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

Title: Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants

Abstract

Summary Mannans are an abundant cell wall polysaccharide in bryophytes, seedless vascular plants and gymnosperms. A previous study has shown that mannan acetylation in Arabidopsis and konjac is mediated by mannan O ‐acetyltransferases belonging to the Domain of Unknown Function ( DUF ) 231 family. However, little is known about the acetylation patterns of mannans in bryophytes and seedless vascular plants, and the evolutionary origin of mannan O ‐acetyltransferases in land plants has not yet been studied. Phylogenetic analysis of the DUF 231 family revealed that DUF 231 members were present in the charophycean green algae and evolved to form overlapped and divergent phylogenetic groups in different taxa of land plants. Acetyltransferase activity assays of recombinant proteins demonstrated that a number of group II DUF 231 members from moss, Selaginella , pine, spruce, rice and poplar were mannan 2‐ O ‐ and 3‐ O ‐acetyltransferases, whereas the two group I DUF 231 members from the alga Klebsormidium nitens were not. Structural analysis of mannans from moss and Selaginella showed they were composed of mannosyl and glucosyl residues and the mannosyl residues were acetylated at O ‐2 and O ‐3. These findings indicate that although the DUF 231 genes originated inmore » algae, their recruitment as mannan O ‐acetyltransferases probably occurred in bryophytes, and the biochemical functions of these O ‐acetyltransferases are evolutionarily conserved throughout land plants.« less

Authors:
 [1];  [2]; 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
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1543044
Grant/Contract Number:  
DE‐FG02‐03ER15415
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Name: New Phytologist Journal Volume: 224 Journal Issue: 1; Journal ID: ISSN 0028-646X
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Zhong, Ruiqin, Cui, Dongtao, and Ye, Zheng‐Hua. Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants. United Kingdom: N. p., 2019. Web. doi:10.1111/nph.15988.
Zhong, Ruiqin, Cui, Dongtao, & Ye, Zheng‐Hua. Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants. United Kingdom. https://doi.org/10.1111/nph.15988
Zhong, Ruiqin, Cui, Dongtao, and Ye, Zheng‐Hua. Thu . "Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants". United Kingdom. https://doi.org/10.1111/nph.15988.
@article{osti_1543044,
title = {Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants},
author = {Zhong, Ruiqin and Cui, Dongtao and Ye, Zheng‐Hua},
abstractNote = {Summary Mannans are an abundant cell wall polysaccharide in bryophytes, seedless vascular plants and gymnosperms. A previous study has shown that mannan acetylation in Arabidopsis and konjac is mediated by mannan O ‐acetyltransferases belonging to the Domain of Unknown Function ( DUF ) 231 family. However, little is known about the acetylation patterns of mannans in bryophytes and seedless vascular plants, and the evolutionary origin of mannan O ‐acetyltransferases in land plants has not yet been studied. Phylogenetic analysis of the DUF 231 family revealed that DUF 231 members were present in the charophycean green algae and evolved to form overlapped and divergent phylogenetic groups in different taxa of land plants. Acetyltransferase activity assays of recombinant proteins demonstrated that a number of group II DUF 231 members from moss, Selaginella , pine, spruce, rice and poplar were mannan 2‐ O ‐ and 3‐ O ‐acetyltransferases, whereas the two group I DUF 231 members from the alga Klebsormidium nitens were not. Structural analysis of mannans from moss and Selaginella showed they were composed of mannosyl and glucosyl residues and the mannosyl residues were acetylated at O ‐2 and O ‐3. These findings indicate that although the DUF 231 genes originated in algae, their recruitment as mannan O ‐acetyltransferases probably occurred in bryophytes, and the biochemical functions of these O ‐acetyltransferases are evolutionarily conserved throughout land plants.},
doi = {10.1111/nph.15988},
journal = {New Phytologist},
number = 1,
volume = 224,
place = {United Kingdom},
year = {Thu Jul 18 00:00:00 EDT 2019},
month = {Thu Jul 18 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/nph.15988

Citation Metrics:
Cited by: 17 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage
journal, July 2015

  • Voiniciuc, Cătălin; Schmidt, Maximilian Heinrich-Wilhelm; Berger, Adeline
  • Plant Physiology, Vol. 169, Issue 1
  • DOI: 10.1104/pp.15.00851

Spectroscopic and Biochemical Analysis of Regions of the Cell Wall of the Unicellular 'Mannan Weed', Acetabularia acetabulum
journal, December 2006

  • Dunn, E. K.; Shoue, D. A.; Huang, X.
  • Plant and Cell Physiology, Vol. 48, Issue 1
  • DOI: 10.1093/pcp/pcl053

Molecular characterisation of a membrane-bound galactosyltransferase of plant cell wall matrix polysaccharide biosynthesis
journal, September 1999


Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition: PMR5 is required for powdery mildew susceptibility
journal, December 2004


The charophycean green algae provide insights into the early origins of plant cell walls
journal, August 2011


Characterisation of water-soluble galactoglucomannans from Norway spruce wood and thermomechanical pulp
journal, May 2003


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


Evolutionary Conservation of Xylan Biosynthetic Genes in Selaginella moellendorffii and Physcomitrella patens
journal, May 2016

  • Haghighat, Marziyeh; Teng, Quincy; Zhong, Ruiqin
  • Plant and Cell Physiology, Vol. 57, Issue 8
  • DOI: 10.1093/pcp/pcw096

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

Galactoglucomannan from the secondary cell wall of Picea abies L. Karst
journal, November 2000


Interactions between locust bean gum and cellulose characterized by13C n.m.r. spectroscopy
journal, July 1998


Chemical Composition and Structure of the cell Walls of the Conchocelis and Thallus Phases of Porphyra Tenera (Rhodophyceae)1,2
journal, June 1981


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

Identification of an additional protein involved in mannan biosynthesis
journal, October 2012

  • Wang, Yan; Mortimer, Jennifer C.; Davis, Jonathan
  • The Plant Journal, Vol. 73, Issue 1
  • DOI: 10.1111/tpj.12019

Structural analysis of acetylated hemicellulose polysaccharides from fibre flax (Linum usitatissimum L.)
journal, September 1996


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


Isolation and characterization of galactoglucomannan from spruce ( Picea abies )
journal, April 2002


The Cellulose Synthase Gene Superfamily and Biochemical Functions of Xylem-Specific Cellulose Synthase-Like Genes in Populus trichocarpa
journal, September 2006

  • Suzuki, Shiro; Li, Laigeng; Sun, Ying-Hsuan
  • Plant Physiology, Vol. 142, Issue 3
  • DOI: 10.1104/pp.106.086678

Cell wall polysaccharides from fern leaves: Evidence for a mannan-rich Type III cell wall in Adiantum raddianum
journal, December 2011


A galactoglucomannan from the stem tissues of the aquatic moss fontinalis antipyretica
journal, August 1972


Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae
journal, September 2014

  • Mikkelsen, Maria D.; Harholt, Jesper; Ulvskov, Peter
  • Annals of Botany, Vol. 114, Issue 6
  • DOI: 10.1093/aob/mcu171

The Patterned Structure of Galactoglucomannan Suggests It May Bind to Cellulose in Seed Mucilage
journal, September 2018

  • Yu, Li; Lyczakowski, Jan J.; Pereira, Caroline S.
  • Plant Physiology, Vol. 178, Issue 3
  • DOI: 10.1104/pp.18.00709

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


Guar Seed  -Mannan Synthase Is a Member of the Cellulose Synthase Super Gene Family
journal, January 2004


Purification and characterisation of a galactoglucomannan from kiwifruit (Actinidia deliciosa)
journal, April 2001


The hemicelluloses of bracken
journal, December 1971


TRICHOME BIREFRINGENCE and Its Homolog AT5G01360 Encode Plant-Specific DUF231 Proteins Required for Cellulose Biosynthesis in Arabidopsis
journal, April 2010

  • Bischoff, Volker; Nita, Silvia; Neumetzler, Lutz
  • Plant Physiology, Vol. 153, Issue 2
  • DOI: 10.1104/pp.110.153320

Recent progress in the chemistry of wood hemicelluloses
journal, January 1967


NMR and rheological study of Aloe barbadensis partially acetylated glucomannan
journal, April 2013


An acetylated galactoglucomannan from Picea abies L. Karst
journal, June 2002


Acetylation and characterization of spruce (Picea abies) galactoglucomannans
journal, April 2010


Chemical and in situ characterization of macromolecular components of the cell walls from the green seaweed Codium fragile
journal, October 2008

  • Estevez, José Manuel; Fernández, Paula Virginia; Kasulin, Luciana
  • Glycobiology, Vol. 19, Issue 3
  • DOI: 10.1093/glycob/cwn101

Mechanistic insights from plant heteromannan synthesis in yeast
journal, December 2018

  • Voiniciuc, Cătălin; Dama, Murali; Gawenda, Niklas
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 2
  • DOI: 10.1073/pnas.1814003116

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


Polysaccharides in some industrially important softwood species
journal, March 2005


Xyloglucan evolution and the terrestrialization of green plants
journal, May 2018


Primary Cell Wall Composition of Bryophytes and Charophytes
journal, January 2003


NMR structural determination of dissolved O-acetylated galactoglucomannan isolated from spruce thermomechanical pulp
journal, January 2004


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


Polysaccharides in some industrially important hardwood species
journal, October 2005


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


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


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


Beyond the Green: Understanding the Evolutionary Puzzle of Plant and Algal Cell Walls
journal, April 2010


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

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

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

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


Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases
journal, January 2005

  • Liepman, A. H.; Wilkerson, C. G.; Keegstra, K.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 6
  • DOI: 10.1073/pnas.0409179102

Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose
journal, February 1998


Primary cell wall composition of pteridophytes and spermatophytes
journal, July 2004


Isolation and Characterisation of an Acetylated Glucomannan from Pine (Pinus silvestris L.).
journal, January 1961


Cell wall synthesis during growth and maturation of Nitella internodal cells
journal, March 1993

  • Morrison, Janice C.; Greve, L. Carl; Richmond, Paul A.
  • Planta, Vol. 189, Issue 3
  • DOI: 10.1007/BF00194428

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

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

The occurrence of mannan microfibrils in the green algae Codium fragile and Acetabularia crenulata
journal, January 1968


Restricted access of proteins to mannan polysaccharides in intact plant cell walls: Masking of mannan polysaccharides
journal, August 2010