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

Abstract

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, XYS1/IRX10 in plants, IRX7, IRX8, IRX9, IRX14 and GUX occurred for the first time in charophyte algae. An XYS1/IRX10 ortholog from Klebsormidium flaccidum, designated K. flaccidumXYLAN SYNTHASE-1 (KfXYS1), possesses 1,4-β-xylan synthase activity, and 1,4-β-xylan occurs in the K. flaccidum cell wall. Finally, 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.

Authors:
 [1];  [2];  [3];  [3];  [4];  [5];  [4];  [3];  [6];  [7];  [8];  [5];  [9];  [10];  [2];  [5];  [4];  [3]
  1. Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology; Michigan State Univ., East Lansing, MI (United States). DOE Great Lakes Bioenergy Research Center
  2. Univ. of Cambridge (United Kingdom). Dept. of Biochemistry
  3. Carlsberg Research Lab., Copenhagen (Denmark)
  4. 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)
  5. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  6. Univ. of Copenhagen (Denmark). Dept. of Plant and Environmental Sciences
  7. Univ. zu Koln (Germany). Botanical Inst., Dept. of Biological Sciences
  8. BGI-Shenzhen, Shenzhen, Guangdong (China)
  9. Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology; Michigan State Univ., East Lansing, MI (United States). DOE Great Lakes Bioenergy Research Center; Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology
  10. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1425434
DOE Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 218; Journal Issue: 3; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biosynthesis; cell wall; evolution; IRX10; Klebsormidium flaccidum; Klebsormidium nitens; xylan; XYS1

Citation Formats

Jensen, Jacob Kruger, Busse-Wicher, Marta, Poulsen, Christian Peter, Fangel, Jonatan Ulrik, Smith, Peter James, Yang, Jeong-Yeh, Peña, Maria-Jesus, Dinesen, Malene Hessellund, Martens, Helle Juel, Melkonian, Michael, Wong, Gane Ka-Shu, Moremen, Kelley W., Wilkerson, Curtis Gene, Scheller, Henrik Vibe, Dupree, Paul, Ulvskov, Peter, Urbanowicz, Breeanna Rae, and Harholt, Jesper. Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis. United States: N. p., 2018. Web. doi:10.1111/nph.15050.
Jensen, Jacob Kruger, Busse-Wicher, Marta, Poulsen, Christian Peter, Fangel, Jonatan Ulrik, Smith, Peter James, Yang, Jeong-Yeh, Peña, Maria-Jesus, Dinesen, Malene Hessellund, Martens, Helle Juel, Melkonian, Michael, Wong, Gane Ka-Shu, Moremen, Kelley W., Wilkerson, Curtis Gene, Scheller, Henrik Vibe, Dupree, Paul, Ulvskov, Peter, Urbanowicz, Breeanna Rae, & Harholt, Jesper. Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis. United States. doi:10.1111/nph.15050.
Jensen, Jacob Kruger, Busse-Wicher, Marta, Poulsen, Christian Peter, Fangel, Jonatan Ulrik, Smith, Peter James, Yang, Jeong-Yeh, Peña, Maria-Jesus, Dinesen, Malene Hessellund, Martens, Helle Juel, Melkonian, Michael, Wong, Gane Ka-Shu, Moremen, Kelley W., Wilkerson, Curtis Gene, Scheller, Henrik Vibe, Dupree, Paul, Ulvskov, Peter, Urbanowicz, Breeanna Rae, and Harholt, Jesper. Tue . "Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis". United States. doi:10.1111/nph.15050. https://www.osti.gov/servlets/purl/1425434.
@article{osti_1425434,
title = {Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis},
author = {Jensen, Jacob Kruger and Busse-Wicher, Marta and Poulsen, Christian Peter and Fangel, Jonatan Ulrik and Smith, Peter James and Yang, Jeong-Yeh and Peña, Maria-Jesus and Dinesen, Malene Hessellund and Martens, Helle Juel and Melkonian, Michael and Wong, Gane Ka-Shu and Moremen, Kelley W. and Wilkerson, Curtis Gene and Scheller, Henrik Vibe and Dupree, Paul and Ulvskov, Peter and Urbanowicz, Breeanna Rae and Harholt, Jesper},
abstractNote = {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, XYS1/IRX10 in plants, IRX7, IRX8, IRX9, IRX14 and GUX occurred for the first time in charophyte algae. An XYS1/IRX10 ortholog from Klebsormidium flaccidum, designated K. flaccidumXYLAN SYNTHASE-1 (KfXYS1), possesses 1,4-β-xylan synthase activity, and 1,4-β-xylan occurs in the K. flaccidum cell wall. Finally, 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.},
doi = {10.1111/nph.15050},
journal = {New Phytologist},
issn = {0028-646X},
number = 3,
volume = 218,
place = {United States},
year = {2018},
month = {2}
}