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Title: Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition

Abstract

GAlactUronosylTransferase12 (GAUT12)/IRregular Xylem8 (IRX8) is a putative glycosyltransferase involved in Arabidopsis secondary cell wall biosynthesis. Previous work showed that Arabidopsis irregular xylem8 (irx8) mutants have collapsed xylem due to a reduction in xylan and a lesser reduction in a subfraction of homogalacturonan (HG). We now show that male sterility in the irx8 mutant is due to indehiscent anthers caused by reduced deposition of xylan and lignin in the endothecium cell layer. The reduced lignin content was demonstrated by histochemical lignin staining and pyrolysis Molecular Beam Mass Spectrometry (pyMBMS) and is associated with reduced lignin biosynthesis in irx8 stems. Examination of sequential chemical extracts of stem walls using 2D 13C-1H Heteronuclear Single-Quantum Correlation (HSQC) NMR spectroscopy and antibody-based glycome profiling revealed a reduction in G lignin in the 1 M KOH extract and a concomitant loss of xylan, arabinogalactan and pectin epitopes in the ammonium oxalate, sodium carbonate, and 1 M KOH extracts from the irx8 walls compared with wild-type walls. Immunolabeling of stem sections using the monoclonal antibody CCRC-M138 reactive against an unsubstituted xylopentaose epitope revealed a bi-lamellate pattern in wild-type fiber cells and a collapsed bi-layer in irx8 cells, suggesting that at least in fiber cells, GAUT12 participates inmore » the synthesis of a specific layer or type of xylan or helps to provide an architecture framework required for the native xylan deposition pattern. The results support the hypothesis that GAUT12 functions in the synthesis of a structure required for xylan and lignin deposition during secondary cell wall formation.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [2];  [4];  [4];  [5];  [6];  [3];  [1];  [7]
  1. Univ. of Georgia, Athens, GA (United States). Dept. of Plant Biology; Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  2. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  3. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Univ. of Georgia, Athens, GA (United States). Dept. of Chemistry
  4. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  5. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Lawrence Univ., Appleton, WI (United States). Dept. of Biology
  6. Univ. of Georgia, Athens, GA (United States). Dept. of Plant Biology
  7. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Univ. of Georgia, Athens, GA (United States). Dept. of Biochemistry and Molecular Biology
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division
OSTI Identifier:
1628260
Grant/Contract Number:  
FG02-93ER20097; FG05-93ER20097; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Plant Sciences; secondary cell walls; xylan; lignin; pectin; wall glycan epitopes; anther dehiscence

Citation Formats

Hao, Zhangying, Avci, Utku, Tan, Li, Zhu, Xiang, Glushka, John, Pattathil, Sivakumar, Eberhard, Stefan, Sholes, Tipton, Rothstein, Grace E., Lukowitz, Wolfgang, Orlando, Ron, Hahn, Michael G., and Mohnen, Debra. Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition. United States: N. p., 2014. Web. doi:10.3389/fpls.2014.00357.
Hao, Zhangying, Avci, Utku, Tan, Li, Zhu, Xiang, Glushka, John, Pattathil, Sivakumar, Eberhard, Stefan, Sholes, Tipton, Rothstein, Grace E., Lukowitz, Wolfgang, Orlando, Ron, Hahn, Michael G., & Mohnen, Debra. Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition. United States. https://doi.org/10.3389/fpls.2014.00357
Hao, Zhangying, Avci, Utku, Tan, Li, Zhu, Xiang, Glushka, John, Pattathil, Sivakumar, Eberhard, Stefan, Sholes, Tipton, Rothstein, Grace E., Lukowitz, Wolfgang, Orlando, Ron, Hahn, Michael G., and Mohnen, Debra. Mon . "Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition". United States. https://doi.org/10.3389/fpls.2014.00357. https://www.osti.gov/servlets/purl/1628260.
@article{osti_1628260,
title = {Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition},
author = {Hao, Zhangying and Avci, Utku and Tan, Li and Zhu, Xiang and Glushka, John and Pattathil, Sivakumar and Eberhard, Stefan and Sholes, Tipton and Rothstein, Grace E. and Lukowitz, Wolfgang and Orlando, Ron and Hahn, Michael G. and Mohnen, Debra},
abstractNote = {GAlactUronosylTransferase12 (GAUT12)/IRregular Xylem8 (IRX8) is a putative glycosyltransferase involved in Arabidopsis secondary cell wall biosynthesis. Previous work showed that Arabidopsis irregular xylem8 (irx8) mutants have collapsed xylem due to a reduction in xylan and a lesser reduction in a subfraction of homogalacturonan (HG). We now show that male sterility in the irx8 mutant is due to indehiscent anthers caused by reduced deposition of xylan and lignin in the endothecium cell layer. The reduced lignin content was demonstrated by histochemical lignin staining and pyrolysis Molecular Beam Mass Spectrometry (pyMBMS) and is associated with reduced lignin biosynthesis in irx8 stems. Examination of sequential chemical extracts of stem walls using 2D 13C-1H Heteronuclear Single-Quantum Correlation (HSQC) NMR spectroscopy and antibody-based glycome profiling revealed a reduction in G lignin in the 1 M KOH extract and a concomitant loss of xylan, arabinogalactan and pectin epitopes in the ammonium oxalate, sodium carbonate, and 1 M KOH extracts from the irx8 walls compared with wild-type walls. Immunolabeling of stem sections using the monoclonal antibody CCRC-M138 reactive against an unsubstituted xylopentaose epitope revealed a bi-lamellate pattern in wild-type fiber cells and a collapsed bi-layer in irx8 cells, suggesting that at least in fiber cells, GAUT12 participates in the synthesis of a specific layer or type of xylan or helps to provide an architecture framework required for the native xylan deposition pattern. The results support the hypothesis that GAUT12 functions in the synthesis of a structure required for xylan and lignin deposition during secondary cell wall formation.},
doi = {10.3389/fpls.2014.00357},
journal = {Frontiers in Plant Science},
number = ,
volume = 5,
place = {United States},
year = {Mon Jul 28 00:00:00 EDT 2014},
month = {Mon Jul 28 00:00:00 EDT 2014}
}

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journal, June 2005

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Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase
journal, March 2006

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  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 13, p. 5236-5241
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Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex
journal, November 2011

  • Atmodjo, M. A.; Sakuragi, Y.; Zhu, X.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 50
  • DOI: 10.1073/pnas.1112816108

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

  • Kulkarni, Ameya R.; Peña, Maria J.; Avci, Utku
  • Glycobiology, Vol. 22, Issue 3
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The final split: the regulation of anther dehiscence
journal, February 2011

  • Wilson, Z. A.; Song, J.; Taylor, B.
  • Journal of Experimental Botany, Vol. 62, Issue 5
  • DOI: 10.1093/jxb/err014

Arabidopsis thaliana T-DNA Mutants Implicate GAUT Genes in the Biosynthesis of Pectin and Xylan in Cell Walls and Seed Testa
journal, September 2009

  • Caffall, Kerry H.; Pattathil, Sivakumar; Phillips, Sarah E.
  • Molecular Plant, Vol. 2, Issue 5
  • DOI: 10.1093/mp/ssp062

Two Poplar Glycosyltransferase Genes, PdGATL1.1 and PdGATL1.2, Are Functional Orthologs to PARVUS/AtGATL1 in Arabidopsis
journal, September 2009

  • Kong, Yingzhen; Zhou, Gongke; Avci, Utku
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  • DOI: 10.1093/mp/ssp068

The GAOLAOZHUANGREN1 Gene Encodes a Putative Glycosyltransferase that is Critical for Normal Development and Carbohydrate Metabolism
journal, October 2004

  • Shao, Minghai; Zheng, Huiqiong; Hu, Yi
  • Plant and Cell Physiology, Vol. 45, Issue 10
  • DOI: 10.1093/pcp/pch168

The PARVUS Gene is Expressed in Cells Undergoing Secondary Wall Thickening and is Essential for Glucuronoxylan Biosynthesis
journal, December 2007

  • Lee, Chanhui; Zhong, Ruiqin; Richardson, Elizabeth A.
  • Plant and Cell Physiology, Vol. 48, Issue 12
  • DOI: 10.1093/pcp/pcm155

MYB83 Is a Direct Target of SND1 and Acts Redundantly with MYB46 in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis
journal, October 2009

  • McCarthy, R. L.; Zhong, R.; Ye, Z. -H.
  • Plant and Cell Physiology, Vol. 50, Issue 11
  • DOI: 10.1093/pcp/pcp139

Transcriptome Analyses Show Changes in Gene Expression to Accompany Pollen Germination and Tube Growth in Arabidopsis
journal, September 2008

  • Wang, Yi; Zhang, Wen-Zheng; Song, Lian-Fen
  • Plant Physiology, Vol. 148, Issue 3
  • DOI: 10.1104/pp.108.126375

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

Biochemical and Immunocytological Characterizations of Arabidopsis Pollen Tube Cell Wall
journal, June 2010

  • Dardelle, Flavien; Lehner, Arnaud; Ramdani, Yasmina
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.158881

Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics
journal, June 2005

  • Brown, David M.; Zeef, Leo A. H.; Ellis, Joanne
  • The Plant Cell, Vol. 17, Issue 8
  • DOI: 10.1105/tpc.105.031542

Arabidopsis Fragile Fiber8 , Which Encodes a Putative Glucuronyltransferase, Is Essential for Normal Secondary Wall Synthesis
journal, November 2005


Arabidopsis MYB26/MALE STERILE35 Regulates Secondary Thickening in the Endothecium and Is Essential for Anther Dehiscence
journal, February 2007


The Arabidopsis irregular xylem8 Mutant Is Deficient in Glucuronoxylan and Homogalacturonan, Which Are Essential for Secondary Cell Wall Integrity
journal, January 2007

  • Persson, Staffan; Caffall, Kerry Hosmer; Freshour, Glenn
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