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Title: Immuno and Affinity Cytochemical Analysis of Cell Wall Composition in the Moss Physcomitrella patens

Abstract

In contrast to homeohydric vascular plants, mosses employ a poikilohydric strategy for surviving in the dry aerial environment. A detailed understanding of the structure, composition, and development of moss cell walls can contribute to our understanding of not only the evolution of overall cell wall complexity, but also the differences that have evolved in response to selection for different survival strategies. The model moss species Physcomitrella patens has a predominantly haploid lifecycle consisting of protonemal filaments that regenerate from protoplasts and enlarge by tip growth, and leafy gametophores composed of cells that enlarge by diffuse growth and differentiate into several different types. Advantages for genetic studies include methods for efficient targeted gene modification and extensive genomic resources. Immuno and affinity cytochemical labeling were used to examine the distribution of polysaccharides and proteins in regenerated protoplasts, protonemal filaments, rhizoids, and sectioned gametophores of P. patens. The cell wall composition of regenerated protoplasts was also characterized by flow cytometry. Crystalline cellulose was abundant in the cell walls of regenerating protoplasts and protonemal cells that developed on media of high osmolarity, whereas homogalactuonan was detected in the walls of protonemal cells that developed on low osmolarity media and not in regenerating protoplasts. Mannanmore » was the major hemicellulose detected in all tissues tested. Arabinogalactan proteins were detected in different cell types by different probes, consistent with structural heterogneity. The results reveal developmental and cell type specific differences in cell wall composition and provide a basis for analyzing cell wall phenotypes in knockout mutants.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1]
  1. Univ. of Rhode Island, Kingston, RI (United States). Dept. of Biological Sciences
Publication Date:
Research Org.:
Univ. of Rhode Island, Kingston, RI (United States). Dept. of Biological Sciences; Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1249327
Grant/Contract Number:  
SC0001090; IOS-1257047
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:
60 APPLIED LIFE SCIENCES; affinity cytochemistry; bryophyte; cell wall, flow cytometry; immunofluorescence; Physcomitrella patens

Citation Formats

Berry, Elizabeth A., Tran, Mai L., Dimos, Christos S., Budziszek, Michael J., Scavuzzo-Duggan, Tess R., and Roberts, Alison W. Immuno and Affinity Cytochemical Analysis of Cell Wall Composition in the Moss Physcomitrella patens. United States: N. p., 2016. Web. doi:10.3389/fpls.2016.00248.
Berry, Elizabeth A., Tran, Mai L., Dimos, Christos S., Budziszek, Michael J., Scavuzzo-Duggan, Tess R., & Roberts, Alison W. Immuno and Affinity Cytochemical Analysis of Cell Wall Composition in the Moss Physcomitrella patens. United States. https://doi.org/10.3389/fpls.2016.00248
Berry, Elizabeth A., Tran, Mai L., Dimos, Christos S., Budziszek, Michael J., Scavuzzo-Duggan, Tess R., and Roberts, Alison W. Tue . "Immuno and Affinity Cytochemical Analysis of Cell Wall Composition in the Moss Physcomitrella patens". United States. https://doi.org/10.3389/fpls.2016.00248. https://www.osti.gov/servlets/purl/1249327.
@article{osti_1249327,
title = {Immuno and Affinity Cytochemical Analysis of Cell Wall Composition in the Moss Physcomitrella patens},
author = {Berry, Elizabeth A. and Tran, Mai L. and Dimos, Christos S. and Budziszek, Michael J. and Scavuzzo-Duggan, Tess R. and Roberts, Alison W.},
abstractNote = {In contrast to homeohydric vascular plants, mosses employ a poikilohydric strategy for surviving in the dry aerial environment. A detailed understanding of the structure, composition, and development of moss cell walls can contribute to our understanding of not only the evolution of overall cell wall complexity, but also the differences that have evolved in response to selection for different survival strategies. The model moss species Physcomitrella patens has a predominantly haploid lifecycle consisting of protonemal filaments that regenerate from protoplasts and enlarge by tip growth, and leafy gametophores composed of cells that enlarge by diffuse growth and differentiate into several different types. Advantages for genetic studies include methods for efficient targeted gene modification and extensive genomic resources. Immuno and affinity cytochemical labeling were used to examine the distribution of polysaccharides and proteins in regenerated protoplasts, protonemal filaments, rhizoids, and sectioned gametophores of P. patens. The cell wall composition of regenerated protoplasts was also characterized by flow cytometry. Crystalline cellulose was abundant in the cell walls of regenerating protoplasts and protonemal cells that developed on media of high osmolarity, whereas homogalactuonan was detected in the walls of protonemal cells that developed on low osmolarity media and not in regenerating protoplasts. Mannan was the major hemicellulose detected in all tissues tested. Arabinogalactan proteins were detected in different cell types by different probes, consistent with structural heterogneity. The results reveal developmental and cell type specific differences in cell wall composition and provide a basis for analyzing cell wall phenotypes in knockout mutants.},
doi = {10.3389/fpls.2016.00248},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Tue Mar 08 00:00:00 EST 2016},
month = {Tue Mar 08 00:00:00 EST 2016}
}

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Distribution of cell wall components in Sphagnum hyaline cells and in liverwort and hornwort elaters
journal, July 2004


A CELLULOSE SYNTHASE (CESA) gene essential for gametophore morphogenesis in the moss Physcomitrella patens
journal, January 2012


A (1→4)-β-mannan-specific monoclonal antibody and its use in the immunocytochemical location of galactomannans
journal, December 2001

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journal, November 2006


Isolation and characterization of the cellulose synthase genes PpCesA6 and PpCesA7 in Physcomitrella patens
journal, December 2010


Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling
journal, September 2009

  • Richardt, Sandra; Timmerhaus, Gerrit; Lang, Daniel
  • Plant Molecular Biology, Vol. 72, Issue 1-2
  • DOI: 10.1007/s11103-009-9550-6

An extended set of monoclonal antibodies to pectic homogalacturonan
journal, September 2009


Evolution and diversity of green plant cell walls
journal, June 2008


Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: Implication for land plant evolution
journal, June 2003

  • Nishiyama, T.; Fujita, T.; Shin-I, T.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 13
  • DOI: 10.1073/pnas.0932694100

Physcomitrella patens : A moss system for the study of plant cell walls
journal, March 2005

  • Lee, Kjd; Knight, Cd; Knox, Jp
  • Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, Vol. 139, Issue 1
  • DOI: 10.1080/11263500500055213

Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants
journal, September 1995


Novel localization of callose in the spores of Physcomitrella patens and phylogenomics of the callose synthase gene family
journal, January 2009

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The ability of land plants to synthesize glucuronoxylans predates the evolution of tracheophytes
journal, November 2011

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  • Glycobiology, Vol. 22, Issue 3
  • DOI: 10.1093/glycob/cwr117

Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens
journal, April 2007

  • Menand, Benoît; Calder, Grant; Dolan, Liam
  • Journal of Experimental Botany, Vol. 58, Issue 7
  • DOI: 10.1093/jxb/erm047

The impact of abiotic factors on cellulose synthesis
journal, November 2015

  • Wang, Ting; McFarlane, Heather E.; Persson, Staffan
  • Journal of Experimental Botany, Vol. 67, Issue 2
  • DOI: 10.1093/jxb/erv488

Cell Wall Biology: Perspectives from Cell Wall Imaging
journal, March 2011

  • Lee, Kieran J. D.; Marcus, Susan E.; Knox, J. Paul
  • Molecular Plant, Vol. 4, Issue 2
  • DOI: 10.1093/mp/ssq075

Functional Genomic Analysis Supports Conservation of Function Among Cellulose Synthase-Like A Gene Family Members and Suggests Diverse Roles of Mannans in Plants
journal, February 2007

  • Liepman, Aaron H.; Nairn, C. Joseph; Willats, William G. T.
  • Plant Physiology, Vol. 143, Issue 4
  • DOI: 10.1104/pp.106.093989

Developmental Stage Specificity and the Role of Mitochondrial Metabolism in the Response of Arabidopsis Leaves to Prolonged Mild Osmotic Stress
journal, November 2009

  • Skirycz, Aleksandra; De Bodt, Stefanie; Obata, Toshihiro
  • Plant Physiology, Vol. 152, Issue 1
  • DOI: 10.1104/pp.109.148965

A Comprehensive Toolkit of Plant Cell Wall Glycan-Directed Monoclonal Antibodies
journal, April 2010

  • Pattathil, S.; Avci, U.; Baldwin, D.
  • Plant Physiology, Vol. 153, Issue 2, p. 514-525
  • DOI: 10.1104/pp.109.151985

Evolution and Function of the Plant Cell Wall Synthesis-Related Glycosyltransferase Family 8
journal, June 2010

  • Yin, Yanbin; Chen, Huiling; Hahn, Michael G.
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.154229

Localization of Pectic Galactan in Tomato Cell Walls Using a Monoclonal Antibody Specific to (1[->]4)-[beta]-D-Galactan
journal, April 1997


Alteration of the Physical and Chemical Structure of the Primary Cell Wall of Growth-Limited Plant Cells Adapted to Osmotic Stress
journal, September 1989

  • Iraki, Naim M.; Bressan, Ray A.; Hasegawa, P. M.
  • Plant Physiology, Vol. 91, Issue 1
  • DOI: 10.1104/pp.91.1.39

Cell Walls of Tobacco Cells and Changes in Composition Associated with Reduced Growth upon Adaptation to Water and Saline Stress
journal, September 1989

  • Iraki, Naim M.; Singh, Narendra; Bressan, Ray A.
  • Plant Physiology, Vol. 91, Issue 1
  • DOI: 10.1104/pp.91.1.48

Arabinogalactan Proteins Are Required for Apical Cell Extension in the Moss Physcomitrella patens
journal, September 2005

  • Lee, Kieran J. D.; Sakata, Yoichi; Mau, Shaio-Lim
  • The Plant Cell, Vol. 17, Issue 11
  • DOI: 10.1105/tpc.105.034413

Flow sorting and culture of plant protoplasts
journal, January 1984


Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss, Physcomitrella patens
journal, October 2007


Mapping the walls of the kingdom: the view from the horsetails
journal, July 2008


Arabidopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases
journal, September 2014

  • Jensen, Jacob Krüger; Johnson, Nathan Robert; Wilkerson, Curtis Gene
  • The Plant Journal, Vol. 80, Issue 2
  • DOI: 10.1111/tpj.12641

The Physcomitrella Genome Reveals Evolutionary Insights into the Conquest of Land by Plants
journal, December 2007


Callose deposition in the primary wall of suspension cells and regenerating protoplasts, and its relationship to patterned cellulose synthesis
journal, July 1996

  • Amstel, Ton N. M. van; Kengen, Harry M. P.
  • Canadian Journal of Botany, Vol. 74, Issue 7
  • DOI: 10.1139/b96-128

Phylogenetic analysis of pectin-related gene families in Physcomitrella patens and nine other plant species yields evolutionary insights into cell walls
journal, January 2014

  • McCarthy, Thomas W.; Der, Joshua P.; Honaas, Loren A.
  • BMC Plant Biology, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2229-14-79

The cellulose synthase superfamily in fully sequenced plants and algae
journal, January 2009


Antibody-based screening of cell wall matrix glycans in ferns reveals taxon, tissue and cell-type specific distribution patterns
journal, January 2015


The Glycosyltransferase Repertoire of the Spikemoss Selaginella moellendorffii and a Comparative Study of Its Cell Wall
journal, May 2012


Moss cell walls: structure and biosynthesis
journal, January 2012

  • Roberts, Alison W.; Roberts, Eric M.; Haigler, Candace H.
  • Frontiers in Plant Science, Vol. 3
  • DOI: 10.3389/fpls.2012.00166

Callose synthesis in higher plants
journal, June 2009

  • Chen, Xiong-Yan; Kim, Jae-Yean
  • Plant Signaling & Behavior, Vol. 4, Issue 6
  • DOI: 10.4161/psb.4.6.8359

Works referencing / citing this record:

Moss Pathogenesis-Related-10 Protein Enhances Resistance to Pythium irregulare in Physcomitrella patens and Arabidopsis thaliana
journal, April 2016

  • Castro, Alexandra; Vidal, Sabina; Ponce de León, Inés
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00580