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Title: Cytosolic Acetyl-CoA Generated by ATP-Citrate Lyase Is Essential for Acetylation of Cell Wall Polysaccharides

Abstract

Abstract Plant cell wall polysaccharides, including xylan, glucomannan, xyloglucan and pectin, are often acetylated. Although a number of acetyltransferases responsible for the acetylation of some of these polysaccharides have been biochemically characterized, little is known about the source of acetyl donors and how acetyl donors are translocated into the Golgi, where these polysaccharides are synthesized. In this report, we investigated roles of ATP-citrate lyase (ACL) that generates cytosolic acetyl-CoA in cell wall polysaccharide acetylation and effects of simultaneous mutations of four Reduced Wall Acetylation (RWA) genes on acetyl-CoA transport into the Golgi in Arabidopsis thaliana. Expression analyses of genes involved in the generation of acetyl-CoA in different subcellular compartments showed that the expression of several ACL genes responsible for cytosolic acetyl-CoA synthesis was elevated in interfascicular fiber cells and induced by secondary wall-associated transcriptional activators. Simultaneous downregulation of the expression of ACL genes was demonstrated to result in a substantial decrease in the degree of xylan acetylation and a severe alteration in secondary wall structure in xylem vessels. In addition, the degree of acetylation of other cell wall polysaccharides, including glucomannan, xyloglucan and pectin, was also reduced. Moreover, Golgi-enriched membrane vesicles isolated from the rwa1/2/3/4 quadruple mutant were found tomore » exhibit a drastic reduction in acetyl-CoA transport activity compared with the wild type. These findings indicate that cytosolic acetyl-CoA generated by ACL is essential for cell wall polysaccharide acetylation and RWAs are required for its transport from the cytosol into the Golgi.« less

Authors:
 [1];  [2];  [3];  [2];  [4];  [4]; ORCiD logo [1]
  1. Department of Plant Biology, University of Georgia, Athens, GA 30602, USA
  2. Department of Chemistry, University of Georgia, Athens, GA 30602, USA
  3. Georgia Electron Microscopy, University of Georgia, Athens, GA 30602, USA
  4. Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USA
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1599930
Alternate Identifier(s):
OSTI ID: 1964042
Grant/Contract Number:  
SC0015662; FG02-03ER15415
Resource Type:
Published Article
Journal Name:
Plant and Cell Physiology
Additional Journal Information:
Journal Name: Plant and Cell Physiology Journal Volume: 61 Journal Issue: 1; Journal ID: ISSN 0032-0781
Publisher:
Oxford University Press
Country of Publication:
Japan
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Acetyl-CoA; Acetylation; Acetyltransferase; Arabidopsis; Cell wall

Citation Formats

Zhong, Ruiqin, Cui, Dongtao, Richardson, Elizabeth A., Phillips, Dennis R., Azadi, Parastoo, Lu, Grace, and Ye, Zheng-Hua. Cytosolic Acetyl-CoA Generated by ATP-Citrate Lyase Is Essential for Acetylation of Cell Wall Polysaccharides. Japan: N. p., 2019. Web. doi:10.1093/pcp/pcz178.
Zhong, Ruiqin, Cui, Dongtao, Richardson, Elizabeth A., Phillips, Dennis R., Azadi, Parastoo, Lu, Grace, & Ye, Zheng-Hua. Cytosolic Acetyl-CoA Generated by ATP-Citrate Lyase Is Essential for Acetylation of Cell Wall Polysaccharides. Japan. https://doi.org/10.1093/pcp/pcz178
Zhong, Ruiqin, Cui, Dongtao, Richardson, Elizabeth A., Phillips, Dennis R., Azadi, Parastoo, Lu, Grace, and Ye, Zheng-Hua. Tue . "Cytosolic Acetyl-CoA Generated by ATP-Citrate Lyase Is Essential for Acetylation of Cell Wall Polysaccharides". Japan. https://doi.org/10.1093/pcp/pcz178.
@article{osti_1599930,
title = {Cytosolic Acetyl-CoA Generated by ATP-Citrate Lyase Is Essential for Acetylation of Cell Wall Polysaccharides},
author = {Zhong, Ruiqin and Cui, Dongtao and Richardson, Elizabeth A. and Phillips, Dennis R. and Azadi, Parastoo and Lu, Grace and Ye, Zheng-Hua},
abstractNote = {Abstract Plant cell wall polysaccharides, including xylan, glucomannan, xyloglucan and pectin, are often acetylated. Although a number of acetyltransferases responsible for the acetylation of some of these polysaccharides have been biochemically characterized, little is known about the source of acetyl donors and how acetyl donors are translocated into the Golgi, where these polysaccharides are synthesized. In this report, we investigated roles of ATP-citrate lyase (ACL) that generates cytosolic acetyl-CoA in cell wall polysaccharide acetylation and effects of simultaneous mutations of four Reduced Wall Acetylation (RWA) genes on acetyl-CoA transport into the Golgi in Arabidopsis thaliana. Expression analyses of genes involved in the generation of acetyl-CoA in different subcellular compartments showed that the expression of several ACL genes responsible for cytosolic acetyl-CoA synthesis was elevated in interfascicular fiber cells and induced by secondary wall-associated transcriptional activators. Simultaneous downregulation of the expression of ACL genes was demonstrated to result in a substantial decrease in the degree of xylan acetylation and a severe alteration in secondary wall structure in xylem vessels. In addition, the degree of acetylation of other cell wall polysaccharides, including glucomannan, xyloglucan and pectin, was also reduced. Moreover, Golgi-enriched membrane vesicles isolated from the rwa1/2/3/4 quadruple mutant were found to exhibit a drastic reduction in acetyl-CoA transport activity compared with the wild type. These findings indicate that cytosolic acetyl-CoA generated by ACL is essential for cell wall polysaccharide acetylation and RWAs are required for its transport from the cytosol into the Golgi.},
doi = {10.1093/pcp/pcz178},
journal = {Plant and Cell Physiology},
number = 1,
volume = 61,
place = {Japan},
year = {Tue Sep 10 00:00:00 EDT 2019},
month = {Tue Sep 10 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1093/pcp/pcz178

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Works referenced in this record:

Demethylesterification of the Primary Wall by PECTIN METHYLESTERASE35 Provides Mechanical Support to the Arabidopsis Stem
journal, June 2012


Roles of Arabidopsis TBL34 and TBL35 in xylan acetylation and plant growth
journal, February 2016


Secondary cell wall biosynthesis
journal, November 2018

  • Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng‐Hua
  • New Phytologist, Vol. 221, Issue 4
  • DOI: 10.1111/nph.15537

The MYB46 Transcription Factor Is a Direct Target of SND1 and Regulates Secondary Wall Biosynthesis in Arabidopsis
journal, September 2007

  • Zhong, R.; Richardson, E. A.; Ye, Z.-H.
  • The Plant Cell Online, Vol. 19, Issue 9, p. 2776-2792
  • DOI: 10.1105/tpc.107.053678

Isolation of a Golgi-rich fraction from rat liver
journal, August 1970

  • Leelavathi, D. E.; Estes, L. W.; Feingold, David Sidney
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 211, Issue 2
  • DOI: 10.1016/0005-2736(70)90087-8

Isolation and structural characterisation of pectin from endocarp of Citrus depressa
journal, March 2008


Regiospecific Acetylation of Xylan is Mediated by a Group of DUF231-Containing O-Acetyltransferases
journal, October 2017

  • Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng-Hua
  • Plant and Cell Physiology, Vol. 58, Issue 12
  • DOI: 10.1093/pcp/pcx147

Characterization of O-acetyl-(4-O-methylglucurono)xylan isolated from birch and beech
journal, February 2002


New Insights Into Wall Polysaccharide O-Acetylation
journal, August 2018


Location of the O-acetyl substituents on a nonasaccharide repeating unit of sycamore extracellular xyloglucan
journal, February 1988


Substrate Specificity, Mode of Action, and of Inhibition by Organic Acids of Purified Acetylesterase from Sclerotinia Fungus
journal, May 1967


Substrate Specificity and Kinetic Characterization of Peptidoglycan O -Acetyltransferase B from Neisseria gonorrhoeae
journal, May 2014

  • Moynihan, Patrick J.; Clarke, Anthony J.
  • Journal of Biological Chemistry, Vol. 289, Issue 24
  • DOI: 10.1074/jbc.M114.567388

Secondary Cell Walls: Biosynthesis, Patterned Deposition and Transcriptional Regulation
journal, October 2014

  • Zhong, Ruiqin; Ye, Zheng-Hua
  • Plant and Cell Physiology, Vol. 56, Issue 2
  • DOI: 10.1093/pcp/pcu140

Molecular Characterization of a Heteromeric ATP-Citrate Lyase That Generates Cytosolic Acetyl-Coenzyme A in Arabidopsis
journal, October 2002

  • Fatland, Beth L.; Ke, Jinshan; Anderson, Marc D.
  • Plant Physiology, Vol. 130, Issue 2
  • DOI: 10.1104/pp.008110

SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis
journal, November 2006


Cytosolic acetyl-CoA promotes histone acetylation predominantly at H3K27 in Arabidopsis
journal, September 2017


Cas1p is a membrane protein necessary for the O-acetylation of the Cryptococcus neoformans capsular polysaccharide
journal, October 2001


A group of Populus trichocarpa DUF231 proteins exhibit differential O-acetyltransferase activities toward xylan
journal, April 2018


9-O-Acetylation of sialic acids is catalysed by CASD1 via a covalent acetyl-enzyme intermediate
journal, July 2015

  • Baumann, Anna-Maria T.; Bakkers, Mark J. G.; Buettner, Falk F. R.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms8673

The biomass distribution on Earth
journal, May 2018

  • Bar-On, Yinon M.; Phillips, Rob; Milo, Ron
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 25
  • DOI: 10.1073/pnas.1711842115

Natural acetylation impacts carbohydrate recovery during deconstruction of Populus trichocarpa wood
journal, February 2017


Identification and Characterization of O -Acetylpeptidoglycan Esterase:  A Novel Enzyme Discovered in Neisseria gonorrhoeae
journal, January 2006

  • Weadge, Joel T.; Clarke, Anthony J.
  • Biochemistry, Vol. 45, Issue 3
  • DOI: 10.1021/bi051679s

Biosynthesis of the Plant Cell Wall Matrix Polysaccharide Xyloglucan
journal, April 2016


P. aeruginosa SGNH Hydrolase-Like Proteins AlgJ and AlgX Have Similar Topology but Separate and Distinct Roles in Alginate Acetylation
journal, August 2014


O-Acetylated Oligosaccharides from Pectins of Potato Tuber Cell Walls
journal, April 1997


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


The protein acetylome and the regulation of metabolism
journal, July 2012


A xylosyltransferase that synthesizes β-(1→4)-xylans in wheat (Triticum aestivum L.) seedlings
journal, June 2001


Colony Organization in the Green Alga Botryococcus braunii (Race B) Is Specified by a Complex Extracellular Matrix
journal, August 2012

  • Weiss, Taylor L.; Roth, Robyn; Goodson, Carrie
  • Eukaryotic Cell, Vol. 11, Issue 12
  • DOI: 10.1128/EC.00184-12

Disruption of Cortical Microtubules by Overexpression of Green Fluorescent Protein-Tagged alpha-Tubulin 6 Causes a Marked Reduction in Cell Wall Synthesis
journal, January 2006


Three Arabidopsis DUF579 Domain-Containing GXM Proteins are Methyltransferases Catalyzing 4-O-Methylation of Glucuronic Acid on Xylan
journal, October 2012

  • Lee, C.; Teng, Q.; Zhong, R.
  • Plant and Cell Physiology, Vol. 53, Issue 11
  • DOI: 10.1093/pcp/pcs138

Isolation and characterization of O-acetylated glucomannans from aspen and birch wood
journal, March 2003


Biochemical characterization of rice xylan O-acetyltransferases
journal, March 2018


Reduced Wall Acetylation Proteins Play Vital and Distinct Roles in Cell Wall O -Acetylation in Arabidopsis
journal, September 2013

  • Manabe, Yuzuki; Verhertbruggen, Yves; Gille, Sascha
  • Plant Physiology, Vol. 163, Issue 3
  • DOI: 10.1104/pp.113.225193

The Role of the Plant-Specific ALTERED XYLOGLUCAN9 Protein in Arabidopsis Cell Wall Polysaccharide O- Acetylation
journal, February 2015

  • Schultink, Alex; Naylor, Dan; Dama, Murali
  • Plant Physiology, Vol. 167, Issue 4
  • DOI: 10.1104/pp.114.256479

A Xyloglucan Backbone 6-O-Acetyltransferase from Brachypodium distachyon Modulates Xyloglucan Xylosylation
journal, April 2016


In vitro characterization of the antivirulence target of Gram-positive pathogens, peptidoglycan O-acetyltransferase A (OatA)
journal, October 2017


Mutations of Arabidopsis TBL32 and TBL33 Affect Xylan Acetylation and Secondary Wall Deposition
journal, January 2016


Xylan O-Acetylation Impacts Xylem Development and Enzymatic Recalcitrance as Indicated by the Arabidopsis Mutant tbl29
journal, July 2013

  • Xiong, Guangyan; Cheng, Kun; Pauly, Markus
  • Molecular Plant, Vol. 6, Issue 4
  • DOI: 10.1093/mp/sst014

O -Acetylation of Arabidopsis Hemicellulose Xyloglucan Requires AXY4 or AXY4L, Proteins with a TBL and DUF231 Domain
journal, November 2011

  • Gille, Sascha; de Souza, Amancio; Xiong, Guangyan
  • The Plant Cell, Vol. 23, Issue 11
  • DOI: 10.1105/tpc.111.091728

The Arabidopsis DUF231 Domain-Containing Protein ESK1 Mediates 2-O- and 3-O-Acetylation of Xylosyl Residues in Xylan
journal, May 2013

  • Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
  • Plant and Cell Physiology, Vol. 54, Issue 7
  • DOI: 10.1093/pcp/pct070

Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants
journal, June 2019

  • Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng‐Hua
  • New Phytologist, Vol. 224, Issue 1
  • DOI: 10.1111/nph.15988

TBL3 and TBL31, Two Arabidopsis DUF231 Domain Proteins, are Required for 3- O -Monoacetylation of Xylan
journal, November 2015

  • Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
  • Plant and Cell Physiology, Vol. 57, Issue 1
  • DOI: 10.1093/pcp/pcv172

Two Arabidopsis proteins synthesize acetylated xylan in vitro
journal, September 2014

  • Urbanowicz, Breeanna R.; Peña, Maria J.; Moniz, Heather A.
  • The Plant Journal, Vol. 80, Issue 2
  • DOI: 10.1111/tpj.12643

Characterization of pectin methyltransferase from soybean hypocotyls
journal, April 2000


TBL10 is required for O -acetylation of pectic rhamnogalacturonan-I in Arabidopsis thaliana
journal, September 2018

  • Stranne, Maria; Ren, Yanfang; Fimognari, Lorenzo
  • The Plant Journal, Vol. 96, Issue 4
  • DOI: 10.1111/tpj.14067

Reverse Genetic Characterization of Cytosolic Acetyl-CoA Generation by ATP-Citrate Lyase in Arabidopsis
journal, December 2004

  • Fatland, Beth L.; Nikolau, Basil J.; Wurtele, Eve Syrkin
  • The Plant Cell, Vol. 17, Issue 1
  • DOI: 10.1105/tpc.104.026211

Structural and Functional Characterization of Pseudomonas aeruginosa AlgX : ROLE OF AlgX IN ALGINATE ACETYLATION
journal, June 2013

  • Riley, Laura M.; Weadge, Joel T.; Baker, Perrin
  • Journal of Biological Chemistry, Vol. 288, Issue 31
  • DOI: 10.1074/jbc.M113.484931