Plant Biol (Stuttg) 2002; 4(1): 2-8
DOI: 10.1055/s-2002-20429
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Interrelation between Lignin Deposition and Polysaccharide Matrices during the Assembly of Plant Cell Walls

K. Ruel 1 , M.-D. Montiel 1 , T. Goujon 2 , L. Jouanin 2 , V. Burlat 3 , J.-P. Joseleau 1
  • 1 Centre de Recherches sur les Macromolécules Végétales, (CERMAV-CNRS, UPR 5301), Université Joseph Fourier, BP 53, 38041 Grenoble Cedex 9, France
  • 2 INRA, Laboratoire de Biologie Cellulaire, route de Saint-Cyr, 78026 Versailles Cedex, France
  • 3 Laboratoire de Physiologie Végétale, Faculté des Sciences et Techniques, 37200 Tours, France
Further Information

Publication History

June 10, 2001

October 25, 2001

Publication Date:
28 February 2002 (online)

Abstract

The modifications caused by genetic down-regulation of the enzyme cinnamoyl CoA reductase (CCR) from monolignol biosynthetic pathways on tobacco and Arabidopsis thaliana were investigated at the ultrastructural level. A typical result was that the same transformation led to similar abnormality in secondary wall formation of fibres in both plants. The cell wall alterations mainly consisted in an important disorganization and loosening of cellulose microfibrils in the inner part of the S2 layer. This inability of the transformants to form a coherent cell wall coincided with a lack of synthesis of non-condensed forms of lignin in this disorganized region of the wall, as demonstrated by immunolabelling of lignin subunits. A similar disorganization was observed during fibre wall formation in the differentiating tissues of young Populus and A. thaliana plants. The transitory lack of organization of cellulose microfibrils, also coincided with a depletion in non-condensed forms of lignins. These results suggest that such lignin substructures may be involved in the cohesion of secondary walls during cell wall biogenesis. The mutual influence of the cellulose-hemicellulose environment and monolignol local polymerization is discussed.

Abbreviations

CCR: Cinnamoyl CoA Reductase

TEM: Transmission Electron Microscopy

S1, S2: Secondary wall sublayers S1 and S2

G; S: Guaiacyl and Syringyl units of lignin

References

  • 01 Agarwal,  U. P., and Atalla,  R. H.. (1986);  In situ Raman microprobe studies of plant cell walls: macromolecular organisation and composition variability in the secondary wall of Picea mariana. .  Planta. 169 325-332
  • 02 Boudet,  A.-M., and Grima-Pettenati,  J.. (1996);  Lignin genetic engineering.  Mol. Breeding. 2 25-39
  • 03 Chabannes,  M.,, Ruel,  K.,, Yoshinaga,  A.,, Chabbert,  B.,, Jauneau,  A.,, Joseleau,  J.-P.,, and Boudet,  A.-M.. (2001);  In situ analysis of lignins in transgenic tobacco reveals a differential impact of individual transformations on the spatial patterns of lignin deposition at the cellular and sub-cellular levels.  Plant J.. in press
  • 04 Goujon,  T.,, Sibout,  R.,, Ferret,  V.,, Maba,  B.,, Nussaume,  N.,, Bechtold,  N.,, Pollet,  B.,, Milla,  I.,, Lapierre,  C.,, and Jouanin,  L.. (2000) Characterization of lignification mutants in Arabidopsis thaliana. . Plant Sciences for the third millenium. Badot, Capelli, and Dat, eds. Besancon; 4th general meeting of the SFPV.5 -7/12/2000,
  • 05 Guan,  S.-Y.,, Mlynar,  J.,, and Sarkanen,  S.. (1997);  Dehydrogenation polymerisation of coniferylalcohol on macromolecular lignin templates.  Phytochemistry. 45 911-918
  • 06 Higuchi,  T.. (1990);  Lignin biochemistry: biosynthesis and biodegradation. Wood Sci.  Technol.. 24 23-63
  • 07 Houtman,  C. J.. (1999);  What factors control dimerization of coniferyl alcohol?.  Holzforschung. 53 585-589
  • 08 Houtman,  C. J., and Atalla,  R. H.. (1995);  Cellulose-lignin interactions. A computational study.  Plant Physiol.. 107 977-984
  • 09 Joseleau,  J.-P., and Ruel,  K.. (1997);  Study of lignification by noninvasive techniques in growing maize internodes - An investigation by Fourier tranform infrared, cross-polarisation-magic angle spinning 13C-nuclear magnetic resonance spectroscopy and immunocytochemical transmission electron microscopy.  Plant Physiol.. 114 1123-1133
  • 10 Jurasek,  L.. (1996);  Morphology of computer-modeled lignin structures: fractal dimensions, orientation and porosity.  J. Pulp Paper Sci.. 22 376-380
  • 11 Jurasek,  L.. (1998) Experimenting virtual lignins.  ACS Symposium series, Vol. 697, . Lewis, N. G. and Sarkanen, S., eds. Lignin and lignin biosynthesis pp. 276-293
  • 12 Lewis,  N. G.,, Davin,  L. B.,, and Sarkanen,  S.. (1999) The nature and function of lignins. Comprehensive natural products chemistry, Vol. 3. Pinto, B. M., ed.
  • 13 Piquemal,  J.,, Lapierre,  C.,, Myton,  K.,, O'Connell,  A.,, Schuch,  W.,, Grima-Pettenati,  J.,, and Boudet,  A.-M.. (1998);  Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in tobacco plants.  Plant J.. 13 71-83
  • 14 Roussel,  M. R., and Lim,  C.. (1995);  Dynamic model of lignin growing in restricted spaces.  Macromolecules. 28 370-376
  • 15 Ruel,  K.,, Barnoud,  F.,, and Goring,  D. A. I.. (1979);  Ultrastructural lamellation in the S2 layer of two hardwoods and a reed.  Cell. Chem. Technol.. 13 429-432
  • 16 Ruel,  K.,, Chabannes,  M.,, Boudet,  A.-M.,, Legrand,  M.,, and Joseleau,  J. P.. (2001);  Reassessment of qualitative changes in lignification of transgenic tobacco plants and their impact on cell wall assembly.  Phytochemistry. 57 875-882
  • 17 Ruel,  K.,, Chabannes,  M.,, Pinçon,  G.,, Piquemal,  J.,, Boudet,  A.-M.,, Legrand,  M.,, and Joseleau,  J. P.. (2000) Modifications in lignin biosynthesis pathways affect plant cell wall assembly, 219th ACS Symposium. San-Francisco, CA; Cellulose, Paper, and Textile Chemistry division. Symposium: Biosynthesis of plant biopolymers and related substances, Part 1 of 2, Abstract N° 134
  • 18 Russel,  A. R.,, Forester,  A. R.,, Chesson,  A.,, and Burkitt,  M. J.. (1996);  Oxidative coupling during lignin polymerisation is determined by unpaired electron delocalisation within parent phenyl propanoid radicals.  Arch. Biochem. Biophys.. 332 357-366
  • 19 Siegel,  S.. (1957);  Non-enzymatic macromolecules as matrices in biological synthesis: the role of polysaccharides in peroxidase-catalysed lignin polymer from eugenol.  J. Am. Chem. Soc.. 79 1628-1632
  • 20 Simon,  P. J., and Eriksson,  K. E. L.. (1995);  A molecular mechanics investigation of lignin structure. I. Conformational analysis of 1-phenoxy-1,3-propanediol using NM3.  Holzforschung. 49 429-438
  • 21 Tanahashi,  M., and Higuchi,  T.. (1990);  Effect of hydrophobic regions of hemicelluloses in dehydrogenative polymerisation of sinapyl alcohol.  Mokuzai Gakkaishi. 36 424-428
  • 22 Terashima,  N., and Fukushima,  K.. (1989) Biogenesis and structure of macromolecular lignin in the cell wall of tree xylem as studied by microautoradiography. Plant cell wall polymers, biogenesis and biodegradation. Lewis, N. G. and Paice, M. G., eds. Washington DC; Am. Chem. Soc. Symposium Series, 339 pp. 160-168
  • 23 Terashima,  N.,, Atalla,  R. H.,, Ralph,  S. A.,, Landucci,  L. L.,, Lapierre,  C.,, and Monties,  B.. (1995);  Preparations of lignin polymer models under conditions that approximate cell wall lignification.  Holzforschung. 49 521-527
  • 24 Xie,  Y.,, Yasuda,  S.,, and Terashima,  N.. (1994);  Selective Carbon 13 - enrichment of side - chain carbons of oleander lignin traced by Carbon 13 nuclear magnetic resonance.  Mokuzai Gakkaishi. 40 191-199
  • 25 Yoshida,  S.,, Tanahashi,  M.,, Shigematsu,  M.,, and Shinoda,  Y.. (1994);  Effect of reaction medium on dehydrogenative polymerization of sinapyl alcohol.  Mokuzai Gakkaishi. 40 974-979

J.-P. Joseleau

CERMAV-CNRS

BP 53
38041 Grenoble Cedex 9
France

Email: joseleau@cermav.cnrs.fr

Section Editor: A. M. C. Emons

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