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Detection in situ and characterization of lignin in the G-layer of tension wood fibres of Populus deltoides

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Abstract

The occurrence of lignin in the additional gelatinous (G-) layer that differentiates in the secondary wall of hardwoods during tension wood formation has long been debated. In the present work, the ultrastructural distribution of lignin in the cell walls of normal and tension wood fibres from poplar (Populus deltoides Bartr. ex Marshall) was investigated by transmission electron microscopy using cryo-fixation–freeze-substitution in association with immunogold probes directed against typical structural motifs of lignin. The specificity of the immunological probes for condensed and non-condensed guaiacyl and syringyl interunit linkages of lignin, and their high sensitivity, allowed detection of lignin epitopes of definite chemical structures in the G-layer of tension wood fibres. Semi-quantitative distribution of the corresponding epitopes revealed the abundance of syringyl units in the G-layer. Predominating non-condensed lignin sub-structures appeared to be embedded in the crystalline cellulose matrix prevailing in the G-layer. The endwise mode of polymerization that is known to lead to these types of lignin structures appears consistent with such an organized cellulose environment. Immunochemical labelling provides the first visualization in planta of lignin structures within the G-layer of tension wood. The patterns of distribution of syringyl epitopes indicate that syringyl lignin is deposited more intensely in the later phase of fibre secondary wall assembly. The data also illustrate that syringyl lignin synthesis in tension wood fibres is under specific spatial and temporal regulation targeted differentially throughout cell wall layers.

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Fig. 1a, b
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Abbreviations

G-layer :

Gelatinous layer

G :

Guaiacyl monomeric unit

PATAg :

Periodic acid–thiocarbohydrazide–silver proteinate

S :

Syringyl monomeric unit

References

  • Aoyama W, Matsumura A, Tsutsumi Y, Nishita (2001) Lignification and peroxidase in tension wood of Eucalyptus viminalis seedlings. J Wood Sci 47:419–424

    CAS  Google Scholar 

  • Araki N, Fujita M, Saiki H, Harada H (1982) Transition of the fiber wall from normal wood to tension wood in Robinia pseudoacacia L. and Populus euroamericana Gunii. Mokuzai Gakkaishi 28:267–273

    Google Scholar 

  • Baillères H, Castan M, Monties B, Pollet B, Lapierre C (1997) Lignin structure in Buxus sempervirens reaction wood. Phytochemistry 44:35–39

    Article  Google Scholar 

  • Besombes S, Robert D, Utille J-P, Taravel F-R, Mazeau K (2003) Molecular modelling of syringyl and p-hydroxyphenyl β-O-4 dimers. Comparative study of the computed experimental conformational properties of lignin β-O-4 model compounds. J Agric Food Chem 51:34–42

    Article  CAS  PubMed  Google Scholar 

  • Blanchette RA, Obst JR, Timell TE (1994) Biodegradation of compression wood and tension wood by white and brown rot fungi. Holzforschung 48:34–42

    CAS  Google Scholar 

  • Dixon RA, Chen F, Guo D, Parvathi K (2001) The biosynthesis of monolignols: a “metabolic grid”, or independent pathways to guaiacyl and syringyl units? Phytochemistry 57:1069–1084

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Furuya N, Tatahashi S, Miyasaki M (1970) The chemical composition of the gelatinous layer from the tension wood of Populus euro-americana. Mokuzai Gakkaishi 16:26–30

    CAS  Google Scholar 

  • Gindl W (2002) Comparing mechanical properties of normal and compression wood in Norway spruce: the role of lignin in compression parallel to grain. Holzforschung 56:395–401

    CAS  Google Scholar 

  • Grünwald C, Ruel K, Kim YS, Schmitt U (2002) On the cytochemistry of cell wall formation in poplar trees. Plant Biol 4:13–21

    Google Scholar 

  • Hawkins S, Boudet A (2003) ‘Defence lignin’ and hydroxycinnamyl alcohol dehydrogenase activities in wounded Eucalyptus gunnii. For Pathol 33:339–352

    Google Scholar 

  • Houtman CJ, Atalla RH (1995) Cellulose–lignin interactions. A computational study. Plant Physiol 107:977–984

    CAS  PubMed  Google Scholar 

  • Hu W-J, Harding SA, Lung J, Popko JL, Stokke DD, Tsai CJ, Chiang VL (1999). Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nature Biotechnol 17:808–812

    Article  CAS  Google Scholar 

  • Imai T, Ruel K, Pilate G, Leple J-C, Joseleau J-P (2002) Influence of environment or genetic factors on the formation of tension wood. Abstract Journées Réseau Français des Parois, Reims May 2002, p 13

  • Joseleau J-P, Ruel K (1997) Study of lignification by non invasive techniques in growing maize internodes—an investigation by Fourier transform infrared, cross-polarisation-magic angle spinning 13C-nuclear magnetic resonance spectroscopy. Plant Physiol 114:1123–1133

    Article  CAS  PubMed  Google Scholar 

  • Joseleau J-P, Petit-Conil M, Jouanin L, DeChoudens C, Chantre G, Sollier JN, Ruel K (1999) Immunological characterization of residual lignins in pulps from poplar clones and from a genetically modified variety. 10th international symposium on wood pulping chemistry, Yokohama, Japan, vol II, pp 190–193

  • Kuo CM, Timell TE (1969) Isolation and characterization of a galactan from tension wood of American beech (Fagus grandifolia Ehrl.) Svensk Papperstidn 72:703–708

    Google Scholar 

  • Lange BM, Lapierre C, Sandermann (1995) Elicitor-induced spruce stress lignin. Structural similarity to developmental lignins. Plant Physiol 108:1277–1287

    CAS  PubMed  Google Scholar 

  • Lapierre C (1993) Application of new methods for the investigation of lignin structure. In: Jung HG, Buxton DR, Hatfield RD, Ralph J (eds) Forage cell wall structure and digestibility. American Society of Agronomy Inc, Madison, pp 133–166

  • Maier-Maercker U, Koch W (1986) Delignification of subsidiary and guard cell walls by SO2 and probable implication on the humidity response of Picea abies (L) Karst. Eur J For Pathol 16:342–351

    CAS  Google Scholar 

  • Nevell TP (1963) Degradation of cellulose—28. Oxidation. In: Wistler RL (ed) Methods in carbohydrate chemistry, vol III. Academic Press, NY, pp 164–284

  • Nicholson RL, Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30:113–157

    Google Scholar 

  • Norberg PH, Meier H (1966) Physical and chemical properties of the gelatinous layer in tension wood fibers of aspen (Populus tremula L.). Holzforschung 20:174–178

    CAS  Google Scholar 

  • Parham RA, Côté WA (1971) Distribution of lignin in normal and compression wood of Pinus taeda. Wood Sci Technol 5:49–54

    CAS  Google Scholar 

  • Robards AW (1966) The application of the modified sine rule to tension wood production in the stem of crack willow (Salix fragilis L). Ann Bot 30:513–523

    Google Scholar 

  • Roussel MR, Lim C (1995) Dynamic model of lignin growing in restricted spaces. Macromolecules 28:370–376

    CAS  Google Scholar 

  • Ruel K, Barnoud F (1978) Détermination quantitative du bois de tension par une méthode analytique chimique: validité du critère galactose. Holzforschung 32:149–156

    CAS  Google Scholar 

  • Ruel K, Barnoud F, Goring DAI (1979) Ultrastructural lamellation in the S2 layer of two hardwoods and a reed. Cell Chem Technol 13:429–432

    CAS  Google Scholar 

  • Ruel K, Faix O, Joseleau J-P (1994) New immunogold probes for studying the distribution of the different lignin types during plant cell wall biogenesis. J Trace Microprobe Tech 12:2247–265

    Google Scholar 

  • Ruel K, Burlat V, Joseleau J-P (1999) Relationship between ultrastructural topochemistry of lignin and wood properties. IAWA J 20:203–211

    Google Scholar 

  • Ruel K, Chabannes M, Boudet A-M, Legrand M, Joseleau J-P (2001) Reassessment of quantitative changes in lignification of transgenic tobacco plants and their impact on cell wall assembly. Phytochemistry 57:875–882

    Article  CAS  PubMed  Google Scholar 

  • Ruel K, Faix O, Kuroda K-I Joseleau J-P (2004) A polyclonal antibody directed against syringyl propane epitopes of native lignins. C R Acad Sci (in press)

  • Sandermann HE, Heller W, Langebartels C (1998) Ozone: an abiotic elicitor of plant defence reactions. Trends Plant Sci 3:47–50

    Article  Google Scholar 

  • Scurfield G (1971) Histochemistry of reaction wood cell walls in two species of Eucalyptus and in Tristinia conferta R. BR. Aust J Bot 20:9–26

    Google Scholar 

  • Scurfield G, Wardrop AB (1963) The nature of reaction wood. VII. Lignification in reaction wood. Aust J Bot 11 107–116

    Google Scholar 

  • Southerton SG, Deverall BJ (1990) Histochemical and chemical for lignin accumulation during the expression of resistance to leaf rust fungi in wheat. Physiol Mol Plant Pathol 36:483–494

    CAS  Google Scholar 

  • Thiery JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1017

    CAS  Google Scholar 

  • Timell TE (1969) The chemical composition of tension wood. Svensk Papperstidn 72:173–178

    CAS  Google Scholar 

  • Vance CP, Kirk TK, Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 18:259–288

    CAS  Google Scholar 

  • Wada M, Okano T, Sugiyama J, Horii F (1995) Characterization of tension and normally lignified wood cellulose in Populus maximowiczii. Cellulose 2:223–233

    CAS  Google Scholar 

  • Wardrop AB, Dadswell HE (1955) Nature of reaction wood. IV. Variations in cell wall organization of tension-wood fibres. Aust J Bot 3:177–189

    Google Scholar 

  • Yamamoto H (1998) Generation process of growth stresses in cell walls: role of lignin deposition and cellulose micro-fibril during cell wall maturation. Wood Sci Technol 32:171–182

    CAS  Google Scholar 

  • Yamamoto H, Okuyama T, Yoshida M (1993) Generation of a process of growth stresses in cell walls. V. Model of tensile stress generation in gelatinous fibers. Mokuzai Gakkaishi 39:118–125

    Google Scholar 

  • Yamauchi K, Yasuda S, Hamada K, Tsutsumi Y, Fukushima K (2003) Multiform biosynthetic pathway of syringyl lignin in angiosperms. Planta 216:496–501

    CAS  PubMed  Google Scholar 

  • Yoshida M, Ohta H, Okuyama T (2002) Tensile growth stress and lignin distribution in the cell walls of black locust (Robinia pseudoacacia). J Wood Sci 48:99–105

    CAS  Google Scholar 

  • Yoshida S, Tanahashi M, Shigematsu M, Shinoda Y (1994) Effect of reaction medium on dehydrogenative polymerisation of sinapyl alcohol. Mokuzai Gakkaishi 40:974–979

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Guillaume Chantre (AFOCELL, Nungis, France) for the gift of the sample of poplar, clone Raspalje. Some of the results were acquired in the framework of European program AIR 3 CT 94-2065.

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Author notes

  1. Takanori Imai

    Present address: School of Bioagricultural Sciences, Nagoya University, 464-8601, Nagoya, Japan

  2. Katsushi Kuroda

    Present address: National Institute of Agrobiological Sciences, Tsukuba, 305-8602, Ibaraki, Japan

Authors and Affiliations

  1. Centre de Recherche sur les Macromolécules Végétales, CERMAV-CNRS, BP 53, 38041, Grenoble Cedex 9, France

    Jean-Paul Joseleau, Takanori Imai, Katsushi Kuroda & Katia Ruel

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  1. Jean-Paul Joseleau
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  2. Takanori Imai
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Correspondence to Katia Ruel.

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Joseleau, JP., Imai, T., Kuroda, K. et al. Detection in situ and characterization of lignin in the G-layer of tension wood fibres of Populus deltoides . Planta 219, 338–345 (2004). https://doi.org/10.1007/s00425-004-1226-5

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