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Structural Insight into Cell Wall Architecture of Micanthus sinensis cv. using Correlative Microscopy Approaches

Published online by Cambridge University Press:  11 September 2015

Jianfeng Ma ,
Xunli Lv ,
Shumin Yang ,
Genlin Tian  and
Xing’e Liu
Jianfeng Ma
Affiliation:
International Center for Bamboo and Rattan, Beijing 100102, China
Xunli Lv
Affiliation:
Shiyan Middle School, Shaanxi province, Xianyang 712000, China
Shumin Yang
Affiliation:
International Center for Bamboo and Rattan, Beijing 100102, China
Genlin Tian
Affiliation:
International Center for Bamboo and Rattan, Beijing 100102, China
Xing’e Liu*
Affiliation:
International Center for Bamboo and Rattan, Beijing 100102, China
*
*Corresponding author.mjfxl31@126.com
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Abstract

Structural organization of the plant cell wall is a key parameter for understanding anisotropic plant growth and mechanical behavior. Four imaging platforms were used to investigate the cell wall architecture of Miscanthus sinensis cv. internode tissue. Using transmission electron microscopy with potassium permanganate, we found a great degree of inhomogeneity in the layering structure (4–9 layers) of the sclerenchymatic fiber (Sf). However, the xylem vessel showed a single layer. Atomic force microscopy images revealed that the cellulose microfibrils (Mfs) deposited in the primary wall of the protoxylem vessel (Pxv) were disordered, while the secondary wall was composed of Mfs oriented in parallel in the cross and longitudinal section. Furthermore, Raman spectroscopy images indicated no variation in the Mf orientation of Pxv and the Mfs in Pxv were oriented more perpendicular to the cell axis than that of Sfs. Based on the integrated results, we have proposed an architectural model of Pxv composed of two layers: an outermost primary wall composed of a meshwork of Mfs and inner secondary wall containing parallel Mfs. This proposed model will support future ultrastructural analysis of plant cell walls in heterogeneous tissues, an area of increasing scientific interest particularly for liquid biofuel processing.

Keywords

layering structurecellulose microfibrils orientationTEMAFMconfocal Raman microscopy
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 21 , Supplement 5 , October 2015 , pp. 1304 - 1313
Copyright
© Microscopy Society of America 2015 

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References

Abe, H. & Funada, R. (2005). Review – The orientation of cellulose microfibrils in the cell walls of tracheids in conifers. IAWA J 26(2), 161–174.Google Scholar
Agarwal, U.P. & Atalla, R.H. (1986). In-situ Raman microprobe studies of plant cell walls: Macromolecular organization and compositional variability in the secondary wall of Picea mariana (Mill.) B.S.P. Planta 169(3), 325–332.CrossRefGoogle Scholar
Brandstrom, J., Bardage, S.L., Daniel, G. & Nilsson, T. (2003). The structural organisation of the S1 cell wall layer of Norway spruce tracheids. IAWA J 24(1), 27–40.CrossRefGoogle Scholar
Brandt, B., Zollfrank, C., Franke, O., Fromm, J., Göken, M. & Durst, K. (2010). Micromechanics and ultrastructure of pyrolysed softwood cell walls. Acta Biomater 6(11), 4345–4351.CrossRefGoogle ScholarPubMed
Chaffey, N., Barlow, P. & Sundberg, B. (2002). Understanding the role of the cytoskeleton in wood formation in angiosperm trees: hybrid aspen (Populus tremula × P. tremuloides) as the model species. Tree physiol 22(4), 239–249.Google Scholar
Cosgrove, D.J. (2005). Growth of the plant cell wall. Nat Rev Mol Cell Bio 6(11), 850–861.CrossRefGoogle ScholarPubMed
Davies, L.M. & Harris, P.J. (2003). Atomic force microscopy of microfibrils in primary cell walls. Planta 217(2), 283–289.CrossRefGoogle ScholarPubMed
Ding, S.Y. & Himmel, M.E. (2006). The maize primary cell wall microfibril: A new model derived from direct visualization. J Agric Food Chem 54(3), 597–606.CrossRefGoogle ScholarPubMed
Ding, S.Y., Zhao, S. & Zeng, Y.N. (2014). Size, shape, and arrangement of native cellulose fibrils in maize cell walls. Cellulose 21(2), 863–871.Google Scholar
Donaldson, L. (2008). Microfibril angle: Measurement, variation and relationships – A review. IAWA J 29(4), 345–386.CrossRefGoogle Scholar
Donaldson, L. & Xu, P. (2005). Microfibril orientation across the secondary cell wall of Radiata pine tracheids. Trees Struct Funct 19(6), 644–653.CrossRefGoogle Scholar
Downes, G., Evans, R., Wimmer, R., French, J., Farrington, A. & Lock, P. (2003). Wood, pulp and handsheet relationships in plantation grown Eucalyptus globulus. Appita J 56(3), 221–228.Google Scholar
Fahlén, J. & Salmén, L. (2005). Pore and matrix distribution in the fiber wall revealed by atomic force microscopy and image analysis. Biomacromolecules 6(1), 433–438.Google Scholar
Gierlinger, N., Luss, S., Koenig, C., Konnerth, J., Eder, M. & Fratzl, P. (2010). Cellulose microfibril orientation of Picea abies and its variability at the micron-level determined by Raman imaging. J Exp Bot 61(2), 587–595.Google Scholar
Gierlinger, N. & Schwanninger, M. (2007). The potential of Raman microscopy and Raman imaging in plant research. Spectroscopy 21(2), 69–89.CrossRefGoogle Scholar
Gritsch, C.S., Kleist, G. & Murphy, R.J. (2004). Developmental changes in cell wall structure of phloem fibres of the Bamboo Dendrocalamus asper . Ann Bot 9(4), 497–505.Google Scholar
Gritsch, C.S. & Murphy, R.J. (2005). Ultrastructure of fibre and parenchyma cell walls during early stages of culm development in Dendrocalamus asper . Ann Bot 95(4), 619–629.Google Scholar
Hanley, S.J., Giasson, J., Revol, J.F. & Gray, D.G. (1992). Atomic force microscopy of cellulose microfibrils: Comparison with transmission electron microscopy. Polymer (Guildf) 33(21), 4639–4642.CrossRefGoogle Scholar
Hanley, S.J., Revol, J.F., Godbout, L. & Gray, D.G. (1997). Atomic force microscopy and transmission electron microscopy of cellulose from Micrasterias denticulata; evidence for a chiral helical microfibril twist. Cellulose 4(3), 209–220.CrossRefGoogle Scholar
Himmel, M.E., Ding, S.Y., Johnson, D.K., Adney, W.S., Nimlos, M.R., Brady, J.W. & Foust, T.D. (2007). Biomass recalcitrance: Engineering plants and enzymes for biofuels production. Science 315(5813), 804–807.CrossRefGoogle ScholarPubMed
Karam, G.N. (2005). Biomechanical model of the xylem vessels in vascular plants. Ann Bot 95(7), 1179–1186.CrossRefGoogle ScholarPubMed
Kim, J.S., Awano, T., Yoshinaga, A. & Takabe, K. (2010). Immunolocalization of beta-1-4-galactan and its relationship with lignin distribution in developing compression wood of Cryptomeria japonica . Planta 232(1), 109–119.CrossRefGoogle ScholarPubMed
Kim, J.S., Lee, K.H., Cho, C.H., Koch, G. & Kim, Y.S. (2008). Micromorphological characteristics and lignin distribution in bamboo (Phyllostachys pubescens) degraded by the white rot fungus Lentinus edodes . Holzforschung 62(4), 481–487.CrossRefGoogle Scholar
Ma, J.F., Ji, Z., Zhou, X., Zhang, Z.H. & Xu, F. ( 2013). Transmission electron microscopy, fluorescence microscopy, and confocal Raman microscopic analysis of ultrastructural and compositional heterogeneity of Cornus alba L. wood cell wall. Microsc Microanal 19(1), 243–253.CrossRefGoogle Scholar
Ma, J.F., Zhang, Z.H., Yang, G., Mao, J. & Xu, F. (2011). Ultrastructural topochemistry of cell wall polymers in Populus nigra by transmission electron microscopy and Raman imaging. Bioresources 6(4), 3944–3959.Google Scholar
Ma, J.F., Zhou, X., Ma, J., Ji, Z., Zhang, Z.H. & Xu, F. ( 2014). Raman microspectroscopy imaging study on topochemical correlation between lignin and hydroxycinnamic acids in Miscanthus sinensis . Microsc Microanal 20(3), 956–963.Google Scholar
Mayo, S.C., Chen, F. & Evans, R. (2010). Micron-scale 3D imaging of wood and plant microstructure using high-resolution X-ray phase-contrast microtomography. J Struct Biol 171(2), 182–188.Google Scholar
Mott, L., Groom, L. & Shaler, S. (2002). Mechanical properties of individual southern pine fibers. Part II. Comparison of earlywood and latewood fibers with respect to tree height and juvenility. Wood Fiber Sci 34(2), 221–237.Google Scholar
Murphy, R.J. & Alvin, K.L. (1992). Variation in fiber wall structure in bamboo. IAWA J 13(4), 403–410.Google Scholar
Murphy, R.J., Sulaiman, O. & Alvin, K.L. (1997). Ultrastructural aspects of cell wall organization in bamboos. In Linnean Society Symposium Series, The Bamboos, Chapman, G.P. (ed.), pp. 305–312. London: Academic Press.Google Scholar
Preston, R.D. (1934). The organization of the cell wall of the conifer tracheid. Philos Trans R Soc Lond B 224, 131–145.Google Scholar
Prislan, P., Koch, G., Schmitt, U., Gricar, J. & Cufar, K. (2012). Cellular and topochemical characteristics of secondary changes in bark tissues of beech (Fagus sylvatica). Holzforschung 66(1), 131–138.Google Scholar
Rehbein, M., Koch, G., Schmitt, U. & Huckfeldt, T. (2013). Topochemical and transmission electron microscopic studies of bacterial decay in pine (Pinus sylvestris L.) harbour foundation piles. Micron 44, 150–158.Google Scholar
Richter, S., Müssig, J. & Gierlinger, N. (2011). Functional plant cell wall design revealed by the Raman imaging approach. Planta 233(4), 763–772.Google Scholar
Rueggeberg, M., Saxe, F., Metzger, T.H., Sundberg, B., Fratzl, P. & Burgert, I. (2013). Enhanced cellulose orientation analysis in complex model plant tissues. J Struct Bio 183(3), 419–428.CrossRefGoogle Scholar
Ruelle, J., Yoshida, M., Clair, B. & Thibaut, B. (2007). Peculiar tension wood structure in Laetia procera (Poepp.) Eichl. (Flacourtiaceae). Trees Struct Funct 21(3), 345–355.Google Scholar
Singh, A.P., Daniel, G. & Nilsson, T. (2002). Ultrastructure of the S2 layer in relation to lignin distribution in Pinus radiata tracheids. J Wood Sci 48(2), 95–98.Google Scholar
Singh, A.P. & Donaldson, L.A. (1999). Ultrastructure of tracheid cell walls in radiata pine (Pinus radiata) mild compression wood. Can J Bot 77(1), 32–40.Google Scholar
Slavov, G., Allison, G. & Bosch, M. (2013). Advances in the genetic dissection of plant cell walls: Tools and resources available in Miscanthus . Front Plant Sci 4(217), 1–21.Google Scholar
Tetard, L., Passian, A., Farahi, R.H., Kalluri, U.C., Davison, B.H. & Thundat, T. (2010). Spectroscopy and atomic force microscopy of biomass. Ultramicroscopy 110(6), 701–707.CrossRefGoogle ScholarPubMed
Wightman, R. & Turner, S.R. (2008). The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 54(5), 794–805.CrossRefGoogle ScholarPubMed
Yu, H., Liu, R., Shen, D., Wu, Z. & Huang, Y. (2008). Arrangement of cellulose microfibrils in the wheat straw cell wall. Carbohyd Polym 72(1), 122–127.Google Scholar
Zhang, Z.H., Ma, J.F., Ji, Z. & Xu, F. ( 2012). Comparison of anatomy and composition distribution between normal and compression wood of Pinus Bungeana Zucc. revealed by microscopic imaging techniques. Microsc Microanal 18(6), 1459–1466.Google Scholar

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