On the Cytochemistry of Cell Wall Formation in Poplar Trees

Abstract

The ultrastructure of cell walls and the mechanisms of cell wall formation are still not fully understood. The objective of our study was therefore to obtain additional fine structural details on the deposition of cell wall components during the differentiation of xylem cells in hybrid aspen (Populus tremula L. × P. tremuloides Michx.) we used as a model tree. At the electron microscope level, PATAg staining revealed a successive deposition of polysaccharides with increasing distance from the cambium. Staining with potassium permanganate and UV microspectrophotometry showed that the cell walls were lignified, with some delay to the deposition of polysaccharides. Immunogold labelling of three lignin types in developing cell walls varied with progressive deposition of cell wall layers. Condensed lignin subunits were localized in corners of cells adjacent to the cambium prior to S1 formation, whereas non-condensed lignin subunits became labelled only in later stages - in secondary walls near cell corners and simultaneously with the completion of S1 formation. As S2 polysaccharide deposition progressed, the labelling extended towards the lumen. Labelling of peroxidases revealed their presence in cell corner regions of young xylem cells, still lacking a secondary wall, implying that peroxidases are incorporated into the developing cell wall at early developmental stages. A weak labelling of middle lamella regions and secondary walls could also be seen at later stages. The results are discussed in relation to current knowledge on the succession of polysaccharide and lignin deposition in woody cell walls.

Populus - wood formation - lignification - electron microscopy - immunogold labelling - UV microspectrophotometry

References

• 01 Abe,  H.,, Funada,  R.,, Ohtani,  Y.,, and Fukazawa,  K.. (1995);  Changes in the arrangement of microtubules and microfibrils in differentiating conifer tracheids during the expansion of cells.  Ann. Bot.. 75 305-310
• 02 Awano,  T.,, Takabe,  K.,, and Fujita,  M.. (1998);  Localization of glucuronoxylans in Japanese beech visulaized by immunogold labelling.  Protoplasma. 202 213-222
• 03 Awano,  T.,, Takabe,  K.,, Fujita,  M.,, and Daniel,  G.. (2000);  Deposition of glucuronoxylans on the secondary cell wall of Japanese beech as observed by immuno-scanning electron microscopy.  Protoplasma. 212 72-79
• 04 Baba,  K.,, Asada,  T.,, and Hayashi,  T.. (2000);  Relation between developmental changes on anatomical structure and on protein pattern in differentiating xylem of tension wood.  J. Wood Sci.. 46 1-7
• 05 Boudet,  A.-M.,, Goffner,  D.,, Marque,  C.,, and Grima Pettenati,  J.. (1998) Genes involved in the final steps of monolignol biosynthesis and their manipulation for tailoring new lignins. Lignin and lignan biosynthesis. Lewis, N. G. and Sarkanen, S., eds. Washington DC; ACS Symposium Series 697, American Chemical Society pp. 65-75
• 06 Chaffey,  N.. (1999);  Cambium: old challenges - new opportunities.  Trees. 13 138-151
• 07 Chaffey,  N.. (2000) Cytoskeleton, cell walls and cambium: New insights into secondary xylem differentiation. Cell and Molecular Biology of Wood Formation. Savidge, R. A., Barnett, J. R., and Napier, R., eds. Oxford; BIOS Scientific Publ. pp. 31-42
• 08 Dean,  J. F. D.,, LaFayette,  P. R.,, Rugh,  C.,, Tristram,  A. H.,, Hoopes,  T.,, Eriksson,  K.-E.,, and Merkle,  S. A.. (1998) Laccases associated with lignifying vascular tissues. Lignin and lignan biosynthesis. Lewis, N. G. and Sarkanen, S., eds. Washington DC; ACS Symposium Series 697, American Chemical Society pp. 96-108
• 09 Dharmawardhana,  D P., and Ellis,  B. E.. (1998) β-Glucosidases and glucosyltransferases in lignifying tissues. Lignin and lignan biosynthesis. Lewis, N. G. and Sarkanen, S., eds. Washington DC; ACS Symposium Series 697, American Chemical Society pp. 76-83
• 10 Delmer,  D. P., and Amor,  Y.. (1995);  Cellulose biosynthesis.  The Plant Cell. 7 987-1000
• 11 Donaldson,  L. A.. (1992);  Lignin distribution during latewood formation in Pinus radiata Don.  IAWA Bull.. 13 381-387
• 12 Emons,  A. M. C., and Mulder,  B. M.. (2000);  How the deposition of cellulose microfibrils builds cell wall architecture.  Trends in Plant Science. 5 35-40
• 13 Fukuda,  H.. (1997);  Tracheary element differentiation.  The Plant Cell. 9 1147-1156
• 14 Funada,  R.,, Abe,  H.,, Furusawa,  O.,, Imaizumi,  H.,, Fukazawa,  K.,, and Ohtani,  J.. (1997);  The orientation and localization of cortical microtubules in differentiating tracheids during cell expansion.  Plant Cell Physiol.. 38 210-212
• 15 Harkin,  J. M., and Obst,  J. R.. (1973);  Lignification in trees: indication of exclusive peroxidase participation.  Science. 180 296-297
• 16 Herth,  W.. (1985);  Plasma membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum. .  Planta. 164 12-21
• 17 Higuchi,  T.. (1997) Biochemistry and molecular biology of wood. Berlin-Heidelberg-New York; Springer Verlag p. 362
• 18 Joseleau,  J.-P., and Ruel,  K.. (1997);  Study of lignification by noninvasive techniques in growing maize internodes. An investigation by FTIR, CP/MAS ¹³C NMR and immunocytochemical transmission electron microscopy.  Plant Physiol.. 114 1123-1133
• 19 Kim,  Y. S.,, Wi,  S.-G.,, Grünwald,  C.,, and Schmitt,  U.. (2002);  Immuno electron microscopic localization of peroxidases in the differentiating xylem of Populus spp.  Holzforschung. in press
• 20 Lewis,  N. G.,, Davin,  L. B.,, and Sarkanen,  S.. (1998) Lignin and lignan biosynthesis: distinctions and reconciliations. Lignin and lignan biosynthesis. Lewis, N. G. and Sarkanen, S., eds. Washington DC; ACS Symposium Series 697, American Chemical Society pp. 1-28
• 21 Maeda,  Y.,, Awano,  T.,, Takabe,  K.,, and Fujita,  M.. (2000);  Immunolocalization of glucomannans in the cell wall of differentiating tracheids in Chamaecyparis obtusa. .  Protoplasma. 213 148-156
• 22 Musha,  Y., and Goring,  D. A. I.. (1975);  Distribution of syringyl and guaiacyl moieties in hardwoods as indicated by ultraviolet microscopy.  Wood Sci. Technol.. 9 45-58
• 23 Ros Barcelo,  A.,, Morales,  M.,, and Pedreno,  M. A.. (1998) Specific compartmentalization of peroxidase isoenzymes in relation to lignin biosynthesis in the plant cell. Lignin and lignan biosynthesis. Lewis, N. G. and Sarkanen, S., eds. Washington DC; ACS Symposium Series 697, American Chemical Society pp. 84-95
• 24 Ruel,  K.,, Comtat,  J.,, and Barnoud,  F.. (1977);  Localisation histologique et ultrastructurale des xylanes dans les parois primaires des tissus d'Arundo donax. .  C. R. Acad. Sci.. 284 1421-1424
• 25 Ruel,  K.,, Barnoud,  F.,, and Eriksson,  K. E.. (1984);  Ultrastructural aspects of wood degradation by Sporotrichum pulverulentum - Observations on spruce wood impregnated with glucose.  Holzforschung. 38 61-68
• 26 Ruel,  K.,, Faix,  O.,, and Joseleau,  J.-P.. (1994);  New immunogold probes for studying the distribution of the different lignin types during plant cell wall biogenesis.  J. Trace Microprobe T.. 12 247-265
• 27 Ruel,  K.,, Burlat,  V.,, and Joseleau,  J.-P.. (1999);  Relationship between ultrastructural topochemistry of lignin and wood properties.  IAWA J.. 20 203-211
• 28 Saleh,  T. M.,, Leney,  L.,, and Sarkanen,  K. V.. (1967);  Radioautographic studies of cottonwood, douglas fir and wheat plants.  Holzforschung. 21 116-120
• 29 Savidge,  R. A.. (1996);  Xylogenesis, genetic and environmental regulation (review).  IAWA J.. 17 269-310
• 30 Savidge,  R. A.. (2000) Biochemistry of seasonal cambial growth and wood formation - an overview of the challenges. Cell and Molecular Biology of Wood Formation. Savidge, R. A., Barnett, J. R., and Napier, R., eds. Oxford; BIOS Scientific Publ. pp. 1-30
• 31 Savidge,  R. A.,, Udagama-Randeniya,  P. V.,, Xu,  Y.,, Leinhos,  V.,, and Förster,  H.. (1998) Coniferyl alcohol oxidase: a new enzyme spatio-temporally associated with lignifying tissues. Lignin and lignan biosynthesis. Lewis, N. G. and Sarkanen, S., eds. Washington DC; ACS Symposium Series 697, American Chemical Society pp. 109-130
• 32 Spurr,  A. R.. (1969);  A low viscosity embedding medium for electron microscopy.  J. Ultrastructural Res.. 26 31-43
• 33 Takabe,  K.,, Harada,  H.,, and Fukazawa,  K.. (1989) Deposition of cell wall components in conifer tracheids. Plant cell wall polymers. Lewis, N. G. and Paice, M. G., eds. Washington DC; ACS Symposium Series 399, American Chemical Society pp. 47-66
• 34 Terashima,  N.. (2000) Formation and ultrastructure of lignified plant cell walls. New horizons in wood anatomy. Kim, Y.S., ed. Kwangju; Chonnam National University Press pp. 169-180
• 35 Terashima,  N., and Fukushima,  K.. (1988);  Heterogeneity in formation of lignin - XI: An autoradiographic study of the heterogeneous formation and structure of pine lignin.  Wood Sci. Technol.. 22 259-270
• 36 Terashima,  N.,, Nakashima,  J.,, and Takabe,  K.. (1998) Proposed structure for protolignin in plant cell walls. Lignin and lignan biosynthesis. Lewis, N. G. and Sarkanen, S., eds. Washington DC; ACS Symposium Series 697, American Chemical Society pp. 180-193
• 37 Thiéry,  J. P.. (1967);  Mise en évidence des polysaccharides sur coupes fines en microscopie électronique.  J. Microsc.. 6 987-1017
• 38 Vander Mijnsbrugge,  K. V.,, Meyermans,  H.,, Van Montagu,  M.,, Bauw,  G.,, and Boerjan,  W.. (2000);  Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins.  Planta. 210 589-598
• 39 Wardrop,  A. B.. (1965) Cellular differentiation in xylem. Cellular ultrastructure of woody plants. Côté, W. A., ed. Syracuse, New York; Syracuse University Press pp. 61-97
• 40 Wodzicki,  T. J.. (2001);  Natural factors affecting wood structure.  Wood Sci. Technol.. 35 5-26
• 41 Yoshinaga,  A.,, Fujita,  M.,, and Saiki,  H.. (1997);  Secondary wall thickening and lignification of oak xylem components during latewood formation.  Mokuzai Gakkaishi. 43 377-383

Section Editor: A. M. C. Emons