Skip to main content
Log in

Parenchyma cell wall structure in twining stem of Dioscorea balcanica

  • Original Paper
  • Published:
Cellulose Aims and scope Submit manuscript

A Correction to this article was published on 23 February 2018

This article has been updated

Abstract

Anatomical adaptation of liana plants includes structural changes in cell walls of different tissues: fibers, vessel elements and tracheids. However, the contribution of parenchyma cells to stem twining in liana plants is mostly unknown. The aim of this investigation is to determine changes in stem parenchyma cell walls that are correlated with the twinning process in liana plants. Parenchyma cell wall structure was studied on the stem cross sections of straight and twisted internodes of monocotyledonous liana Dioscorea balcanica, by different microscopy techniques: light microscopy, scanning electron microscopy, fluorescence detected linear dichroism microscopy and Fourier transform infrared microspectrometry. In addition, chemical analysis of the entire stem internodes was performed using photometric and chromatographic methods. Parenchyma cell walls of twisted D. balcanica internodes are characterized by: lower amounts of cellulose (obtained by FTIR microspectrometry) with different cellulose microfibril orientation (shown by Scanning electron microscopy), but no changes in “cellulose fibril order” (obtained by Differential polarization laser scanning microscopy); lower amounts of xyloglucan, higher amounts of xylan, higher amounts of lignin with modified organization—less condensed lignin (obtained by FTIR microspectrometry). At the same time, chemical analysis of the entire internodes did not show significant differences in lignin content and cell wall bound phenols related to stem twining, except for the presence of diferulate cross-links exclusively in twisted internodes. Our results indicate that adaptations to mechanical strain in D. balcanica stems involve modifications in parenchyma cell wall structure and chemistry, which provide decreased stiffness, higher strength and increased elasticity of twisted internodes.

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
Fig. 5
Fig. 6

Similar content being viewed by others

Change history

  • 23 February 2018

    In the original publication of the article, one of the project numbers was omitted in the Acknowledgments. The correct version is provided below.

References

  • Adams RP (2001) Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. Allured Publishing Corporation, Illinois

    Google Scholar 

  • Akerholm M, Salmen L (2001) Interactions between wood polymers studied by dynamic FT-IR spectroscopy. Polymer 42:963–969

    Article  CAS  Google Scholar 

  • Akerholm M, Hinterstoisser B, Salmén L (2004) Characterization of the crystalline structure of cellulose using static and dynamic FT-IR spectroscopy. Carbohydr Res 339:569–578

    Article  CAS  Google Scholar 

  • Alméras T, Clair B (2016) Critical review on the mechanisms of maturation stress generation in trees. J R Soc Interface 13:20160550. doi:10.1098/rsif.2016.0550

    Article  Google Scholar 

  • Atalla RH, Agarwal UP (1985) Raman microprobe evidence for lignin orientation in the cell walls of native woody tissue. Science 227:636–638

    Article  CAS  Google Scholar 

  • Barnet JR, Bonham VA (2004) Cellulose microfibril angle in the cell wall of wood fibres. Biol Rev 79:461–472

    Article  Google Scholar 

  • Berlyn GP, Miksche JP (1976) Botanical microtechnique and cytochemistry. The Iowa State University Press, Ames

    Google Scholar 

  • Bowling AJ, Vaughn KC (2009) Gelatinous fibers are widespread in coiling rendrils and twining vines. Am J Bot 96:719–727

    Article  Google Scholar 

  • Bunzel M, Ralph J, Lu F, Hatfield RD, Steinhart H (2004) Lignins and ferulate-coniferyl alcohol cross-coupling products in cereal grains. J Agric Food Chem 52:6496–6502

    Article  CAS  Google Scholar 

  • Burgert I, Fratzl P (2009) Plants control the properties and actuation of their organs through the orientation of cellulose fibrils in their cell walls. Integr Comp Biol 49:69–79

    Article  Google Scholar 

  • Carlquist S (1985) Observations on functional wood histology of vines and lianas: vessel dimorphism, tracheids, vasicentric tracheids, narrow vessels, and parenchyma. Aliso 11:139–157

    Article  Google Scholar 

  • Carlquist S (2015) Living cells in wood. 1. Absence, scarcity and histology of axial parenchyma as keys to function. Bot J Linn Soc 177:291–321

    Article  Google Scholar 

  • Chen M, Sommer AJ, McClure JW (2000) Fourier transform-IR determination of protein contamination in thioglycolic acid lignin from radish seedlings, and improved methods for extractive-free cell wall preparation. Phytochem Anal 11:153–159

    Article  CAS  Google Scholar 

  • Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3:204

    Article  Google Scholar 

  • Donaldson LA (2001) Lignification and lignin topochemistry—an ultrastructural view. Phytochem 57:859–873

    Article  CAS  Google Scholar 

  • Donaldson LA, Knox JP (2012) Localization of cell wall polysaccharides in normal and compression wood of radiata pine: relationships with lignification and microfibril orientation. Plant Physiol 158:642–653

    Article  CAS  Google Scholar 

  • Donaldson LA, Nanayakkara B, Radotić K, Djikanović Golubović D, Mitrović A, Bogdanović Pristov J, Simonović Radosavljević J, Kalauzi A (2015) Xylem parenchyma cell walls lack a gravitropic response in conifer compression wood. Planta 242:413–1424

    Article  Google Scholar 

  • Faix O (1991) Classification of lignins from different botanical origins by FTIR spectroscopy. Holzforschung 45:21–27

    Article  CAS  Google Scholar 

  • Fergus BJ, Goring DAI (1970) The distribution of lignin in birch wood as determined by ultraviolet microscopy. Holzforschung 24:118–124

    Article  CAS  Google Scholar 

  • Fergus BJ, Procter AR, Scott JAN, Goring DAI (1969) The distribution of lignin in spruce wood as determined by ultra-violet microscopy. Wood Sci Technol 3:117–138

    Article  Google Scholar 

  • Fry SC, Miller JC (1989) Toward a working model of the growing plant cell wall. Phenolic cross-linking reactions in the primary cell walls of dicotyledons. In: Lewis NG, Paice MG (eds) Plant cell wall polymers, biogenesis and biodegradation, vol 399. American Chemical Society, Washington, DC, pp 33–46

    Chapter  Google Scholar 

  • Garab G, Pomozi I, Jörgens R, Weiss G (2005) Method and apparatus for determining the polarization properties of light emitted, reflected or transmitted by a material using a laser scanning microscope. US Patent 6,856,391

  • Grabber JH, Ralph J, Hatfield RD (2002) Model studies of ferulate-coniferyl alcohol cross-product formation in primary maize walls: implications for lignification in grasses. J Agric Food Chem 50:6008–6016

    Article  CAS  Google Scholar 

  • Hatfield RD, Ralph J, Grabber JH (1999) Cell wall cross-linking by ferulates and diferulates in grasses. J Sci Food Agric 79:403–407

    Article  CAS  Google Scholar 

  • Hayashi T (1989) Xyloglucans in the primary-cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168

    Article  CAS  Google Scholar 

  • He XQ, Suzuki K, Kitamura S, Lin JX, Cui KM, Itoh T (2002) Toward understanding the different function of two types of parenchyma cells in bamboo culms. Plant Cell Physiol 43:186–195

    Article  CAS  Google Scholar 

  • Ishii T (1991) Isolation and characterization of diferuloyl arabinoxylan hexasaccharide from bamboo shoot cell-wall. Carbohydr Res 219:15–22

    Article  CAS  Google Scholar 

  • Ishii T, Hiroi T (1990) Isolation and characterization of feruloylated arabinoxylan oligosaccharides from bamboo shoot cell-walls. Carbohydr Res 196:175–183

    Article  CAS  Google Scholar 

  • Isnard S, Silk WK (2009) Moving with climbing plants from Charles Darwin’s time into the 21st century. Am J Bot 96:1205–1221

    Article  Google Scholar 

  • Iwata T, Indrarti L, Azuma J-I (1998) Affinity of hemicellulose for cellulose produced by Acetobacter xylinum. Cellulose 5:215–228

    Article  CAS  Google Scholar 

  • Jacquet G, Pollet B, Lapierre C (1995) New ether-linked ferulic acid-coniferyl alcohol dimers identified in grass straws. J Agric Food Chem 43:2746–2751

    Article  CAS  Google Scholar 

  • Jensen WA (1962) Botanical histochemistry: principles and practice. W.H. Freeman and Company San Francisco, California

    Google Scholar 

  • Kačuráková M, Smith AC, Gidley MJ, Wilson RH (2002) Molecular interactions in bacterial cellulose composites studied by 1D FT-IR and dynamic 2D FT-IR spectroscopy. Carbohydr Res 337:1145–1153

    Article  Google Scholar 

  • Kim JS, Daniel G (2012) Distribution of glucomannans and xylans in poplar xylem and their changes under tension stress. Planta 236:35–50

    Article  CAS  Google Scholar 

  • Köhler L, Speck T, Spatz HC (2000) Micromechanics and anatomical changes during early ontogeny of two lianescent Aristolochia species. Planta 210:691–700

    Article  Google Scholar 

  • Lam TBT, Iiyama K, Stone BA (1992) Cinnamic acid bridges between cell wall polymers in wheat and Phalaris internodes. Phytochem 32:1179–1183

    Google Scholar 

  • Lam MSJWQ, Martinez Y, Barbier O, Jauneau A, Pichon M (2013) Maize cell wall degradability, from whole plant to tissue level: different scales of complexity. Maydica 58:103–110

    Google Scholar 

  • Liang CY, Basset KH, McGinnes EA, Marchessault RH (1960) Infrared spectra of crystalline polysaccharides; VII. Thin wood sections. Tappi 43:232–235

    Google Scholar 

  • Marchessault RH (1962) Application of infra-red spectroscopy to cellulose and wood polysaccharides. Pure Appl Chem 5:107–129

    Article  CAS  Google Scholar 

  • McCann MC, Hammouri M, Wilson R, Belton P, Roberts K (1992) Fourier transform infrared micro-spectroscopy is a new way to look at plant cell walls. Plant Physiol 100:1940–1947

    Article  CAS  Google Scholar 

  • Mellerowicz EJ, Gorshkova TA (2011) Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. J Exp Bot 63:551–565

    Article  Google Scholar 

  • Meloche CG, Knox JP, Vaughn KC (2007) A cortical band of gelatinous fibers causes the coiling of redvine tendrils: a model based upon cytochemical and immunocytochemical studies. Planta 225:485–498

    Article  CAS  Google Scholar 

  • Morrison IM (1972) A semi-micro method for the determination of lignin and its use in predicting the digestibility of forage crops. Sci Food Agric 23:455–463

    Article  CAS  Google Scholar 

  • Mouille G, Robin S, Lecompte M, Pagant S, Höfte H (2003) Classification and identification of Arabidopsis wall mutants using Fourier-Transform InfraRed (FT-IR) microspectroscopy. Plant J 35:393–404

    Article  CAS  Google Scholar 

  • Obel N, Porchia AC, Scheller HV (2003) Intracellular feroloylation of arabinoxylan in wheat: evidence for feruloyl-glucose as precursor. Planta 216:620–629

    CAS  Google Scholar 

  • O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue-O. Protoplasma 59:368–373

    Article  Google Scholar 

  • Pretsch E, Seibl J, Simon W (1982) Tabellen zur strukturaufklarung organischer verbindungen mit spektroskopischen methoden. Springer Verlag, Berlin Heidelberg

    Google Scholar 

  • Pruyn ML (2007) Parencyma. In: Roberts K (ed) Handbook of plant science, vol 2. Wiley, USA, pp 170–180

    Google Scholar 

  • Pulević V (1973) Protected plant species in SR Montenegro. Glasnik Republičkog zavoda za Zaštitu Prirode. Prirodnjački Muzej u Titogradu 16:33–34 (in Serbian)

    Google Scholar 

  • Quideau S, Ralph J (1997) Lignin–ferulate cross-links in grasses. Part 4. 1–3 Incorporation of 5-5-coupled dehydrodiferulate into synthetic lignin. J Chem Soc 1:2351–2358 (Perkin Trans)

    Google Scholar 

  • Radotić K, Todorović S, Zakrzewska J, Jeremić M (1998) Study of photochemical reactions of coniferyl alcohol. II. Comparative structural study of a photochemical and enzymatic polymer of coniferyl alcohol. Photochem Photobiol 68:703–709

    Article  Google Scholar 

  • Ralph J, Helm RF, Quideau S, Hatfield RD (1992) Lignin-feruloyl ester crosslinks in grasses. Part 1. Incorporation of feruloyl esters into coniferyl alcohol dehydrogenation polymers. J Chem Soc 1:2961–2969 (Perkin Trans)

    Google Scholar 

  • Ralph J, Hatfield RD, Grabber JH, Jung HG, Quideau S, Helm RF (1998) Cell wall cross-linking in grasses by ferulates and diferulates. In: Lewis NG, Sarkanen S (eds) Lignin and lignan biosynthesis, vol 697. American Chemical Society symposium series. American Chemical Society, Washington, pp 209–236

    Chapter  Google Scholar 

  • Reis D, Vian B (2004) Helicoidal pattern in secondary cell walls and possible role of xylans in their construction. C R Biol 327:785–790

    Article  CAS  Google Scholar 

  • Robin S, Lecomte M, Höfte H, Mouille G (2003) A procedure for the clustering of cell wall mutants in the model plant Arabidopsis based on Fourier-transform infrared (FT-IR) spectroscopy. J Appl Stat 30:669–681

    Article  Google Scholar 

  • Roussel JR, Clair B (2015) Evidence of the late lignification of the G-layer in Simarouba tension wood, to assist understanding how non-G-layer species produce tensile stress. Tree Physiol 35:1366–1377. doi:10.1093/treephys/tpv082

    Article  Google Scholar 

  • Ruelle J (2014) Morphology, anatomy and ultrastructure of reaction wood. In: Gardiner B, et al. (eds) The biology of reaction wood, Springer series in wood science. Springer, Berlin, pp 13–35. doi:10.1007/978-3-642-10814-3_2

  • Ruelle J, Yamamoto H, Thibaut B (2007) Growth stress and cellulose structural parameters in tension and normal wood from three tropical rainforest angiosperms species. BioResources 2:235–251

    CAS  Google Scholar 

  • Savić A, Mitrović A, Donaldson L, Simonović Radosavljević J, Bogdanović Pristov J, Steinbach G, Garab G, Radotić K (2016) Fluorescence-detected linear dichroism of wood cell walls in juvenile Serbian spruce: estimation of compression wood severity. Microsc Microanal 22:361–367

    Article  Google Scholar 

  • Scalbert A, Monties B, Lallemand JY, Guittet E, Rolando C (1985) Ether linkage between phenolic acids and lignin fractions from wheat straw. Phytochem 24:1359–1362

    Article  CAS  Google Scholar 

  • Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289

    Article  CAS  Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic- phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T et al (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211

    Article  CAS  Google Scholar 

  • Spicer R (2014) Symplasmic networks in vascular tissues: parenchyma distribution and activity supporting long distance transport. J Exp Bot 65:1829–1848

    Article  CAS  Google Scholar 

  • Steinbach G, Pomozi I, Zsiros O, Páy A, Horváth GV, Garab G (2008) Imaging fluorescence detected linear dichroism of plant cell walls in laser scanning confocal microscope. Cytometry 73A:202–208

    Article  Google Scholar 

  • Steinbach G, Pomozi I, Zsiros O, Menczel L, Garab G (2009) Imaging anisotropy using differential polarization laser scanning confocal microscopy. Acta Histochem 111:316–325

    Article  Google Scholar 

  • Strack D, Heilemann J, Wray V, Dirks H (1988) Structures and accumulation patterns of soluble and insoluble phenolics from Norway spruce needles. Phytochem 28:2071–2078

    Article  Google Scholar 

  • Sun R, Sun XF, Wang SQ, Zhu W, Wang XY (2002) Ester and ether linkages between hydroxycinnamic acids and lignins from wheat, rice, rye, and barley straws, maize stems, and fast-growing poplar wood. Ind Crop Prod 15:179–188

    Article  CAS  Google Scholar 

  • Verbelen JP, Stickens D (1995) In vivo determination of fibril orientation in plant cell walls with polarization CSLM. J Microsc 177:101–107

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by: the Grants 173017 and 173015 of the Ministry of education and science of the Republic of Serbia, Project Algamic (CZ 1.05/2.1.00/19.0392) of Czech Republic. The authors wish to thank Prof. Ljubinka Ćulafić for providing D. balcanica photographs.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ksenija Radotić.

Additional information

A correction to this article is available online at https://doi.org/10.1007/s10570-018-1706-6.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Simonović Radosavljević, J., Bogdanović Pristov, J., Lj. Mitrović, A. et al. Parenchyma cell wall structure in twining stem of Dioscorea balcanica . Cellulose 24, 4653–4669 (2017). https://doi.org/10.1007/s10570-017-1460-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10570-017-1460-1

Keywords

Navigation