Home LiteratureArticle Details
PMID: 21949134 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Down-regulation of UDP-glucuronic acid biosynthesis leads to swollen plant cell walls and severe developmental defects associated with changes in pectic polysaccharides.

The Journal of biological chemistry ·Vol. 286 ·No. 46 ·2011-11-18 ·Pages 39982-92

Reboul R, Geserick C, Pabst M, Frey B, Wittmann D, Lütz-Meindl U, Léonard R, Tenhaken R

Abstract

UDP-glucose dehydrogenase (UGD) plays a key role in the nucleotide sugar biosynthetic pathway, as its product UDP-glucuronic acid is the common precursor for arabinose, xylose, galacturonic acid, and apiose residues found in the cell wall. In this study we characterize an Arabidopsis thaliana double mutant ugd2,3 that lacks two of the four UGD isoforms. This mutant was obtained from a cross of ugd2 and ugd3 single mutants, which do not show phenotypical differences compared with the WT. In contrast, ugd2,3 has a strong dwarfed phenotype and often develops seedlings with severe root defects suggesting that the UGD2 and UGD3 isoforms act in concert. Differences in its cell wall composition in comparison to the WT were determined using biochemical methods indicating a significant reduction in arabinose, xylose, apiose, and galacturonic acid residues. Xyloglucan is less substituted with xylose, and pectins have a reduced amount of arabinan side chains. In particular, the amount of the apiose containing side chains A and B of rhamnogalacturonan II is strongly reduced, resulting in a swollen cell wall. The alternative pathway to UDP-glucuronic acid with the key enzyme myo-inositol oxygenase is not up-regulated in ugd2,3. The pathway also does not complement the ugd2,3 mutation, likely because the supply of myo-inositol is limited. Taken together, the presented data underline the importance of UDP GlcA for plant primary cell wall formation.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Cell Wall/genetics,metabolism Down-Regulation Mutation Pectins/biosynthesis,genetics Uridine Diphosphate Glucose Dehydrogenase/genetics,metabolism Uridine Diphosphate Glucuronic Acid/biosynthesis,genetics
Chemicals
Arabidopsis Proteins Uridine Diphosphate Glucuronic Acid Pectins Uridine Diphosphate Glucose Dehydrogenase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Reboul Rebecca
Department of Cell Biology, Molecular Cell Physiology, University of Salzburg, 5020 Salzburg, Austria.
Geserick Claudia
Pabst Martin
Frey Beat
Wittmann Doris
Lütz-Meindl Ursula
Léonard Renaud
Tenhaken Raimund
References (42)
42 references, click to expand
  1. Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside.
    Curr Opin Plant Biol. 2004 Jun;7(3):277-84 PMID: 15134748
  2. QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis.
    Plant Cell. 2002 Oct;14(10):2577-90 PMID: 12368506
  3. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings.
    Plant J. 2007 Feb;49(3):463-91 PMID: 17217462
  4. Structural characterisation of the pectic polysaccharide rhamnogalacturonan II using an acidic fingerprinting methodology.
    Planta. 2009 Oct;230(5):947-57 PMID: 19672621
  5. Radioisotope ratios discriminate between competing pathways of cell wall polysaccharide and RNA biosynthesis in living plant cells.
    Plant J. 2007 Oct;52(2):252-62 PMID: 17764499
  6. ARABINAN DEFICIENT 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis.
    Plant Physiol. 2006 Jan;140(1):49-58 PMID: 16377743
  7. Matrix polysaccharide precursors in Arabidopsis cell walls are synthesized by alternate pathways with organ-specific expression patterns.
    Plant J. 2000 Mar;21(6):537-46 PMID: 10758504
  8. Cloning of an enzyme that synthesizes a key nucleotide-sugar precursor of hemicellulose biosynthesis from soybean: UDP-glucose dehydrogenase.
    Plant Physiol. 1996 Nov;112(3):1127-34 PMID: 8938413
  9. The mur4 mutant of arabidopsis is partially defective in the de novo synthesis of uridine diphospho L-arabinose.
    Plant Physiol. 1999 Oct;121(2):383-9 PMID: 10517829
  10. Genome-wide analysis of the UDP-glucose dehydrogenase gene family in Arabidopsis, a key enzyme for matrix polysaccharides in cell walls.
    J Exp Bot. 2007;58(13):3609-21 PMID: 18057039
  11. Local expression of expansin induces the entire process of leaf development and modifies leaf shape.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11812-7 PMID: 11562463
  12. UDP-sugar pyrophosphorylase with broad substrate specificity toward various monosaccharide 1-phosphates from pea sprouts.
    J Biol Chem. 2004 Oct 29;279(44):45728-36 PMID: 15326166
  13. Novel characteristics of UDP-glucose dehydrogenase activities in maize: non-involvement of alcohol dehydrogenases in cell wall polysaccharide biosynthesis.
    Planta. 2006 Mar;223(4):858-70 PMID: 16453102
  14. Pectin: cell biology and prospects for functional analysis.
    Plant Mol Biol. 2001 Sep;47(1-2):9-27 PMID: 11554482
  15. Biochemical genetics of nucleotide sugar interconversion reactions.
    Curr Opin Plant Biol. 2008 Jun;11(3):236-43 PMID: 18486535
  16. Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7.
    Carbohydr Res. 2003 Aug 12;338(17):1797-800 PMID: 12892947
  17. Dissociation and in vitro reconstitution of bovine liver uridine diphosphoglucose dehydrogenase. The paired subunit nature of the enzyme.
    Biochemistry. 1986 Nov 18;25(23):7283-7 PMID: 3099833
  18. Cloning of Glucuronokinase from Arabidopsis thaliana, the last missing enzyme of the myo-inositol oxygenase pathway to nucleotide sugars.
    J Biol Chem. 2010 Jan 29;285(5):2902-10 PMID: 19951951
  19. Down-regulation of the myo-inositol oxygenase gene family has no effect on cell wall composition in Arabidopsis.
    Planta. 2011 Jul;234(1):157-69 PMID: 21394467
  20. Myo-inositol oxygenase genes are involved in the development of syncytia induced by Heterodera schachtii in Arabidopsis roots.
    New Phytol. 2009 Oct;184(2):457-472 PMID: 19691674
  21. Growth regulators and the control of nucleotide sugar flux.
    Plant Cell. 2004 Mar;16(3):723-30 PMID: 14973160
  22. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  23. Rapid structural phenotyping of plant cell wall mutants by enzymatic oligosaccharide fingerprinting.
    Plant Physiol. 2002 Dec;130(4):1754-63 PMID: 12481058
  24. Partial purification and study of pollen glucuronokinase.
    Arch Biochem Biophys. 1977 Mar;179(2):559-64 PMID: 192151
  25. Comparison of cryofixation and aldehyde fixation for plant actin immunocytochemistry: aldehydes do not destroy F-actin.
    Histochem J. 2000 Aug;32(8):457-66 PMID: 11095070
  26. Myoinositol oxygenase controls the level of myoinositol in Arabidopsis, but does not increase ascorbic acid.
    Plant Physiol. 2009 Feb;149(2):1042-9 PMID: 19091876
  27. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.
    Plant Physiol. 2004 Sep;136(1):2621-32 PMID: 15375207
  28. Evidence for in vitro binding of pectin side chains to cellulose.
    Plant Physiol. 2005 Sep;139(1):397-407 PMID: 16126855
  29. Generation of monoclonal antibody specific to (1-->5)-alpha-L-arabinan.
    Carbohydr Res. 1998 Mar;308(1-2):149-52 PMID: 9675359
  30. A general approach to desalting oligosaccharides released from glycoproteins.
    Glycoconj J. 1998 Aug;15(8):737-47 PMID: 9870349
  31. Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component.
    Plant Cell. 2008 Jun;20(6):1519-37 PMID: 18544630
  32. Cell wall and rhizoid polarity in Pelvetia embryos.
    Dev Biol. 1993 Dec;160(2):303-14 PMID: 8253266
  33. Pectin-like carbohydrates in the green alga Micrasterias characterized by cytochemical analysis and energy filtering TEM.
    J Microsc. 2008 Aug;231(2):201-14 PMID: 18778418
  34. Molecular genetics of nucleotide sugar interconversion pathways in plants.
    Plant Mol Biol. 2001 Sep;47(1-2):95-113 PMID: 11554483
  35. The inositol oxygenase gene family of Arabidopsis is involved in the biosynthesis of nucleotide sugar precursors for cell-wall matrix polysaccharides.
    Planta. 2005 May;221(2):243-54 PMID: 15660207
  36. Inositol and plant cell wall polysaccharide biogenesis.
    Subcell Biochem. 2006;39:21-45 PMID: 17121270
  37. Reconstruction of de novo pathway for synthesis of UDP-glucuronic acid and UDP-xylose from intrinsic UDP-glucose in Saccharomyces cerevisiae.
    FEBS J. 2006 Jun;273(12):2645-57 PMID: 16817893
  38. Use of energy-filtering transmission electron microscopy for routine ultrastructural analysis of high-pressure-frozen or chemically fixed plant cells.
    Protoplasma. 2004 Jun;223(2-4):155-62 PMID: 15221520
  39. Glycosyltransferases and cell wall biosynthesis: novel players and insights.
    Curr Opin Plant Biol. 2004 Jun;7(3):285-95 PMID: 15134749
  40. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth.
    Science. 2001 Oct 26;294(5543):846-9 PMID: 11679668
  41. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling.
    Phytochemistry. 2001 Jul;57(6):929-67 PMID: 11423142
  42. Cell wall alterations in the arabidopsis emb30 mutant.
    Plant Cell. 2000 Nov;12(11):2047-60 PMID: 11090208
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2011-11-18
Epub
2011-00-23
Pages
39982-92
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC3220558
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com