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

Title: Functional Characterization of UDP-apiose Synthases from Bryophytes and Green Algae Provides Insight into the Appearance of Apiose-containing Glycans during Plant Evolution

Abstract

Apiose is a branched monosaccharide that is found in the cell wall pectic polysaccharides rhamnogalacturonan II and apiogalacturonan and in numerous plant secondary metabolites. These apiose-containing glycans are synthesized using UDP-apiose as the donor. UDP-apiose (UDP-Api) together with UDP-xylose is formed from UDP-glucuronic acid (UDP-GlcA) by UDP-Api synthase (UAS). It was hypothesized that the ability to form Api distinguishes vascular plants from the avascular plants and green algae. UAS from several dicotyledonous plants has been characterized; however, it is not known if avascular plants or green algae produce this enzyme. Here we report the identification and functional characterization of UAS homologs from avascular plants (mosses, liverwort, and hornwort), from streptophyte green algae, and from a monocot (duckweed). The recombinant UAS homologs all form UDP-Api from UDP-glucuronic acid albeit in different amounts. Apiose was detected in aqueous methanolic extracts of these plants. Apiose was detected in duckweed cell walls but not in the walls of the avascular plants and algae. Overexpressing duckweed UAS in the moss Physcomitrella patens led to an increase in the amounts of aqueous methanol-acetonitrile-soluble apiose but did not result in discernible amounts of cell wall-associated apiose. Thus, bryophytes and algae likely lack the glycosyltransferase machinery required tomore » synthesize apiose-containing cell wall glycans. Yet, these plants may have the ability to form apiosylated secondary metabolites. Our data are the first to provide evidence that the ability to form apiose existed prior to the appearance of rhamnogalacturonan II and apiogalacturonan and provide new insights into the evolution of apiose-containing glycans.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
OSTI Identifier:
1769193
Alternate Identifier(s):
OSTI ID: 1535357
Grant/Contract Number:  
FG02-12ER16324 & DE-FG02–12ER16326; SC0008472; FG02-93ER20097; FG02-12ER16324; FG02-12ER16326
Resource Type:
Published Article
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Name: Journal of Biological Chemistry Journal Volume: 291 Journal Issue: 41; Journal ID: ISSN 0021-9258
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; algae; decarboxylase; glycosyltransferase; plant cell wall; vascular

Citation Formats

Smith, James, Yang, Yiwen, Levy, Shahar, Adelusi, Oluwatoyin Oluwayemi, Hahn, Michael G., O'Neill, Malcolm A., and Bar-Peled, Maor. Functional Characterization of UDP-apiose Synthases from Bryophytes and Green Algae Provides Insight into the Appearance of Apiose-containing Glycans during Plant Evolution. United States: N. p., 2016. Web. doi:10.1074/jbc.M116.749069.
Smith, James, Yang, Yiwen, Levy, Shahar, Adelusi, Oluwatoyin Oluwayemi, Hahn, Michael G., O'Neill, Malcolm A., & Bar-Peled, Maor. Functional Characterization of UDP-apiose Synthases from Bryophytes and Green Algae Provides Insight into the Appearance of Apiose-containing Glycans during Plant Evolution. United States. https://doi.org/10.1074/jbc.M116.749069
Smith, James, Yang, Yiwen, Levy, Shahar, Adelusi, Oluwatoyin Oluwayemi, Hahn, Michael G., O'Neill, Malcolm A., and Bar-Peled, Maor. Sat . "Functional Characterization of UDP-apiose Synthases from Bryophytes and Green Algae Provides Insight into the Appearance of Apiose-containing Glycans during Plant Evolution". United States. https://doi.org/10.1074/jbc.M116.749069.
@article{osti_1769193,
title = {Functional Characterization of UDP-apiose Synthases from Bryophytes and Green Algae Provides Insight into the Appearance of Apiose-containing Glycans during Plant Evolution},
author = {Smith, James and Yang, Yiwen and Levy, Shahar and Adelusi, Oluwatoyin Oluwayemi and Hahn, Michael G. and O'Neill, Malcolm A. and Bar-Peled, Maor},
abstractNote = {Apiose is a branched monosaccharide that is found in the cell wall pectic polysaccharides rhamnogalacturonan II and apiogalacturonan and in numerous plant secondary metabolites. These apiose-containing glycans are synthesized using UDP-apiose as the donor. UDP-apiose (UDP-Api) together with UDP-xylose is formed from UDP-glucuronic acid (UDP-GlcA) by UDP-Api synthase (UAS). It was hypothesized that the ability to form Api distinguishes vascular plants from the avascular plants and green algae. UAS from several dicotyledonous plants has been characterized; however, it is not known if avascular plants or green algae produce this enzyme. Here we report the identification and functional characterization of UAS homologs from avascular plants (mosses, liverwort, and hornwort), from streptophyte green algae, and from a monocot (duckweed). The recombinant UAS homologs all form UDP-Api from UDP-glucuronic acid albeit in different amounts. Apiose was detected in aqueous methanolic extracts of these plants. Apiose was detected in duckweed cell walls but not in the walls of the avascular plants and algae. Overexpressing duckweed UAS in the moss Physcomitrella patens led to an increase in the amounts of aqueous methanol-acetonitrile-soluble apiose but did not result in discernible amounts of cell wall-associated apiose. Thus, bryophytes and algae likely lack the glycosyltransferase machinery required to synthesize apiose-containing cell wall glycans. Yet, these plants may have the ability to form apiosylated secondary metabolites. Our data are the first to provide evidence that the ability to form apiose existed prior to the appearance of rhamnogalacturonan II and apiogalacturonan and provide new insights into the evolution of apiose-containing glycans.},
doi = {10.1074/jbc.M116.749069},
journal = {Journal of Biological Chemistry},
number = 41,
volume = 291,
place = {United States},
year = {Sat Oct 01 00:00:00 EDT 2016},
month = {Sat Oct 01 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1074/jbc.M116.749069

Citation Metrics:
Cited by: 12 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Real-time NMR monitoring of intermediates and labile products of the bifunctional enzyme UDP-apiose/UDP-xylose synthase
journal, June 2009


Branched-chain Sugars and Sugar Alcohols
book, January 1990


Man o’ War Mutation in UDP-α- d -Xylose Synthase Favors the Abortive Catalytic Cycle and Uncovers a Latent Potential for Hexamer Formation
journal, January 2015

  • Walsh, Richard M.; Polizzi, Samuel J.; Kadirvelraj, Renuka
  • Biochemistry, Vol. 54, Issue 3
  • DOI: 10.1021/bi501357c

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

Apiose: one of nature's witty games
journal, February 2016

  • Pičmanová, Martina; Møller, Birger Lindberg
  • Glycobiology, Vol. 26, Issue 5
  • DOI: 10.1093/glycob/cww012

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

Data access for the 1,000 Plants (1KP) project
journal, October 2014


Structure of Plant Cell Walls: VIII. A New Pectic Polysaccharide
journal, September 1978

  • Darvill, Alan G.; McNeil, Michael; Albersheim, Peter
  • Plant Physiology, Vol. 62, Issue 3
  • DOI: 10.1104/pp.62.3.418

A Transcriptome Atlas of Physcomitrella patens Provides Insights into the Evolution and Development of Land Plants
journal, February 2016

  • Ortiz-Ramírez, Carlos; Hernandez-Coronado, Marcela; Thamm, Anna
  • Molecular Plant, Vol. 9, Issue 2
  • DOI: 10.1016/j.molp.2015.12.002

The biosynthesis of Apiose in parsley (Apium petroselinum L.)
journal, December 1964


Identification of Galacturonic Acid-1-phosphate Kinase, a New Member of the GHMP Kinase Superfamily in Plants, and Comparison with Galactose-1-phosphate Kinase
journal, June 2009

  • Yang, Ting; Bar-Peled, Liron; Gebhart, Lindsay
  • Journal of Biological Chemistry, Vol. 284, Issue 32
  • DOI: 10.1074/jbc.M109.014761

Purification and properties of udpapiose: ( apiosyltransferase from cell suspension cultures of parsley
journal, December 1972

  • Ortmann, Rainer; Sutter, Arne; Grisebach, Hans
  • Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 289, Issue 2
  • DOI: 10.1016/0005-2744(72)90080-0

An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets
journal, August 2007


Isolation and partial characterization of apiogalacturonans from the cell wall of Lemna minor
journal, February 1970

  • Hart, David A.; Kindel, Paul K.
  • Biochemical Journal, Vol. 116, Issue 4
  • DOI: 10.1042/bj1160569

The Plant Cell Wall Polysaccharide Rhamnogalacturonan II Self-assembles into a Covalently Cross-linked Dimer
journal, May 1999

  • Ishii, Tadashi; Matsunaga, Toshiro; Pellerin, Patrice
  • Journal of Biological Chemistry, Vol. 274, Issue 19
  • DOI: 10.1074/jbc.274.19.13098

Purification and cDNA Cloning of UDP-d-Glucuronate Carboxy-lyase (UDP-d-xylose Synthase) from Pea Seedlings
journal, November 2002

  • Kobayashi, Masaru; Nakagawa, Hironobu; Suda, Izumi
  • Plant and Cell Physiology, Vol. 43, Issue 11
  • DOI: 10.1093/pcp/pcf157

Molecular Cloning and Expression of Human UDP-d-Xylose:Proteoglycan Core Protein β-d-Xylosyltransferase and its First Isoform XT-II
journal, December 2000

  • Götting, Christian; Kuhn, Joachim; Zahn, Roland
  • Journal of Molecular Biology, Vol. 304, Issue 4
  • DOI: 10.1006/jmbi.2000.4261

Human UDP-α- d -xylose Synthase and Escherichia coli ArnA Conserve a Conformational Shunt That Controls Whether Xylose or 4-Keto-Xylose Is Produced
journal, October 2012

  • Polizzi, Samuel J.; Walsh, Richard M.; Peeples, William B.
  • Biochemistry, Vol. 51, Issue 44
  • DOI: 10.1021/bi301135b

Two Chains of Rhamnogalacturonan II Are Cross-Linked by Borate-Diol Ester Bonds in Higher Plant Cell Walls
journal, March 1996


First Isolation of Human UDP-d-Xylose: Proteoglycan Core Protein β-d-Xylosyltransferase Secreted from Cultured JAR Choriocarcinoma Cells
journal, November 2000

  • Kuhn, Joachim; Götting, Christian; Schnölzer, Martina
  • Journal of Biological Chemistry, Vol. 276, Issue 7
  • DOI: 10.1074/jbc.M005111200

Oxidative stress and plant secondary metabolism: 6″-O-malonylapiin in parsley
journal, October 1993


Tagged Mutagenesis and Gene-trap in the Moss, Physcomitrella patens by Shuttle Mutagenesis
journal, January 2000


Structural studies of the pectic polysaccharide from duckweed Lemna minor L.
journal, May 2002


Structural Characterization and Cytotoxic Properties of an Apiose-Rich Pectic Polysaccharide Obtained from the Cell Wall of the Marine Phanerogam Zostera marina
journal, June 2010

  • Gloaguen, Vincent; Brudieux, Véronique; Closs, Brigitte
  • Journal of Natural Products, Vol. 73, Issue 6
  • DOI: 10.1021/np100092c

Rhamnogalacturonan-II, a Pectic Polysaccharide in the Walls of Growing Plant Cell, Forms a Dimer That Is Covalently Cross-linked by a Borate Ester
journal, September 1996

  • O'Neill, Malcolm A.; Warrenfeltz, Dennis; Kates, Keith
  • Journal of Biological Chemistry, Vol. 271, Issue 37
  • DOI: 10.1074/jbc.271.37.22923

Isolation and characterization of plant cell walls and cell wall components
book, January 1986


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


Boron in Plants: Deficiency and Toxicity
journal, October 2008

  • Camacho-Cristóbal, Juan J.; Rexach, Jesús; González-Fontes, Agustín
  • Journal of Integrative Plant Biology, Vol. 50, Issue 10
  • DOI: 10.1111/j.1744-7909.2008.00742.x

Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp
journal, April 1996


Developmental Control of Apiogalacturonan Biosynthesis and UDP-Apiose Production in a Duckweed
journal, July 1989

  • Longland, Jane M.; Fry, Stephen C.; Trewavas, Anthony J.
  • Plant Physiology, Vol. 90, Issue 3
  • DOI: 10.1104/pp.90.3.972

Analysis of UDP- d -Apiose/UDP- d -Xylose Synthase-Catalyzed Conversion of UDP- d -Apiose Phosphonate to UDP- d -Xylose Phosphonate: Implications for a Retroaldol–Aldol Mechanism
journal, August 2012

  • Choi, Sei-hyun; Mansoorabadi, Steven O.; Liu, Yung-nan
  • Journal of the American Chemical Society, Vol. 134, Issue 34
  • DOI: 10.1021/ja305322x

In-microbe formation of nucleotide sugars in engineered Escherichia coli
journal, February 2012

  • Yang, Ting; Bar-Peled, Yael; Smith, James Amor
  • Analytical Biochemistry, Vol. 421, Issue 2
  • DOI: 10.1016/j.ab.2011.12.028

Ubiquity of a Borate-Rhamnogalacturonan II Complex in the Cell Walls of Higher Plants
journal, July 1996


Profilin Is Essential for Tip Growth in the Moss Physcomitrella patens
journal, November 2007

  • Vidali, Luis; Augustine, Robert C.; Kleinman, Ken P.
  • The Plant Cell, Vol. 19, Issue 11
  • DOI: 10.1105/tpc.107.053413

Analysis Tool Web Services from the EMBL-EBI
journal, May 2013

  • McWilliam, Hamish; Li, Weizhong; Uludag, Mahmut
  • Nucleic Acids Research, Vol. 41, Issue W1
  • DOI: 10.1093/nar/gkt376

Dendroscope 3: An Interactive Tool for Rooted Phylogenetic Trees and Networks
journal, September 2012


The Pore Size of Non-Graminaceous Plant Cell Walls Is Rapidly Decreased by Borate Ester Cross-Linking of the Pectic Polysaccharide Rhamnogalacturonan II
journal, November 1999

  • Fleischer, Axel; O'Neill, Malcolm A.; Ehwald, Rudolf
  • Plant Physiology, Vol. 121, Issue 3
  • DOI: 10.1104/pp.121.3.829

Significance of Flavonoids in Plant Resistance and Enhancement of Their Biosynthesis
journal, November 2005


Biosynthesis of d-apiose IV. Formation of UDP-apiose from UDP-d-glucuronic acid in cell-free extracts of parsley (Apium petroselinum L.) and Lemna minor
journal, October 1968

  • Sandermann, H.; Tisue, G. T.; Grisebach, H.
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 165, Issue 3
  • DOI: 10.1016/0304-4165(68)90239-0

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


Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

The EMBL-EBI bioinformatics web and programmatic tools framework
journal, April 2015

  • Li, Weizhong; Cowley, Andrew; Uludag, Mahmut
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv279

Depletion of UDP-d-apiose/UDP-d-xylose Synthases Results in Rhamnogalacturonan-II Deficiency, Cell Wall Thickening, and Cell Death in Higher Plants
journal, March 2006

  • Ahn, Joon-Woo; Verma, Rajeev; Kim, Moonil
  • Journal of Biological Chemistry, Vol. 281, Issue 19
  • DOI: 10.1074/jbc.M512403200

Plant chemical defense: at what cost?
journal, May 2013


Composition and Synthesis of the Pectin and Protein Components of the cell wall of Closterium Acerosum (Chlorophyta)
journal, October 2001


The Synthesis and Origin of the Pectic Polysaccharide Rhamnogalacturonan II – Insights from Nucleotide Sugar Formation and Diversity
journal, January 2012

  • Bar-Peled, Maor; Urbanowicz, Breeanna R.; O’Neill, Malcolm A.
  • Frontiers in Plant Science, Vol. 3
  • DOI: 10.3389/fpls.2012.00092

Evolutionary Divergence of Plant Borate Exporters and Critical Amino Acid Residues for the Polar Localization and Boron-Dependent Vacuolar Sorting of AtBOR1
journal, January 2015

  • Wakuta, Shinji; Mineta, Katsuhiko; Amano, Taro
  • Plant and Cell Physiology, Vol. 56, Issue 5
  • DOI: 10.1093/pcp/pcv011

Evolution of Plant Nucleotide-Sugar Interconversion Enzymes
journal, November 2011


Works referencing / citing this record:

Deciphering the enzymatic mechanism of sugar ring contraction in UDP-apiose biosynthesis
journal, November 2019


Identification of an apiosyltransferase in the plant pathogen Xanthomonas pisi
journal, October 2018