Skip to main content
Log in

Arabinogalactan proteins are involved in cell aggregation of cell suspension cultures of Beta vulgaris L.

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Arabinogalactan proteins (AGPs) are glycoproteins present at cell surfaces. Although exact functions of AGPs remain elusive, they are implicated in plant growth and development. The aim of this study was to evaluate the role of AGPs in the process of cell aggregation of Beta vulgaris L. suspension cultures. It was observed that B. vulgaris suspension cultures accumulated AGPs in parallel form to its cell growth. The AGPs maximum content in the stationary phase was 0.330 mg g−1 dry weight (DW) in the cell wall (CW) and 1.534 mg g−1 DW in the culture medium (CM), generating cell aggregates >500 μm (93.21% DW). The addition of tunicamycin (TM) caused a reduction of AGPs content in CW and CM of 46 and 64%, respectively. These changes were associated with inhibition of growth and the reduction of the cell aggregates >500 μm (50.0% DW). When TM was removed from the CM, cell growth, aggregation, and AGPs content on CW and CM were recovered. Precipitation of AGPs with Yariv reagent generated a reduction of 61.14% of AGPs content in CW and a total inhibition of AGPs secretion in CM. This Yariv treatment generated a reduction in the cell aggregates >500 μm of 51.31% of DW. When the Yariv reagent was removed from the culture, cells did not recover their AGPs accumulation. In addition, cell cultures did not recover their ability to grow and aggregate. These results indicate that AGPs are molecules required in the cellular aggregation process of B. vulgaris L. suspension cultures.

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

Access this article

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

Similar content being viewed by others

Abbreviations

AGPs:

Arabinogalactan proteins

CW:

Cell wall

CM:

Culture media

2,4-D:

2,4-Dichlorophenoxyacetic acid

DW:

Dry weight

β-ManY:

β-Manosil Yariv reagent

SPB:

Sodium buffer phosphate

TM:

Tunicamycin

References

  • Agyare-Tabbi A, Zhang J, Xiong A-S, Atnaseo C, Bahramnejad B, Erickson L (2010) A protein coding for a pollen-specific gene in alfalfa (Medicago sativa L.) is localized mainly in the intine of the pollen wall. Plant Cell Tiss Organ Cult. doi:10.1007/s11240-010-9820-7

  • Ben Amar A, Cobanov P, Ghorbel A, Mliki A, Reustle GM (2010) Involvement of arabinogalactan proteins in the control of cell proliferation of Cucurbita pepo suspension cultures. Biol Plant 54:321–324

    Article  CAS  Google Scholar 

  • Bonga JM, Klimaszewska KK, von Aderkas P (2010) Recalcitrance in clonal propagation, in particular of conifers. Plant Cell Tiss Organ Cult 100:241–254

    Article  Google Scholar 

  • Borderies G, Béchec M, Rossignol M, Lafitte C, Deunff E, Beckert M, Dumas C, Matthys-Rochon E (2004) Characterization of proteins secreted during maize microspore culture: arabinogalactan proteins (AGPs) stimulate embryo development. Eur J Cell Biol 83:205–212

    Article  PubMed  CAS  Google Scholar 

  • Capataz-Tafur J, Hernández-Sánchez A, Rodríguez-Monroy M, Trejo-Tapia G, Sepúlveda-Jiménez G (2010) Sucrose induces arabinogalactan protein secretion by Beta vulgaris L. cell suspension cultures. Acta Physiol Plant 32:757–764

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chaves I, Regalado AP, Chen M, Ricardo CP, Showalter AM (2002) Programmed cell death induced by (β-D-galactosyl)3 Yariv reagent in Nicotiana tabacum BY-2 suspension-cultured cells. Physiol Plant 116:548–553

    Article  CAS  Google Scholar 

  • Classen B (2007) Characterization of an arabinogalactan-protein from suspension culture of Echinacea purpurea. Plant Cell Tiss Organ Cult 88:267–275

    Article  CAS  Google Scholar 

  • Dass S, Ramawat KG (2009) Elicitation of guggulsterone production in cell cultures of Commiphora wightii by plant gums. Plant Cell Tiss Organ Cult 96:349–353

    Article  Google Scholar 

  • Ellis M, Egelund J, Schultz C, Bacic A (2010) Arabinogalactan-proteins: key regulators at the cell surface. Plant Physiol 153:403–419

    Article  PubMed  CAS  Google Scholar 

  • Gamborg O, Miller R, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    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 

  • Hernández Sánchez AM, Capataz Tafur J, Rodriguez-Monroy M, Sepúlveda-Jiménez G (2009) Arabinogalactan proteins in plant cell cultures. Interciencia 34:170–176

    Google Scholar 

  • Hori H, Elbein AD (1981) Tunicamycin inhibits protein glycosylation in suspension cultured soybean cells. Plant Physiol 67:882–886

    Article  PubMed  CAS  Google Scholar 

  • Hortsch M, Goodman CS (1990) Drosophila fasciclin I, a neural cell adhesion molecule, has a phosphatidylinositol membrane anchor that is developmentally regulated. J Biol Chem 265:15104–15109

    PubMed  CAS  Google Scholar 

  • Johnson KL, Jones BJ, Bacic A, Schultz CJ (2003) The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol 133:1911–1925

    Article  PubMed  CAS  Google Scholar 

  • Kieran PM, MacLoughlin PF, Malone DM (1997) Plant cell suspension cultures: some engineering considerations. J Biotechnol 59:39–52

    Article  PubMed  CAS  Google Scholar 

  • Knox JP, Linstead PJ, Peart J, Cooper C, Roberts K (1991) Developmentally regulated epitopes of cell surface arabinogalactan proteins and their relation to root tissue pattern formation. Plant J 1:317–326

    Google Scholar 

  • Kolewe ME, Henson MA, Roberts SE (2010) Characterization of aggregate size of Taxus suspension cell culture. Plant Cell Rep 29:485–494

    Article  PubMed  CAS  Google Scholar 

  • Lamport DT, Kieliszewiski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytol 169:479–492

    Article  PubMed  CAS  Google Scholar 

  • Langan KJ, Nothnagel EA (1997) Cell surface arabinogalactan proteins and their relation to cell proliferation and viability. Protoplasma 96:87–98

    Article  Google Scholar 

  • Leboeuf E, Thoiron S, Lahaye M (2004) Physico-chemical characteristics of cell walls from Arabidopsis thaliana microcalli showing different adhesion strengths. J Exp Bot 55:2087–2097

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–9

    Article  PubMed  CAS  Google Scholar 

  • Mitra N, Sinha S, Ramya TNC, Surolia A (2006) N-linked oligosaccharides as outfitters for glycoprotein folding, form and function. Trends Biochem Sci 31:156–163

    Article  PubMed  CAS  Google Scholar 

  • Nakata N, Ochiai H (1996) Inhibitory effects of tunicamycin on cell-cell adhesion and cell reaggregation of the cellular slime mold, Polysphondylium pallidum. J Plant Res 109:193–199

    Article  CAS  Google Scholar 

  • Paire A, Devaux P, Lafitte C, Dumas C, Matthys-Rochon E (2003) Proteins produced by barley microspores and their derived androgenic structures promote in vitro zygotic maize embryo formation. Plant Cell Tiss Organ Cult 73:167–176

    Article  CAS  Google Scholar 

  • Park MH, Suzuki Y, Chono M, Knox JP, Yamaguchi I (2003) CsAGP1, a gibberellin-responsive gene from cucumber hypocotyls, encodes a classical arabinogalactan protein and is involved in stem elongation. Plant Physiol 131:1450–1459

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Monroy M, Galindo E (1999) Broth rheology, growth and metabolite production of Beta vulgaris suspension culture: a comparative study between cultures grown in shake flasks and in a stirred tank. Enzyme Microb Technol 24:687–693

    Article  Google Scholar 

  • Sămaj J, Baluška F, Bobák M, Volkmann D (1999) Extracellular matrix surface network of embryogenic units of friable maize callus contains arabinogalactan-proteins recognized by monoclonal antibody JIM4. Plant Cell Rep 18:369–374

    Article  Google Scholar 

  • Seifert G, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161

    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 

  • Shi HZ, Kim YS, Guo Y, Stevenson B, Zhu JK (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal expansion. Plant Cell 15:19–32

    Article  PubMed  CAS  Google Scholar 

  • Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417

    Article  PubMed  CAS  Google Scholar 

  • Trejo-Tapia G, Rodríguez-Monroy M (2007) Cellular aggregation in secondary metabolite production in in vitro plant cell cultures. Interciencia 32:669–674

    Google Scholar 

  • Trejo-Tapia G, Hernández-Trujillo R, Trejo-Espino JL, Jimenéz-Aparicio A, Rodríguez-Monroy M (2003) Analysis of morphological characteristics of Solanum chrysotrichum cell suspension cultures. World J Microbiol Biotechnol 19:929–932

    Article  Google Scholar 

  • van Holst GJ, Clarke A (1985) Quantification of arabinogalactan-protein in plant extracts by single radial diffusion gel. Anal Biochem 148:446–450

    Article  PubMed  Google Scholar 

  • Vidal JR, Rama J, Taboada L, Martin C, Ibañez M, Segura A, González-Benito ME (2008) Improved somatic embryogenesis of grapevine (Vitis vinifera) with focus on induction parameters and efficient plant regeneration. Plant Cell Tiss Organ Cult 96:85–94

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wu HM, Wong E, Ogdahl J, Cheung AY (2000) A pollen tube growth-promoting arabinogalactan-protein from Nicotiana alata is similar to the tobacco TTS protein. Plant J 22:165–176

    Article  PubMed  CAS  Google Scholar 

  • Yamada H, Hirano T, Toshio Miyazaki T, Akira Takatsuki A, Tamura G (1982) Effects of tunicamycin on cell adhesion and biosynthesis of glycoproteins in aggregation-competent cells of Dictyostelium discoideum. J Biochem 92(2):399–406

    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 

Download references

Acknowledgments

This work was financed by SIP (grants #20100308 and #20100781). J. Capataz-Tafur is indebted to CONACyT for the doctoral fellowship awarded and PIFI-IPN.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gabriela Sepúlveda-Jiménez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Capataz-Tafur, J., Trejo-Tapia, G., Rodríguez-Monroy, M. et al. Arabinogalactan proteins are involved in cell aggregation of cell suspension cultures of Beta vulgaris L.. Plant Cell Tiss Organ Cult 106, 169–177 (2011). https://doi.org/10.1007/s11240-010-9905-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-010-9905-3

Keywords

Navigation