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Physcomitrella patens arabinogalactan proteins contain abundant terminal 3-O-methyl-l-rhamnosyl residues not found in angiosperms

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Abstract

A biochemical investigation of arabinogalactan proteins (AGPs) in Physcomitrella patens was undertaken with particular emphasis on the glycan chains. Following homogenization and differential centrifugation of moss gametophytes, AGPs were obtained by Yariv phenylglycoside-induced precipitation from the soluble, microsomal membrane, and cell wall fractions. Crossed-electrophoresis indicated that each of these three AGP fractions was a mixture of several AGPs. The soluble AGP fraction was selected for further separation by anion-exchange and gel-permeation chromatography. The latter indicated molecular masses of ∼100 and 224 kDa for the two major soluble AGP subfractions. The AGPs in both of these subfractions contained the abundant (1,3,6)-linked galactopyranosyl residues, terminal arabinofuranosyl residues, and (1,4)-linked glucuronopyranosyl residues that are typical of many angiosperm AGPs. Unexpectedly, however, the moss AGP glycan chains contained about 15 mol% terminal 3-O-methyl-l-rhamnosyl residues, which have not been found in angiosperm AGPs. This unusual and relatively nonpolar sugar, also called l-acofriose, is likely to have considerable effects on the overall polarity of Physcomitrella AGPs. A review of the literature indicates that the capacity to synthesize polymers containing 3-O-methyl-l-rhamnosyl residues is present in a variety of bacteria, algae and lower land plants but became less common through evolution to the extent that this sugar has been found in only a few species of angiosperms where it occurs as a single residue on steroidal glycosides.

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Abbreviations

AGP:

Arabinogalactan protein

Ara:

Arabinose

DMSO:

Dimethyl sulfoxide

Fuc:

Fucose

Gal:

Galactose

Glc:

Glucose

(β-d-Glc)3 :

β-glucosyl Yariv phenylglycoside

GlcUA:

Glucuronic acid

GLC-MS:

Gas–liquid chromatography-mass spectrometry

Hyp:

Hydroxyproline

Man:

Mannose

Rha:

Rhamnose

TMS:

Trimethylsilyl

Xyl:

Xylose

References

  • Akiyama T, Tanaka K, Yamamoto S, Iseki S (1988) Blood-group active proteoglycan containing 3-O-methylrhamnose (acofriose) from young plants of Osmunda japonica. Carbohydr Res 178:320–326

    Article  PubMed  CAS  Google Scholar 

  • Allard B, Casadevall E (1990) Carbohydrate composition and characterization of sugars from the green microalga Botryococcus braunii. Phytochemistry 29:1875–1878

    Article  CAS  Google Scholar 

  • Anderson DMW, Munro AC (1969) The presence of 3-O-methylrhamnose in Araucaria resinous exudates. Phytochemistry 8:633–634

    Article  CAS  Google Scholar 

  • Ashwell G (1966) New colorimetric methods of sugar analysis. Methods Enzymol 8:85–95

    CAS  Google Scholar 

  • Basile DV, Basile MR (1988) Procedures used for the axenic culture and experimental treatment of bryophytes. In: Glime JM (eds) Methods in bryology. Proceedings of the bryological methods workshop, Mainz. Hattori Botanical Laboratory, Nichinan, Japan, pp 1–16

    Google Scholar 

  • Basile DV, Basile MR, Mignone MM (2000) Arabinogalactan-proteins, place-dependent suppression and plant morphogenesis. In: Nothnagel EA, Bacic A, Clarke AE (eds) Cell and developmental biology of arabinogalactan-proteins. Kluwer /Plenum, New York, pp 169–178

    Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  PubMed  CAS  Google Scholar 

  • Carpita NC, Shea EM (1989) Linkage structure of carbohydrates by gas chromatography-mass spectrometry (GC-MS) of partially methylated alditol acetates. In: Biermann CJ, McGinnis GD (eds) Analysis of carbohydrates by GLC and MS. CRC, Boca Raton, pp 157–216

    Google Scholar 

  • Ciucanu I, Kerek F (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131:209–217

    Article  CAS  Google Scholar 

  • Doares SH, Albersheim P, Darvill AG (1991) An improved method for the preparation of standards for glycosyl-linkage analysis of complex carbohydrates. Carbohydr Res 210:311–317

    Article  CAS  Google Scholar 

  • Edelmann H, Neinhuis C, Jarvis MC, Evans B, Fisher E, Barthlott W (1998) Ultrastructure and chemistry of the cell wall of the moss Rhacocarpus purpurascens (Rhacocarpaceae): a puzzling architecture among plants. Planta 206:315–321

    Article  CAS  Google Scholar 

  • Fry SC (1988) The growing plant cell wall: chemical and metabolic analysis. Longman Scientific and Technical, Harlow, UK

    Google Scholar 

  • Gaspar YM, Nam J, Schultz CJ, Lee L-Y, Gilson PR, Gelvin SB, Bacic A (2004) Characterization of the Arabidopsis lysine-rich arabinogalactan-protein AtAGP17 mutant (rat1) that results in a decreased efficiency of Agrobacterium transformation. Plant Physiol 135:2162–2171

    Article  PubMed  CAS  Google Scholar 

  • Gerwig GJ, Kamerling JP, Vliegenthart JFG (1979) Determination of the absolute configuration of monosaccharides in complex carbohydrates by capillary GLC. Carbohdyr Res 77:1–7

    Article  CAS  Google Scholar 

  • Gorrod ARN, Jones JKN (1954) The hemicelluloses of Scots pine (Pinus sylvestis) and black spruce (Picea nigra) woods. J Chem Soc 2522–2525

  • Jackson LK, Slodki ME, Plattner RD, Burton KA, Cadmus MC (1982) Capsular and extracellular polysaccharides from Rhizobium microsymbionts of Acacia decurrens. Carbohydr Res 110:267–276

    Article  CAS  Google Scholar 

  • Kaplan M, Stephen AM, Vogt D (1966) 3-O-Methyl-L-rhamnose as a constituent of plant polysaccharide gums. S African Med J 40:702

    Google Scholar 

  • Komalavilas P, Zhu JK, Nothnagel EA (1991) Arabinogalactan-proteins from the suspension culture medium and plasma membrane of rose cells. J Biol Chem 266:15956–15965

    PubMed  CAS  Google Scholar 

  • Kremer C, Pettolino F, Bacic A, Drinnan A (2004) Distribution of cell wall components in Sphagnum haline cells and in liverwort and hornwort elaters. Planta 219:1023–1035

    Article  PubMed  CAS  Google Scholar 

  • Lee KJD, Sakata Y, Mau S-L, Pettolino F, Bacic A, Quatrano RS, Knight CD, Knox JP (2005) Arabinogalactan proteins are required for apical cell extension in the moss Physcomitrella patens. Plant Cell 17:3051–3065

    Article  PubMed  CAS  Google Scholar 

  • Ligrone R, Vaughn KC, Renzaglia KS, Knox JP, Duckett JG (2002) Diversity in the distribution of polysaccharide and glycoprotein epitopes in the cell walls of bryophytes: new evidence for the multiple evolution of water-conducting cells. New Phytol 156:491–508

    Article  CAS  Google Scholar 

  • MacLennan AP (1962) The monosaccharide units in specific glycolipids of Mycobacterium avium. Biochem J 82:394–400

    PubMed  CAS  Google Scholar 

  • Matsunaga T, Ishii T, Matsumoto S, Higuchi M, Darvill A, Albersheim P, O’Neill MA (2004) Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 134:339–351

    Article  PubMed  CAS  Google Scholar 

  • Métraux J-P (1982) Changes in cell-wall polysaccharide composition of developing Nitella internodes: analysis of walls of single cells. Planta 155:459–466

    Article  Google Scholar 

  • Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429:873–878

    Article  PubMed  CAS  Google Scholar 

  • Muhr H, Hunger A, Reichstein T (1954) Die Glykosider der Samen von Acokanthera friesiorum Markgr. Glykoside und Aglykone. Helv Chim Acta 37:403–427

    Article  CAS  Google Scholar 

  • Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174:195–291

    PubMed  CAS  Google Scholar 

  • Ogawa K, Yamaura M, Maruyama I (1997) Isolation and identification of 2-O-methyl-L-rhamnose and 3-O-methyl-L-rhamnose as constituents of an acidic polysaccharide of Chlorella vulgaris. Biosci Biotechnol Biochem 61:539–540

    Article  CAS  Google Scholar 

  • Popper ZA, Fry SC (2003) Primary cell wall composition of bryophytes and charophytes. Ann Bot 91:1–12

    Article  PubMed  CAS  Google Scholar 

  • Popper ZA, Fry SC (2004) Primary cell wall composition of pteridophytes and spermatocytes. New Phytol 164:165–174

    Article  CAS  Google Scholar 

  • Popper ZA, Sadler IH, Fry SC (2004) 3-O-Methylrhamnose in lower land plant primary cell walls. Biochem Syst Ecol 32:279–289

    Article  CAS  Google Scholar 

  • Qiu Y-L, Palmer JD (1999) Phylogeny of early land plants: insights from genes and genomes. Trends Plant Sci 4:6–30

    Article  Google Scholar 

  • Quatrano RS, McDaniel SF, Khandelwal A, Perroud P-F, Cove DJ (2007) Physcomitrella patens: mosses enter the genomic age. Curr Opin Plant Biol 10:182–189

    Article  PubMed  CAS  Google Scholar 

  • Serpe MD, Nothnagel EA (1995) Fractionation and structural characterization of arabinogalactan-proteins from the cell wall of rose cells. Plant Physiol 109:1007–1016

    PubMed  CAS  Google Scholar 

  • Serpe MD, Nothnagel EA (1996) Heterogeneity of arabinogalactan-proteins on the plasma membrane of Rosa cells. Plant Physiol 112:1261–1271

    PubMed  CAS  Google Scholar 

  • Serpe MD, Nothnagel EA (1999) Arabinogalactan-proteins in the multiple domains of the plant cell surface. Adv Bot Res 30:207–289

    Article  CAS  Google Scholar 

  • Shaw J, Renzaglia K (2004) Phylogeny and diversification of bryophytes. Am J Bot 91:1557–1581

    Google Scholar 

  • Shekharam KM, Venkataraman LV, Salimath PV (1987) Carbohydrate composition and characterization of two unusual sugars from the blue-green alga Spirulina platensis. Phytochemistry 26:2267–2269

    Article  CAS  Google Scholar 

  • Shibaya T, Kaneko Y, Sugawara Y (2005) Involvement of arabinogalactan proteins in protonema development from cultured cells of Marchantia polymorpha. Physiol Plant 124:504–514

    Article  CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Kieliszewski MJ, Showalter AM (2004) Overexpression of tomato LeAGP-1 arabinogalactan-protein promotes lateral branching and hampers reproductive development. Plant J 40:870–881

    Article  PubMed  CAS  Google Scholar 

  • Svetek J, Yadav MP, Nothnagel EA (1999) Presence of a glycosylphosphatidyl inositol lipid anchor on rose arabinogalactan proteins. J Biol Chem 274:14724–14733

    Article  PubMed  CAS  Google Scholar 

  • Thomas RJ (1977) Wall analyses of Lophocolea seta cells (Bryophyta) before and after elongation. Plant Physiol 59:337–340

    Article  PubMed  CAS  Google Scholar 

  • Tsai C-M, Frasch CE (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119:115–119

    Article  PubMed  CAS  Google Scholar 

  • Turvey JR, Griffiths LM (1973) Mucilage from a fresh-water red alga of the genus Batrachospermum. Phytochemistry 12:2901–2907

    Article  CAS  Google Scholar 

  • van Hengel AJ, Roberts K (2003) AtAGP30, an arabinogalactan-protein in the cell walls of the primary root plays a role in root regeneration and seed germination. Plant J 36:256–270

    Article  PubMed  CAS  Google Scholar 

  • Vinogradov EV, Campos-Portuguez S, Yokota A, Mayer H (1994) The structure of the O-specific polysaccharide from Thiobacillus ferrooxidans IFO 14262. Carbohydr Res 261:103–109

    Article  PubMed  CAS  Google Scholar 

  • Weckesser J, Katz A, Drews G, Mayer H, Fromme I (1974) Lipopolysaccharide containing L-acofriose in the filamentous blue-green algae Anabaena variabilis. J Bacteriol 120:672–678

    PubMed  CAS  Google Scholar 

  • Youl JJ, Bacic A, Oxley D (1998) Arabinogalactan proteins from Nicotiana alata and Pyrus communis contain glycosylphosphatidylinositol membrane anchors. Proc Natl Acad Sci USA 95:7921–7926

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Plant Biochemistry Program of the USDA National Research Initiative Competitive Grants Program (award no. 2002-35318-12616). Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture.

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  1. Madhav P. Yadav

    Present address: Eastern Regional Research Center, U.S. Department of Agriculture, Agricultural Research Service, 600 East Mermaid Lane, Wyndmoor, PA, 19038, USA

Authors and Affiliations

  1. Department of Botany and Plant Sciences-072, University of California, Riverside, CA, 92521-0124, USA

    Hu Fu, Madhav P. Yadav & Eugene A. Nothnagel

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  1. Hu Fu
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  2. Madhav P. Yadav
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  3. Eugene A. Nothnagel
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Correspondence to Eugene A. Nothnagel.

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Fu, H., Yadav, M.P. & Nothnagel, E.A. Physcomitrella patens arabinogalactan proteins contain abundant terminal 3-O-methyl-l-rhamnosyl residues not found in angiosperms. Planta 226, 1511–1524 (2007). https://doi.org/10.1007/s00425-007-0587-y

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