Abstract
Cellulose microfibril orientation in plant cell walls changes during cell expansion and development. The cellulose microfibril orientation in the abaxial epidermis of onion scales was studied by atomic force microscopy (AFM) and sum frequency generation (SFG) vibrational spectroscopy. Onion epidermal cells in all scales are elongated along the onion bulb axis. AFM images showed that cellulose microfibrils exposed at the innermost surface of the abaxial epidermis are oriented perpendicular to the bulb axis in the outer scales and more dispersed in the inner scales of onion bulb. SFG analyses can determine the orientation of cellulose microfibrils averaged over the entire thickness of the cell wall. We found that the average orientation of cellulose microfibrils inside onion abaxial epidermal cell walls as revealed by SFG is similar to the orientation observed at the innermost cell wall surface by AFM. The capability to determine the average orientation of cellulose microfibrils in intact cell walls will be useful to study how cellulose microfibril orientation is related to biomechanical properties and the growth mechanism of plant cell walls.
This is a preview of subscription content, access via your institution.







References
Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152(2):787–796
Barnette AL, Bradley LC, Veres BD, Schreiner EP, Park YB, Park J, Park S, Kim SH (2011) Selective detection of crystalline cellulose in plant cell walls with sum-frequency-generation (SFG) vibration spectroscopy. Biomacromolecules 12(7):2434–2439
Barnette AL, Lee C, Bradley LC, Schreiner EP, Park YB, Shin H, Cosgrove DJ, Park S, Kim SH (2012) Quantification of crystalline cellulose in lignocellulosic biomass using sum frequency generation (SFG) vibration spectroscopy and comparison with other analytical methods. Carbohydr Polym 89(3):802–809
Baskin T (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222
Brown RM Jr, Millard AC, Campagnola PJ (2003) Macromolecular structure of cellulose studied by second-harmonic generation imaging microscopy. Opt Lett 28(22):2207–2209
Chen L, Wilson RH, McCann MC (1997) Investigation of macromolecule orientation in dry and hydrated walls of single onion epidermal cells by FTIR microspectroscopy. J Mol Struct 408:257–260
Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38(1):109–124
Cox G, Moreno N, Feijó J (2005) Second-harmonic imaging of plant polysaccharides. J Biomed Opt 10(2):024013
Davies LM, Harris PJ (2003) Atomic force microscopy of microfibrils in primary cell walls. Planta 217(2):283–289
Ding SY, Himmel ME (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. J Agric Food Chem 54(3):597–606
Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356
Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC (2011) Nanostructure of cellulose microfibrils in spruce wood. PNAS 108(47):E1195–E1203
Giddings TH Jr, Staehelin LA (1988) Spatial relationship between microtubules and plasma-membrane rosettes during the deposition of primary wall microfibrils in Closterium sp. Planta 173(1):22–30
Green PB (1960) Multinet growth in the cell wall of Nitella. J Biophys Biochem Cytol 7(2):289–296
Green PB (1962) Mechanism for plant cellular morphogenesis. Science 138(3548):1404–1405
Green P (1964) Cell walls and the geometry of plant growth. Brookhaven Symp Biol 16:203–217
Ha MA, Apperley DC, Jarvis MC (1997) Molecular rigidity in dry and hydrated onion cell walls. Plant Physiol 115(2):593–598
Heath IB (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J Theor Biol 48(2):445–449
Hieu HC, Tuan NA, Li H, Miyauchi Y, Mizutani G (2011) Sum frequency generation microscopy study of cellulose fibers. Appl Spectrosc 65(11):1254–1259
Hutter JL, Bechhoefer J (1993) Calibration of atomic-force microscope tips. Rev Sci Instrum 64:1868
Kutschera U (2008) The growing outer epidermal wall: design and physiological role of a composite structure. Ann Bot 101(5):615–621
LaComb R, Nadiarnykh O, Townsend SS, Campagnola PJ (2008) Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology. Opt Commun 281(7):1823–1832
Lambert AG, Davies PB, Neivandt DJ (2005) Implementing the theory of sum frequency generation vibrational spectroscopy: a tutorial review. Appl Spectrosc Rev 40(2):103–145
Lee CM, Mittal A, Barnette AL, Kafle K, Park Y, Shin H, Johnson DK, Park S, Kim SH (2013a) Cellulose polymorphism study with sum-frequency-generation (SFG) vibration spectroscopy: identification of exocyclic CH2OH conformation and chain orientation. Cellulose 20(3):991–1000
Lee CM, Mohamed NMA, Watts HD, Kubicki JD, Kim SH (2013b) Sum-frequency-generation vibration spectroscopy and density functional theory calculations with dispersion corrections (DFT-D2) for cellulose Iα and Iβ. J Phys Chem B 117(22):6681–6692
Li S, Gu Y (2012) Cellulose biosynthesis in higher plants and the role of the cytoskeleton. In: Hetherington AM (ed) eLS. Wiley, Chichester, pp 1–8
Marechal Y, Chanzy H (2000) The hydrogen bond network in Iβ cellulose as observed by infrared spectrometry. J Mol Struct 523(1):183–196
Marga F, Grandbois M, Cosgrove DJ, Baskin TI (2005) Cell wall extension results in the coordinate separation of parallel microfibrils: evidence from scanning electron microscopy and atomic force microscopy. Plant J 43(2):181–190
McCann M, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96(2):323–334
Mita T, Shibaoka H (1983) Changes in microtubules in onion leaf sheath cells during bulb development. Plant Cell Physiol 24(1):109–117
Neville A (1985) Molecular and mechanical aspects of helicoid development in plant cell walls. BioEssays 3(1):4–8
Neville A, Gubb D, Crawford R (1976) A new model for cellulose architecture in some plant cell walls. Protoplasma 90(3–4):307–317
Ng A, Parker ML, Parr AJ, Saunders PK, Smith AC, Waldron KW (2000) Physicochemical characteristics of onion (Allium cepa L.) tissues. J Agric Food Chem 48(11):5612–5617
Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312(5779):1491–1495
Park YB, Lee CM, Koo B-W, Park S, Cosgrove DJ, Kim SH (2013) Monitoring meso-scale ordering of cellulose in intact plant cell walls using sum frequency generation spectroscopy. Plant Physiol 163(2):907–913
Preston RD (1974) The physical biology of plant cell walls. Chapman & Hall, London
Richmond PA, Métraux JP, Taiz L (1980) Cell expansion patterns and directionality of wall mechanical properties in Nitella. Plant Physiol 65(2):211–217
Roelofsen PA, Houwink A (1953) Architecture and growth of the primary cell wall in some plant hairs and in the Phycomyces sporangiophore. Acta Bot Ner 2:218–225
Roland J-C, Vian B, Reis D (1977) Further observations on cell wall morphogenesis and polysaccharide arrangement during plant growth. Protoplasma 91(2):125–141
Satiat-Jeunemaifre B, Martin B, Hawes C (1992) Plant cell wall architecture is revealed by rapid-freezing and deep-etching. Protoplasma 167(1–2):33–42
Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol 124(4):1493–1506
Suslov D, Verbelen JP, Vissenberg K (2009) Onion epidermis as a new model to study the control of growth anisotropy in higher plants. J Exp Bot 60(14):4175–4187
Thimm JC, Burritt DJ, Ducker WA, Melton LD (2000) Celery (Apium graveolens L.) parenchyma cell walls examined by atomic force microscopy: effect of dehydration on cellulose microfibrils. Planta 212(1):25–32
Thomas LH, Forsyth VT, Šturcová A, Kennedy CJ, May RP, Altaner CM, Apperley DC, Wess TJ, Jarvis MC (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol 161(1):465–476
Wang H-F, Gan W, Lu R, Rao Y, Wu B-H (2005) Quantitative spectral and orientational analysis in surface sum frequency generation vibrational spectroscopy (SFG-VS). Int Rev Phys Chem 24(2):191–256
Wellner N, Kačuráková M, Malovíková A, Wilson RH, Belton PS (1998) FT-IR study of pectate and pectinate gels formed by divalent cations. Carbohydr Res 308(1):123–131
Wells B, McCann M, Shedletzky E, Delmer D, Roberts K (1994) Structural features of cell walls from tomato cells adapted to grow on the herbicide 2,6-dichlorobenzonitrile. J Microsc 173(2):155–164
Wiley JH, Atalla RH (1987) Band assignments in the Raman spectra of celluloses. Carbohydr Res 160:113–129
Wilson RH, Smith AC, Kačuráková 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(1):397–406
Wood PJ (1980) Specificity in the interaction of direct dyes with polysaccharides. Carbohydr Res 85(2):271–287
Wood PJ, Fulcher R, Stone BA (1983) Studies on the specificity of interaction of cereal cell wall components with Congo Red and Calcofluor. Specific detection and histochemistry of (1 → 3), (1 → 4),-β-D-glucan. J Cereal Sci 1(2):95–110
Yoneda A, Ito T, Higaki T, Kutsuna N, Saito T, Ishimizu T, Osada H, Hasezawa S, Matsui M, Demura T (2010) Cobtorin target analysis reveals that pectin functions in the deposition of cellulose microfibrils in parallel with cortical microtubules. Plant J 64(4):657–667
Zhang T, Mahgsoudy-Louyeh S, Tittmann B, Cosgrove D (2013) Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis. Cellulose 1–10. doi:10.1007/s10570-013-9996-1
Zugenmaier P (2008) Crystalline cellulose and derivatives. In: Timell TE, Wimmer R (eds) Springer series in wood science. Springer, Berlin, pp 101–174
Acknowledgments
This work was supported by The Center for Lignocellulose Structure and Formation, an Energy Frontier Research Center funded by the US Department of Energy, Office of Science, and Office of Basic Energy Sciences under award number DE-SC0001090. We acknowledge Anthony J. Barthel for help with optical profilometry measurements, Liza Wilson with FTIR, and Lin Fang with 2D XRD measurements.
Author information
Affiliations
Corresponding authors
Electronic Supplementary Material
Below is the link to the Electronic Supplementary Material.
Rights and permissions
About this article
Cite this article
Kafle, K., Xi, X., Lee, C.M. et al. Cellulose microfibril orientation in onion (Allium cepa L.) epidermis studied by atomic force microscopy (AFM) and vibrational sum frequency generation (SFG) spectroscopy. Cellulose 21, 1075–1086 (2014). https://doi.org/10.1007/s10570-013-0121-2
Received:
Accepted:
Published:
Issue Date:
Keywords
- Onion epidermis
- Cellulose microfibril
- Microfibril orientation
- Sum frequency generation spectroscopy
- Atomic force microscopy