skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.15050· OSTI ID:1630145
 [1];  [2];  [3];  [3];  [4];  [5];  [4];  [3];  [6];  [7];  [8];  [5];  [9];  [10];  [2];  [5];  [4];  [3]
  1. Department of Plant Biology Michigan State University East Lansing MI 48823 USA, DOE Great Lakes Bioenergy Research Center Michigan State University East Lansing MI 48823 USA
  2. Department of Biochemistry University of Cambridge Cambridge CB2 1QW UK
  3. Carlsberg Research Laboratory 1799 Copenhagen V Denmark
  4. Complex Carbohydrate Research Center University of Georgia 315 Riverbend Road Athens GA 30602 USA, BioEnergy Science Center Oak Ridge National Lab Laboratory Oak Ridge TN 37831 USA
  5. Complex Carbohydrate Research Center University of Georgia 315 Riverbend Road Athens GA 30602 USA
  6. Department of Plant and Environmental Sciences University of Copenhagen 1971 Frederiksberg C Denmark
  7. Botanical Institute Department of Biological Sciences Universität zu Köln Köln D‐50674 Germany
  8. BGI‐Shenzhen Beishan Industrial Zone Yantian District Shenzhen 518083 China
  9. Department of Plant Biology Michigan State University East Lansing MI 48823 USA, DOE Great Lakes Bioenergy Research Center Michigan State University East Lansing MI 48823 USA, Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI 48824 USA
  10. Joint BioEnergy Institute Emeryville CA 94608 USA, Environmental Genomics and Systems Biology Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA

Summary Insights into the evolution of plant cell walls have important implications for comprehending these diverse and abundant biological structures. In order to understand the evolving structure–function relationships of the plant cell wall, it is imperative to trace the origin of its different components. The present study is focused on plant 1,4‐β‐xylan, tracing its evolutionary origin by genome and transcriptome mining followed by phylogenetic analysis, utilizing a large selection of plants and algae. It substantiates the findings by heterologous expression and biochemical characterization of a charophyte alga xylan synthase. Of the 12 known gene classes involved in 1,4‐β‐xylan formation, XYS 1/ IRX 10 in plants, IRX 7, IRX 8, IRX 9, IRX 14 and GUX occurred for the first time in charophyte algae. An XYS 1/ IRX 10 ortholog from Klebsormidium flaccidum , designated K. flaccidum XYLAN SYNTHASE ‐1 ( Kf XYS 1), possesses 1,4‐β‐xylan synthase activity, and 1,4‐β‐xylan occurs in the K. flaccidum cell wall. These data suggest that plant 1,4‐β‐xylan originated in charophytes and shed light on the origin of one of the key cell wall innovations to occur in charophyte algae, facilitating terrestrialization and emergence of polysaccharide‐based plant cell walls.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1630145
Alternate ID(s):
OSTI ID: 1425434
Journal Information:
New Phytologist, Journal Name: New Phytologist Vol. 218 Journal Issue: 3; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English
Citation Metrics:
Cited by: 43 works
Citation information provided by
Web of Science

References (52)

The location of (1?3)-?-glucans in the walls of pollen tubes of Nicotiana alata using a (1?3)-?-glucan-specific monoclonal antibody journal August 1991
Hemicelluloses journal June 2010
Phylotranscriptomic analysis of the origin and early diversification of land plants journal October 2014
Monoclonal Antibodies to Plant Cell Wall Xylans and Arabinoxylans journal April 2005
SALAD database: a motif-based database of protein annotations for plant comparative genomics journal October 2009
Xylan biosynthesis journal April 2014
The charophycean green algae provide insights into the early origins of plant cell walls journal August 2011
HMDB: a knowledgebase for the human metabolome journal January 2009
Correlative Imaging of Fluorescent Proteins in Resin-Embedded Plant Material 1 journal March 2013
GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns journal March 2013
Why Plants Were Terrestrial from the Beginning journal February 2016
Data access for the 1,000 Plants (1KP) project journal October 2014
Classification, Naming and Evolutionary History of Glycosyltransferases from Sequenced Green and Red Algal Genomes journal October 2013
Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism journal August 2017
An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14 journal June 2015
Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth journal January 1993
Arabidopsis irregular xylem8 and irregular xylem9 : Implications for the Complexity of Glucuronoxylan Biosynthesis journal February 2007
Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose journal June 2016
Cell wall evolution and diversity journal January 2012
Designer biomass for next-generation biorefineries: leveraging recent insights into xylan structure and biosynthesis journal November 2017
Site-Directed Mutagenesis of IRX9, IRX9L and IRX14 Proteins Involved in Xylan Biosynthesis: Glycosyltransferase Activity Is Not Required for IRX9 Function in Arabidopsis journal August 2014
Discovery of diversity in xylan biosynthetic genes by transcriptional profiling of a heteroxylan containing mucilaginous tissue journal January 2013
The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis: A DUF579 protein affects xylan accumulation journal February 2011
Asparagus IRX9, IRX10, and IRX14A Are Components of an Active Xylan Backbone Synthase Complex that Forms in the Golgi Apparatus journal March 2016
Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis journal December 2007
Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae journal September 2014
Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures journal May 2004
Versatile High Resolution Oligosaccharide Microarrays for Plant Glycobiology and Cell Wall Research journal September 2012
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils? journal October 2004
2-Keto-Sugar Acids in Green Flagellates: a Chemical Marker for Prasinophycean Scales1,2 journal August 1991
Basket scales of the green alga, Mesostigma viride: Chemistry and ultrastructure journal October 1991
4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein journal August 2012
Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses journal January 2012
Evidence That GH115 α-Glucuronidase Activity, Which Is Required to Degrade Plant Biomass, Is Dependent on Conformational Flexibility journal November 2013
Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature journal January 2015
β-d-(1→4), β-d-(1→3) ‘mixed linkage’ xylans from red seaweeds of the order Nemaliales and Palmariales journal June 2011
The structure and biochemistry of charophycean cell walls: I. Pectins of Penium margaritaceum journal November 2006
Overexpression of a BAHD Acyltransferase, OsAt10 , Alters Rice Cell Wall Hydroxycinnamic Acid Content and Saccharification journal February 2013
Enzymatic Basis for N -Glycan Sialylation : STRUCTURE OF RAT α2,6-SIALYLTRANSFERASE (ST6GAL1) REVEALS CONSERVED AND UNIQUE FEATURES FOR GLYCAN SIALYLATION journal October 2013
The Glycosyltransferase Repertoire of the Spikemoss Selaginella moellendorffii and a Comparative Study of Its Cell Wall journal May 2012
Biosynthesis of UDP-Xylose. Cloning and Characterization of a Novel Arabidopsis Gene Family, UXS , Encoding Soluble and Putative Membrane-Bound UDP-Glucuronic Acid Decarboxylase Isoforms journal December 2002
Insoluble (1 → 3), (1 → 4)-β-D-glucan is a component of cell walls in brown algae (Phaeophyceae) and is masked by alginates in tissues journal June 2017
Monoclonal antibodies indicate low-abundance links between heteroxylan and other glycans of plant cell walls journal July 2015
Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation journal May 2014
Arabidopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases journal September 2014
Two Arabidopsis proteins synthesize acetylated xylan in vitro journal September 2014
Polysaccharide Analysis Using Carbohydrate Gel Electrophoresis: A Method to Study Plant Cell Wall Polysaccharides and Polysaccharide Hydrolases journal January 2002
The ability of land plants to synthesize glucuronoxylans predates the evolution of tracheophytes journal November 2011
Three Members of the Arabidopsis Glycosyltransferase Family 8 Are Xylan Glucuronosyltransferases journal June 2012
Arabidopsis genes IRREGULAR XYLEM (IRX15) and IRX15L encode DUF579-containing proteins that are essential for normal xylan deposition in the secondary cell wall: DUF579 and xylan biosynthesis journal February 2011
Fluorescent labeling of pectic oligosaccharides with 2-aminobenzamide and enzyme assay for pectin journal June 2002
XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan journal October 2012