiotic stress
journal, January 2015


Growth control by cell wall pectins
journal, January 2012


Examination of water phase transitions in Loblolly pine and cell wall components by differential scanning calorimetry
journal, April 2012


Differential expression of genes encoding cell wall proteins in vascular tissues from vertical and bent loblolly pine trees
journal, April 2000


Hydrogel Control of Xylem Hydraulic Resistance in Plants
journal, January 2001


Automated Synthesis of Arabinoxylan-Oligosaccharides Enables Characterization of Antibodies that Recognize Plant Cell Wall Glycans
journal, February 2015

  • Schmidt, Deborah; Schuhmacher, Frank; Geissner, Andreas
  • Chemistry - A European Journal, Vol. 21, Issue 15
  • DOI: 10.1002/chem.201500065

Changes in the tobacco leaf apoplast proteome in response to salt stress
journal, January 2005


Control of thickness of collenchyma cell walls by pectins
journal, May 1992


Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense
journal, September 2004


Growth control by cell wall pectins
journal, January 2012


Functional groups show distinct differences in nitrogen cycling during early stand development: implications for forest management
journal, August 2011


Plant cell walls: supramolecular assembly, signalling and stress
journal, February 2009


Cell wall proteome of wheat roots under flooding stress using gel-based and LC MS/MS-based proteomics approaches
journal, January 2010

  • Kong, Fan-Jiang; Oyanagi, Atsushi; Komatsu, Setsuko
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 1
  • DOI: 10.1016/j.bbapap.2009.09.023

Revealing the structural and functional diversity of plant cell walls
journal, June 2008


An automated system for controlling drought stress and irrigation in potted plants
journal, November 2006


Examination of water phase transitions in Loblolly pine and cell wall components by differential scanning calorimetry
journal, April 2012


Identification of Extracellular Matrix Proteins of Rice ( Oryza sativa L.) Involved in Dehydration-Responsive Network: A Proteomic Approach
journal, July 2010

  • Pandey, Aarti; Rajamani, Uma; Verma, Jitendra
  • Journal of Proteome Research, Vol. 9, Issue 7
  • DOI: 10.1021/pr901098p

Application of monoclonal antibodies to investigate plant cell wall deconstruction for biofuels production
journal, January 2011

  • DeMartini, Jaclyn D.; Pattathil, Sivakumar; Avci, Utku
  • Energy & Environmental Science, Vol. 4, Issue 10
  • DOI: 10.1039/c1ee02112e

Apparent homology of expressed genes from wood-forming tissues of loblolly pine (Pinus taeda L.) with Arabidopsis thaliana
journal, May 2003

  • Kirst, M.; Johnson, A. F.; Baucom, C.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 12
  • DOI: 10.1073/pnas.1132171100

Wood contains a cell-wall structural protein.
journal, July 1992

  • Bao, W.; O'Malley, D. M.; Sederoff, R. R.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 14
  • DOI: 10.1073/pnas.89.14.6604

Chemical Linkage of Pine Polysaccharides to Lignin
journal, January 1982


Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis
journal, October 2013

  • Liang, Yan; Basu, Debarati; Pattathil, Sivakumar
  • Journal of Experimental Botany, Vol. 64, Issue 18
  • DOI: 10.1093/jxb/ert321

"Contrasting Patterns of Selection at Pinus pinaster Ait. Drought Stress Candidate Genes as Revealed by Genetic Differentiation Analyses"
journal, January 2008

  • Eveno, E.; Collada, C.; Guevara, M. A.
  • Molecular Biology and Evolution, Vol. 25, Issue 2
  • DOI: 10.1093/molbev/msm272

Differential expression of genes encoding cell wall proteins in vascular tissues from vertical and bent loblolly pine trees
journal, April 2000


Water stress-responsive genes in loblolly pine (Pinus taeda) roots identified by analyses of expressed sequence tag libraries
journal, January 2006


Carbohydrate-related genes and cell wall biosynthesis in vascular tissues of loblolly pine (Pinus taeda)
journal, July 2008


Distribution of (1->4)- -galactans, arabinogalactan proteins, xylans and (1->3)- -glucans in tracheid cell walls of softwoods
journal, April 2010


Solute accumulation and elastic modulus changes in six radiata pine breeds exposed to drought
journal, January 2013


Developmental and Tissue-Specific Structural Alterations of the Cell-Wall Polysaccharides of Arabidopsis thaliana Roots
journal, April 1996

  • Freshour, G.; Clay, R. P.; Fuller, M. S.
  • Plant Physiology, Vol. 110, Issue 4
  • DOI: 10.1104/pp.110.4.1413

Hydrogel Control of Xylem Hydraulic Resistance in Plants
journal, January 2001


Abnormal Lignin in a Loblolly Pine Mutant
journal, July 1997


Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants
journal, June 2011


Assembly and Enlargement of the Primary cell wall in Plants
journal, November 1997


Carbon Isotope Discrimination and Photosynthesis
journal, June 1989

  • Farquhar, G. D.; Ehleringer, J. R.; Hubick, K. T.
  • Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 40, Issue 1, p. 503-537
  • DOI: 10.1146/annurev.pp.40.060189.002443

Earlywood and latewood elastic properties in loblolly pine
journal, September 2005

  • Cramer, Steven; Kretschmann, David; Lakes, Roderic
  • Holzforschung, Vol. 59, Issue 5
  • DOI: 10.1515/hf.2005.088

Cell wall evolution and diversity
journal, January 2012


Cell Wall Metabolism in Response to Abiotic Stress
journal, February 2015

  • Le Gall, Hyacinthe; Philippe, Florian; Domon, Jean-Marc
  • Plants, Vol. 4, Issue 1
  • DOI: 10.3390/plants4010112

Works referencing / citing this record:

ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE 1 (ADPG1) releases latent defense signals in stems with reduced lignin content
journal, January 2020

  • Gallego-Giraldo, Lina; Liu, Chang; Pose-Albacete, Sara
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 6
  • DOI: 10.1073/pnas.1914422117

ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE 1 (ADPG1) releases latent defense signals in stems with reduced lignin content
journal, January 2020

  • Gallego-Giraldo, Lina; Liu, Chang; Pose-Albacete, Sara
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 6
  • DOI: 10.1073/pnas.1914422117