Skip to main content
SpringerLink
Log in

Induction of multinucleation by β-glucosyl Yariv reagent in regenerated cells from Marchantia polymorpha protoplasts and involvement of arabinogalactan proteins in cell plate formation

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Arabinogalactan proteins (AGPs) are abundant plant cell surface proteoglycans widely distributed in plant species. Since high concentrations of β-glucosyl Yariv reagent (βglcY), which binds selectively to AGPs, inhibited cell division of protoplast-regenerated cells of the liverwort Marchantia polymorpha L. (Shibaya and Sugawara in Physiol Plant 130:271–279, 2007), we investigated the mechanism underlying the inability of the cells to divide normally by staining nuclei, cell walls and β-1,3-glucan. Microscopic observation showed that the diameter of regenerated cells cultured with βglcY was about 2.8-fold larger than that of cells cultured without βglcY. The cells cultured with βglcY were remarkably multinucleated. These results indicated that βglcY did not inhibit mitosis but induced multinucleation. In the regenerated cells cultured with low concentrations of βglcY (5 and 1 μg ml−1), the cell plate was stained strongly by βglcY, suggesting abundant AGPs in the forming cell plate. In these cell plates, β-1,3-glucan was barely detectable or not detected. In multinucleated cells, cell plate-like fragments, which could not reach the cell wall, were frequently observed and they were also stained strongly by βglcY. Our results indicated that AGPs might have an important role in cell plate formation, and perturbation of AGPs with βglcY might result in remarkable multinucleation in protoplast-regenerated cells of M. polymorpha.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

AGP:

Arabinogalactan protein

βglcY:

β-Glucosyl Yariv reagent

αgalY:

α-Galactosyl Yariv reagent

βmanY:

β-Mannosyl Yariv reagent

References

  • Basile DV, Basile MR (1987) The occurrence of cell wall-associated arabinogalactan proteins in the Hepaticae. Bryologist 90:401–404

    Article  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 Academic/Plenum Publishers, New York, pp 169–178

    Google Scholar 

  • Butowt R, Niklas A, Rodriguez-Garcia MI, Majewska-Sawka A (1999) Involvement of JIM13- and JIM18-responsive carbohydrate epitopes in early stages of cell wall formation. J Plant Res 112:107–116

    Article  Google Scholar 

  • Chapman A, Blervacq AS, Vasseur J, Hilbert JL (2000) Arabinogalactan-proteins in Cichorium somatic embryogenesis: effect of β-glucosyl Yariv reagent and epitope localisation during embryo development. Planta 211:305–314

    Article  PubMed  CAS  Google Scholar 

  • Currier HB (1957) Callose substances in plant cells. Am J Bot 44:478–488

    Article  Google Scholar 

  • Fincher GB, Stone BA, Clarke AE (1983) Arabinogalactan proteins: structure, biosynthesis, and function. Annu Rev Plant Physiol 34:47–70

    Article  CAS  Google Scholar 

  • Fu H, Yadav MP, Nothnagel EA (2007) Physcomitrella patens arabinogalactan proteins contain abundant terminal 3-o-methyl-L-rhamnosyl residues not found in angiosperms. Planta 226:1511–1524

    Article  PubMed  CAS  Google Scholar 

  • Guan Y, Nothnagel EA (2004) Binding of arabinogalactan proteins by Yariv phenylglycoside triggers wound-like responses in Arabidopsis cell cultures. Plant Physiol 135:1346–1366

    Article  PubMed  Google Scholar 

  • Jauh G-Y, Lord EM (1996) Localization of pectins and arabinogalactan-proteins in lily (Lilium longiflorum L.) pollen tube and style, and their possible roles in pollination. Planta 199:251–261

    Article  CAS  Google Scholar 

  • Knox JP (1992) Molecular probes for the plant cell surface. Protoplasma 167:1–9

    Article  CAS  Google Scholar 

  • Kreuger M, van Holst G-J (1995) Arabinogalactan-protein epitopes in somatic embryogenesis of Daucus carota L. Planta 197:135–141

    Article  CAS  Google Scholar 

  • Larkin PJ (1977) Plant protoplast agglutination and membrane-bound β-lectins. J Cell Sci 26:31–46

    PubMed  CAS  Google Scholar 

  • Larkin PJ (1978) Plant protoplast agglutination by artificial carbohydrate antigens. J Cell Sci 30:283–292

    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 wall of bryophytes: new evidence for the multiple evolution of water-conducting cells. New Phytol 156:491–508

    Article  CAS  Google Scholar 

  • Majewska-Sawka A, Münster A (2003) Cell-wall antigens in mesophyll cells and mesophyll-derived protoplasts of sugar beet: possible implication in protoplast recalcitrance? Plant Cell Rep 21:946–954

    Article  PubMed  CAS  Google Scholar 

  • Mashiguchi K, Urakami E, Hasegawa M, Sanmiya K, Matsumoto I, Yamaguchi I, Asami T, Suzuki Y (2008) Defense-related signaling by interaction of arabinogalactan proteins and β-glucosyl Yariv reagent inhibits gibberellin signaling in barley aleurone cells. Plant Cell Physiol 49:178–190

    Article  PubMed  CAS  Google Scholar 

  • Meyer Y, Herth W (1978) Chemical inhibition of cell wall formation and cytokinesis, but not of nuclear division, in protoplasts of Nicotiana tabacum L. cultivated in vitro. Planta 142:253–262

    Article  CAS  Google Scholar 

  • Mock HP, Emmerling M, Seitz HU (1990) Cell wall synthesis in carrot cells: comparison of suspension-cultured cells and regenerating protoplasts. Physiol Plant 79:347–353

    Article  CAS  Google Scholar 

  • Mollet JC, Kim S, Jauh G-Y, Load EM (2002) Arabinogalactan proteins, pollen tube growth, and the reversible effects of Yariv phenylglycoside. Protoplasma 219:89–98

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nagata T, Takebe I (1970) Cell wall regeneration and cell division in isolated tobacco protoplasts. Planta 92:301–308

    Article  Google Scholar 

  • Nguema-Ona E, Bannigan A, Chevalier L, Baskin T, Driouich A (2007) Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana. Plant J 52:240–251

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nothnagel EA, Lyon JL (1986) Structural requirements for the binding of phenylglycosides to the surface of protoplasts. Plant Physiol 80:91–98

    Article  PubMed  CAS  Google Scholar 

  • Rauh RA, Basile DV (2003) Phenovariation induced in Streptocarpus prolixus (Gesneriaceae) by β-glucosyl Yariv reagent. Can J Bot 81:338–344

    Article  CAS  Google Scholar 

  • Roy SJ, Jauh GY, Hepler PK, Lord EM (1998) Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube. Planta 204:450–458

    Article  PubMed  CAS  Google Scholar 

  • Samson MR, Klis FM, Sigon CAM, Stegwee D (1983) Localization of arabinogalactan proteins in the membrane system of etiolated hypocotyls of Phaseolus vulgaris L. Planta 159:322–328

    Article  CAS  Google Scholar 

  • Samuels AL, Giddings TH Jr, Staehelin A (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357

    Article  PubMed  CAS  Google Scholar 

  • Sardar HS, Yang J, Showalter AM (2006) Molecular interactions of arabinogalactan proteins with cortical microtubules and F-actin in Bright Yellow-2 tobacco cultured cells. Plant Physiol 142:1469–1479

    Article  PubMed  CAS  Google Scholar 

  • Serpe MD, Nothnagel EA (1994) Effects of Yariv phenylglycosides on Rosa cell-suspensions: evidence for the involvement of arabinogalactan-proteins in cell proliferation. Planta 193:542–550

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shea EM, Gibeaut DM, Carpita NC (1989) Structural analysis of the cell walls regenerated by carrot protoplasts. Planta 179:293–308

    Article  CAS  Google Scholar 

  • Sherrier DJ, Prime TA, Dupree P (1999) Glycosylphosphatidylinositol-anchored cell surface proteins from Arabidopsis. Electrophoresis 20:2027–2035

    Article  PubMed  CAS  Google Scholar 

  • Shibaya T, Sugawara Y (2007) Involvement of arabinogalactan proteins in the regeneration process of cultured protoplasts of Marchantia polymorpha. Physiol Plant 130:271–279

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stone BA, Clarke AE (1992) Chemistry and biology of (1 → 3)-β-glucans. La Trobe University Press, Victoria, pp 365–803

    Google Scholar 

  • Sugawara Y, Mori K, Matsushima H, Takeuchi M (1983) Enhancement of cell division in Marchantia protoplast culture by activated charcoal. Z Pflanzenphysiol 109:275–278

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Komamine A (1978) Composition of the cell wall formed by protoplasts isolated from cell suspension cultures of Vinca rosea. Planta 140:227–232

    Article  CAS  Google Scholar 

  • Takeuchi M, Matsushima H, Sugawara Y (1980) Long-term freeze-preservation of protoplast carrot and Marchantia. Cryo-Letters 1:519–524

    CAS  Google Scholar 

  • Thompson HJ, Knox JP (1998) Stage-specific responses of embryogenic carrot cell suspension cultures to arabinogalactan protein-binding β-glucosyl Yariv reagent. Planta 205:32–38

    Article  CAS  Google Scholar 

  • Vissenberg K, Feijo JA, Weisenseel MH, Verbelen J-P (2001) Ion fluxes, auxin and the induction of elongation growth in Nicotiana tabacum cells. J Exp Bot 52:2161–2167

    PubMed  CAS  Google Scholar 

  • Willats WGT, Knox JP (1996) A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of β-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J 9:919–925

    Article  PubMed  CAS  Google Scholar 

  • Yariv J, Rapport MM, Graf L (1962) The interaction of glycosides and saccharides with antibody to the corresponding phenylazo glycosides. Biochem J 85:383–388

    PubMed  CAS  Google Scholar 

  • Yariv J, Lis H, Katchalski E (1967) Precipitation of arabic acid and some seed polysaccharides of glycosyl-phenylazo dyes. Biochem J 105:1C–2C

    PubMed  CAS  Google Scholar 

  • Yates EA, Valdor JE, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6:131–139

    Article  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 

Download references

Acknowledgment

The authors thank Dr. P. Knox (University of Leeds, UK) for providing the JIM13 and LM2 antibodies.

Author information

Author notes

  1. Taeko Shibaya

    Present address: National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, 305-8602, Japan

Authors and Affiliations

  1. Department of Regulation-Biology, Faculty of Science, Saitama University, Saitama, 338-8570, Japan

    Taeko Shibaya & Yasutake Sugawara

Authors
  1. Taeko Shibaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasutake Sugawara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Taeko Shibaya.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure S1 (DOC 1,005 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shibaya, T., Sugawara, Y. Induction of multinucleation by β-glucosyl Yariv reagent in regenerated cells from Marchantia polymorpha protoplasts and involvement of arabinogalactan proteins in cell plate formation. Planta 230, 581–588 (2009). https://doi.org/10.1007/s00425-009-0954-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-0954-y

Keywords

Search

Navigation