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Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes

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Abstract

Two lines of transgenic potato (Solanum tuberosum L.) plants modified in their cell wall structure were characterized and compared to wild type with regard to biomechanical properties in order to assign functional roles to the particular cell wall polysaccharides that were targeted by the genetic changes. The targeted polymer was rhamnogalacturonan I (RG-I), a complex pectic polysaccharide comprised of mainly neutral oligosaccharide side chains attached to a backbone of alternating rhamnosyl and galacturonosyl units. Tuber rhamnogalacturonan I molecules from the two transformed lines are reduced in linear galactans and branched arabinans, respectively. The transformed tuber tissues were found to be more brittle when subjected to uniaxial compression and the side-chain truncation was found to be correlated with the physical properties of the tissue. Interpretation of the force–deflection curves was aided by a mathematical model that describes the contribution of the cellulose microfibrils, and the results lead to the proposition that the pectic matrix plays a role in transmitting stresses to the load-bearing cellulose microfibrils and that even small changes to the rheological properties of the matrix have consequences for the biophysical properties of the wall.

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Fig. 1
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Abbreviations

RG-I (II) :

Rhamnogalacturonan I (II)

T13.1 :

Transformant with truncated galactan side chains of RG-I

T7.2 :

Transformant with truncated arabinan side chains of RG-I

WT :

Wild type

References

  • Alvarez MD, Canet W (1998) Rheological characterization of fresh and cooked potato tissues (cv. Monalisa). Z Lebensm Unters Forsch A 207:55-65

    Article  CAS  Google Scholar 

  • Baker DB, Ray PM (1965) The relation between the effects of auxin on cell wall synthesis and cell elongation. Plant Physiol 40:360–368

    Google Scholar 

  • Belton PS (1997) NMR and the mobility of water in polysaccharide gels. Int J Biol Macromol 21:81–88

    Article  CAS  PubMed  Google Scholar 

  • Bruce DM (2003) Mathematical modelling of the cellular mechanics of plants. Philos Trans R Soc Lond Ser B 358:1437–1444

    Article  Google Scholar 

  • Bush MS, Marry M, Huxam IM, Jarvis MC, McCann MC (2001) Developmental regulation of pectic epitopes during potato tuberization. Planta 213:869–880

    CAS  PubMed  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 walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Chanliaud E, Gidley MJ (1999) In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites. Plant J 20:25–35

    Article  CAS  PubMed  Google Scholar 

  • Davies GC, Hiller S, Bruce DM (1998) A membrane model for elastic deflection of individual plant cell walls. J Texture Stud 29: 645–667

    Google Scholar 

  • Falk S, Hertz CH, Virgin HI (1958) On the relation between turgor pressure and tissue rigidity. I. Experiments on resonance frequency and tissue rigidity. Physiol Plant 11:802–817

    Google Scholar 

  • Foster, TJ, Ablett S, McCann MC, Gidley MJ (1996) Mobility-resolved 13C-NMR spectroscopy of primary plant cell walls. Biopolymers 39:51–66

    Article  CAS  Google Scholar 

  • Fry SC (2000) The growing plant cell wall: chemical and metabolic analysis. The Blackburn Press, Caldwell, NJ

    Google Scholar 

  • Girault R, Bert F, Rihouey C, Jauneau A, Morvan C, Jarvis M (1997) Galactans and cellulose on flax fibres: putative contributions to the tensile strength. Int J Biol Macromol 21:179–188

    Article  CAS  PubMed  Google Scholar 

  • Goldberg R, Morvan C, Hervé du Penhoat C, Michon V (1989) Structure and properties of acidic polysaccharides from mung bean hypocotyls. Plant Cell Physiol 30:163–173

    CAS  Google Scholar 

  • Hepworth DG, Bruce DM (2000a) A method of calculating the mechanical properties of nanoscopic plant cell wall components from tissue properties. J Mater Sci 35:5861–5865

    Article  CAS  Google Scholar 

  • Hepworth DG, Bruce DM (2000b) Measuring the deformation of cells within a piece of compressed potato tuber tissue. Ann Bot 86:287–292

    Article  Google Scholar 

  • Hiller SH, Jeronimidis G (1996) Fracture in potato tuber parenchyma. J Mater Sci 31:2779–2796

    CAS  Google Scholar 

  • Hiller SH, Bruce DM, Jeronimidis G (1996) A micropenetration technique for mechanical testing of plant cell walls. J Texture Stud 27:559–587

    Google Scholar 

  • Huisman MMH, Fransen CTM, Kamerling JP, Vliegenthart JFG, Schols HA, Voragen AGJ (2001) The CDTA-soluble pectic substances from soybean meal are composed of rhamnogalacturonan and xylogalacturonan but not homogalacturonan. Biopolymers 58:279–294

    Article  CAS  PubMed  Google Scholar 

  • Hwang J, Pyun YR, Kokini JL (1993) Side chains of pectin: some thoughts on their role in plant cell walls and foods. Food Hydrocoll 7:39–53

    CAS  Google Scholar 

  • Jarvis MC, McCann MC (2000) Macromolecular biophysics of the plant cell wall: concepts and methodology. Plant Physiol Biochem 38:1–13

    Article  CAS  Google Scholar 

  • Jarvis MC, Hall MA, Threlfall DR, Friend J (1981) The polysaccharide structure of potato cell walls: chemical fractionation. Planta 152:93–100

    CAS  Google Scholar 

  • Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci USA 100:11783–11788

    Article  CAS  PubMed  Google Scholar 

  • Köhler L, Spatz H-C (2002) Micromechanics of plant tissues beyond the linear-elastic range. Planta 215:33–40

    Article  PubMed  Google Scholar 

  • Labavitch JM, Ray PM (1974) Turnover of cell wall polysaccharides in elongating pea stem segments. Plant Physiol 53:105–113

    Google Scholar 

  • Lau JM, McNeil M, Darvill AG, Albersheim P (1985) Structure of the backbone of rhmanogalacturonan I, a pectic polysaccharide in the primary walls of plants. Carbohydr Res 137:111–125

    Article  CAS  Google Scholar 

  • Mark RE (1967) Cell wall mechanics of tracheids. Yale University Press, New Haven

  • McCann MC, Roberts K (1994) Changes in cell wall architecture during cell elongation. J Exp Bot 45:1683–1691

    CAS  Google Scholar 

  • McCann MC, Bush M, Milioni D, Sado P, Stacey NJ, Catchpole G, Defernez M, Carpita NC, Höfte H, Ulvskov P, Wilson RH, Roberts K (2001) Approaches to understanding the functional architecture of the plant cell wall Phytochemistry 57:811–821

    Article  CAS  Google Scholar 

  • McCartnery L, Ormerod AP, Gidley MJ, Knox JP (2000) Temporal and spatial regulation of pectic (1→4)-β-d-galactan in cell walls of developing pea cotyledons. Plant J 22:105–113

    Article  CAS  PubMed  Google Scholar 

  • McCartney L, Steele-King CG, Jordan E, Knox JP (2003) Cell wall pectic (1→4)-β-d-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J 33:447–454

    Article  CAS  PubMed  Google Scholar 

  • Oomen RJFJ, Doeswijk-Voragen C, Bush MS, Vincken J-P, Borkhardt B, van den Broek LAM, Corsar J, Ulvskov P, Voragen AGJ, McCann MC, Visser RGF (2002) In muro fragmentation of the rhamnogalacturonan I backbone in potato (Solanum tuberosum) results in a reduction and altered location of the galactan and arabinan side-chains and abnormal periderm development. Plant J 30:1-12

    Article  PubMed  Google Scholar 

  • Ray PM (1962) Cell wall synthesis and cell elongation in oat coleoptile tissue. Am J Bot 49:928–939

    CAS  Google Scholar 

  • Ray PM (1967) Autoradiographic study of cell wall deposition in growing plant cells. J Cell Biol 35:659–674

    Article  CAS  PubMed  Google Scholar 

  • Renard CMGC, Jarvis MC (1999) A cross polarization, magic-angle-spinning, 13C-nuclear-magnetic-resonance study of polysaccharides in sugar beet cell walls. Plant Physiol 119:1315–1322

    Article  CAS  PubMed  Google Scholar 

  • Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967

    Article  CAS  PubMed  Google Scholar 

  • Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter W-D, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132:1033–1040

    Article  CAS  PubMed  Google Scholar 

  • Schols HA, Voragen AGJ (1994) Occurrence of pectic hairy regions in various plant cell wall materials and their degradability by rhamnogalacturonase. Carbohydr Res 256:83–95

    Article  CAS  Google Scholar 

  • Skjøt M, Kauppinen S, Kofod LV, Fuglsang CC, Pauly M, Dalbøge H, Andersen LN (2001) Functional cloning of an endo-arabinanase from Apergillus aculeatus and its heterologous expression in Aspergillus oryzae and tobacco. Mol Gen Genomics 265:913–921

    Article  Google Scholar 

  • Skjøt M, Pauly M, Bush MS, Borkhardt, B, McCann MC, Ulvskov P (2002) Direct interference with rhamnogalacturonan I biosynthesis in golgi vesicles. Plant Physiol 129:95–102

    Article  PubMed  Google Scholar 

  • Sørensen SO, Pauly M, Bush M, Skjøt M, McCann MC, Borkhardt B, Ulvskov P (2000) Pectin engineering: modification of potato pectin by in vivo expression of an endo-1,4-β-d-galactanase. Proc Natl Acad Sci USA97: 7639–7644

    Google Scholar 

  • Tang H, Belton PS, Ng A, Ryden P (1999) 13C MAS NMR studies of the effects of hydration on the cell walls of potatoes and chinese water chestnuts. J Agric Food Chem 47:510–217

    Article  CAS  PubMed  Google Scholar 

  • Thomas JR, Darvill AG, Albersheim P (1989) Rhamnogalacturonan I, a pectic polysaccharide that is a component of monocot cell-walls. Carbohydr Res 185:279–305

    Article  CAS  Google Scholar 

  • Vincken J-P (2000) Remodelling pectin structure in potato. In: de Vries GE Metzlaff K (eds) Phytosphere ‘99 —Highlights in European biotechnology. Elsevier, New York, pp 245–256

  • Vincken J-P, Schols HA, Oomen RJFJ, McCann MC, Ulvskov P, Voragen AGJ, Visser RGF (2003) If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol 132:1781–1789

    Article  CAS  PubMed  Google Scholar 

  • Virgin HI (1955) A new method for the determination of the turgor of plant tissues. Physiol Plant 8:954–962

    Google Scholar 

  • Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    Article  CAS  PubMed  Google Scholar 

  • Wilson RH, Smith AC, Kacuráková M, Saunders PK, Wellner N, Waldron KW (2000) The mechanical properties and molecular dynamics of plant cell wall polysaccharides studied by Fourier-transform infrared spectroscopy. Plant Physiol 124:397–405

    Article  CAS  PubMed  Google Scholar 

  • Whitney SEC, Gothard MGE, Mitchell JT, Gidley MJ (1999) Roles of cellulose and xyloglucan in determining the mechanical properties of primary cell walls. Plant Physiol 121:657–663

    Article  CAS  PubMed  Google Scholar 

  • Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291:1059–1062

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Vibeke Strange, Morten Laessøe Stephensen and Dorthe Christiansen are acknowledged for skillful technical assistance. Dr. Peter M. Ray is acknowledged for sharing his insights in cell wall biology and inspiring discussions while this manuscript was prepared. Søren Balling Engelsen is acknowledged for introducing us to the Mettler Moisture Analyzer. This investigation was supported by the Danish National Research Foundation. The Danish Research Agency is acknowledged for funding Michael Skjøt, and the work at Silsoe Research Institute was funded by SRI’s competitive strategic grant from the UK Biotechnology and Biological Sciences Research Council.

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Authors and Affiliations

  1. Biotechnology Group, Danish Institute of Agricultural Sciences, Thorvaldsensvej 40, 1871, Frederiksberg C, Denmark

    Peter Ulvskov, Bodil Jørgensen, Michael Skjøt & Bernhard Borkhardt

  2. Department of Dairy and Food Science and Centre for Advanced Food Studies, The Royal Veterinary and Agricultural University, Rolighedsvej 30, 1958, Frederiksberg C, Denmark

    Helle Wium & Karsten Bruun Qvist

  3. Biophysics Group, Silsoe Research Institute, Wrest Park, Silsoe, Bedford, MK45 4HS, UK

    David Bruce & David Hepworth

  4. Plant Biochemistry Laboratory, Department of Plant Biology, Royal Veterinary & Agricultural University, Thorvaldsensvej 40, 1871, Frederiksberg C, Denmark

    Susanne Oxenbøll Sørensen

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  1. Peter Ulvskov
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  2. Helle Wium
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  3. David Bruce
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Correspondence to Peter Ulvskov.

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Ulvskov, P., Wium, H., Bruce, D. et al. Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta 220, 609–620 (2005). https://doi.org/10.1007/s00425-004-1373-8

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  • DOI: https://doi.org/10.1007/s00425-004-1373-8

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