Recent Advances on the Posttranslational Modifications of EXTs and Their Roles in Plant Cell Walls

The genetic set up and the enzymes that define the O-glycosylation sites and transfer the activated sugars to cell wall glycoprotein Extensins (EXTs) have remained unknown for a long time. We are now beginning to see the emerging components of the molecular machinery that assembles these complex O-glycoproteins on the plant cell wall. Genes conferring the posttranslational modifications, i.e., proline hydroxylation and subsequent O-glycosylation, of the EXTs have been recently identified. In this review we summarize the enzymes that define the O-glycosylation sites on the O-glycoproteins, i.e., the prolyl 4-hydroxylases (P4Hs), the glycosyltransferases that transfer arabinose units (named arabinosyltransferases, AraTs), and the one responsible for transferring a single galactose (galactosyltransferase, GalT) on the protein EXT backbones. We discuss the effects of posttranslational modifications on the structure and function of extensins in plant cell walls.

• Publication year

  2012

• Venue

  Frontiers in Plant Science

• Publication date

  2012-05-15

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.3389/fpls.2012.00093PMID 22639676PMCID 3355594
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Identification of Novel Peptidyl Serine α-Galactosyltransferase Gene Family in Plants*♦

  2014influential reference
• Root hair sweet growth

  2011influential reference
• O-Glycosylated Cell Wall Proteins Are Essential in Root Hair Growth

  2011cited by this paper
• The charophycean green algae provide insights into the early origins of plant cell walls.

  2011cited by this paper
• Role of the Extensin Superfamily in Primary Cell Wall Architecture1

  2011influential reference
• Hydroxyproline‐Rich Glycoproteins: Form and Function

  2010influential reference
• The hydroxyproline-rich glycoprotein domain of the Arabidopsis LRX1 requires Tyr for function but not for insolubilization in the cell wall.

  2010cited by this paper
• Characterization of two carnation petal prolyl 4 hydroxylases.

  2010cited by this paper
• A Bioinformatics Approach to the Identification, Classification, and Analysis of Hydroxyproline-Rich Glycoproteins[W][OA]

  2010cited by this paper
• A simple method for gene expression and chromatin profiling of individual cell types within a tissue.

  2010cited by this paper
• Elaboration of extensin-pectin thin film model of primary plant cell wall.

  2010cited by this paper
• Contiguous O-galactosylation of 4(R)-hydroxy-l-proline residues forms very stable polyproline II helices.

  2010cited by this paper
• Secreted Peptide Signals Required for Maintenance of Root Stem Cell Niche in Arabidopsis

  2010cited by this paper
• A glycopeptide regulating stem cell fate in Arabidopsis thaliana.

  2009cited by this paper
• cis-Element- and Transcriptome-Based Screening of Root Hair-Specific Genes and Their Functional Characterization in Arabidopsis1[C][W][OA]

  2009cited by this paper
• Identification of extensin protein associated with sugar beet pectin.

  2009cited by this paper
• The Crystal Structure of an Algal Prolyl 4-Hydroxylase Complexed with a Proline-rich Peptide Reveals a Novel Buried Tripeptide Binding Motif*

  2009cited by this paper
• Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases

  2009influential reference
• Prolyl-4-hydroxylase (AtP4H1) mediates and mimics low oxygen response in Arabidopsis thaliana

  2009cited by this paper
• Prolyl 4-hydroxylases, key enzymes in the synthesis of collagens and regulation of the response to hypoxia, and their roles as treatment targets

  2008cited by this paper
• Self-assembly of the plant cell wall requires an extensin scaffold

  2008cited by this paper
• Between-Species Analysis of Short-Repeat Modules in Cell Wall and Sex-Related Hydroxyproline-Rich Glycoproteins of Chlamydomonas1[W][OA]

  2007cited by this paper
• Arabidopsis prolyl 4‐hydroxylases are differentially expressed in response to hypoxia, anoxia and mechanical wounding

  2007cited by this paper
• Sentinels at the wall: cell wall receptors and sensors.

  2007cited by this paper
• Chlamydomonas reinhardtii Has Multiple Prolyl 4-Hydroxylases, One of Which Is Essential for Proper Cell Wall Assembly[W]

  2007influential reference
• Involvement of Arabidopsis Prolyl 4 Hydroxylases in Hypoxia, Anoxia and Mechanical Wounding

  2007cited by this paper
• Molecular characterization of two Arabidopsis thaliana glycosyltransferase mutants, rra1 and rra2, which have a reduced residual arabinose content in a polymer tightly associated with the cellulosic wall residue

  2007influential reference
• Structural analysis of linear hydroxyproline-bound O-glycans of Chlamydomonas reinhardtii--conservation of the inner core in Chlamydomonas and land plants.

  2007cited by this paper
• The Active Site of an Algal Prolyl 4-Hydroxylase Has a Large Structural Plasticity*

  2007cited by this paper
• Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis.

  2006cited by this paper
• Dodeca-CLE Peptides as Suppressors of Plant Stem Cell Differentiation

  2006cited by this paper
• A Plant Peptide Encoded by CLV3 Identified by in Situ MALDI-TOF MS Analysis

  2006cited by this paper
• Characterization of a Second Arabidopsis thaliana Prolyl 4-Hydroxylase with Distinct Substrate Specificity*

  2005cited by this paper
• Growth of the plant cell wall

  2005cited by this paper
• Purification of extensin from cell walls of tomato (hybrid of Lycopersicon esculentum and L. peruvianum) cells in suspension culture

  2004cited by this paper
• Toward a Systems Approach to Understanding Plant Cell Walls

  2004influential reference
• Di-isodityrosine Is the Intermolecular Cross-link of Isodityrosine-rich Extensin Analogs Cross-linked in Vitro*

  2004influential reference
• The class III peroxidase multigenic family in rice and its evolution in land plants.

  2004cited by this paper
• Membrane-anchored prolyl hydroxylase with an export signal from the endoplasmic reticulum.

  2004influential reference
• Toward a systems approach to understanding plant cell walls.

  2004cited by this paper
• Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development.

  2003influential reference
• Polyadenylation Regulates the Stability of Trypanosoma brucei Mitochondrial RNAs*

  2003cited by this paper
• Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis.

  2003influential reference
• Systemic Signaling in Tomato Plants for Defense against Herbivores

  2003cited by this paper
• A Biochemical and Molecular Characterization of LEP1, an Extensin Peroxidase from Lupin*

  2003cited by this paper
• Whole-Genome Comparison of Leucine-Rich Repeat Extensins in Arabidopsis and Rice. A Conserved Family of Cell Wall Proteins Form a Vegetative and a Reproductive Clade1,212

  2003cited by this paper
• Cloning and Characterization of a Low Molecular Weight Prolyl 4-Hydroxylase from Arabidopsis thaliana

  2002influential reference
• Plant Metabolomics

  2002cited by this paper
• The Cell Wall Hydroxyproline-Rich Glycoprotein RSH Is Essential for Normal Embryo Development in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010477.

  2002influential reference
• Tomato LeAGP-1 arabinogalactan-protein purified from transgenic tobacco corroborates the Hyp contiguity hypothesis.

  2002cited by this paper
• Cloning and characterization of a low molecular weight prolyl 4-hydroxylase from Arabidopsis thaliana. Effective hydroxylation of proline-rich, collagen-like, and hypoxia-inducible transcription factor alpha-like peptides.

  2002influential reference
• The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana.

  2001cited by this paper
• The latest hype on Hyp-O-glycosylation codes.

  2001cited by this paper
• Contiguous Hydroxyproline Residues Direct Hydroxyproline Arabinosylation in Nicotiana tabacum *

  2001influential reference
• Glycosylated polyproline II rods with kinks as a structural motif in plant hydroxyproline-rich glycoproteins.

  2001cited by this paper
• Rapid deposition of extensin during the elicitation of grapevine callus cultures is specifically catalyzed by a 40-kilodalton peroxidase.

  2001cited by this paper
• Role of extensin peroxidase in tomato (Lycopersicon esculentum Mill.) seedling growth

  2000cited by this paper
• Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation.

  2000cited by this paper
• Synthetic genes for glycoprotein design and the elucidation of hydroxyproline-O-glycosylation codes.

  1999cited by this paper
• Characterization and expression of four proline-rich cell wall protein genes in Arabidopsis encoding two distinct subsets of multiple domain proteins.

  1999cited by this paper
• Biochemistry of the extracellular matrix of Volvox.

  1998cited by this paper
• Pulcherosine, an oxidatively coupled trimer of tyrosine in plant cell walls: its role in cross-link formation.

  1998cited by this paper
• In vitro cross-linking of extensin precursors by mustard extracellular isoforms of peroxidase that respond either to phytochrome or to wounding

  1998cited by this paper
• Isolation of pl 4.6 extensin peroxidase from tomato cell suspension cultures and identification of Val-Tyr-Lys as putative intermolecular cross-link site.

  1996cited by this paper
• Di-isodityrosine, a novel tetrametric derivative of tyrosine in plant cell wall proteins: a new potential cross-link.

  1996cited by this paper
• Solubilization and Partial Characterization of Extensin Fragments from Cell Walls of Cotton Suspension Cultures (Evidence for a Covalent Cross-Link between Extensin and Pectin)

  1995cited by this paper
• Purification and Partial Characterization of Tomato Extensin Peroxidase

  1995cited by this paper
• Pex1, a pollen-specific gene with an extensin-like domain.

  1995cited by this paper
• A style-specific hydroxyproline-rich glycoprotein with properties of both extensins and arabinogalactan proteins.

  1994cited by this paper
• Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny.

  1994influential reference
• Trypsin cleaves lysylproline in a hydroxyproline-rich glycoprotein from Zea mays.

  1989cited by this paper
• Enzymic cross-linkage of monomeric extensin precursors in vitro.

  1988cited by this paper
• Prolyl 4-hydroxylase from Volvox carteri. A low-Mr enzyme antigenically related to the alpha subunit of the vertebrate enzyme.

  1988cited by this paper
• The role of carbohydrate in maintaining extensin in an extended conformation.

  1986cited by this paper
• Reinforced Polyproline II Conformation in a Hydroxyproline-Rich Cell Wall Glycoprotein from Carrot Root.

  1984influential reference
• Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein.

  1982influential reference
• Plant prolyl hydroxylase recognizes poly(L-proline) II helix.

  1981cited by this paper
• Structure and Function of Plant Glycoproteins

  1980cited by this paper
• Structure, Biosynthesis and Significance of Cell Wall Glycoproteins

  1977cited by this paper
• Hydroxyproline-O-glycosidic Linkage of the Plant Cell Wall Glycoprotein Extensin

  1967cited by this paper
• Oxygen fixation into hydroxyproline of plant cell wall protein.

  1963cited by this paper
• Hydroxyproline in Primary Cell Walls of Higher Plants

  1960cited by this paper
• Biochemical chlorination in Streptomvces aureofaciens.

  1960cited by this paper

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• Land plant peptide signaling: What we know—and don't know—about its evolution

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  2023cites this paper
• Transcription factor NAC1 activates expression of peptidase-encoding AtCEPs in roots to limit root hair growth.

  2023cites this paper
• Exploring the extensin gene family: an updated genome-wide survey in plant and algae.

  2023cites this paper
• Bifidobacterial GH146 β‐l‐Arabinofuranosidase (Bll4HypBA1) as the Last Enzyme for the Complete Removal of Oligoarabinofuranosides from Hydroxyproline‐Rich Glycoproteins

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• Pretreatment of seeds with hydrogen peroxide improves deep-sowing tolerance of wheat seedlings.

  2021cites this paper
• 3,4-Dehydro-L-proline Induces Programmed Cell Death in the Roots of Brachypodium distachyon

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  2021cites this paper
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  2021cites this paper
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• The placenta of Physcomitrium patens: transfer cell wall polymers compared across the three bryophyte groups.

  2021cites this paper
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  2021cites this paper
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  2019cites this paper
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  2019cites this paper
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  2018cites this paper
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  2018cites this paper
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  2017cites this paper
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