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Plant Cell Advance Online Publication
Published on November 16, 2007; 10.1105/tpc.107.054148

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Received July 11, 2007
Returned for revision October 12, 2007
Accepted October 19, 2007

Downregulation of Cinnamoyl-Coenzyme A Reductase in Poplar: Multiple-Level Phenotyping Reveals Effects on Cell Wall Polymer Metabolism and Structure

Jean-Charles Leplé 1, Rebecca Dauwe 2, Kris Morreel 2, Véronique Storme 2, Catherine Lapierre 3, Brigitte Pollet 3, Annette Naumann 4, Kyu-Young Kang 5, Hoon Kim 6, Katia Ruel 7, Andrée Lefèbvre 7, Jean-Paul Joseleau 7, Jacqueline Grima-Pettenati 8, Riet De Rycke 2, Sara Andersson-Gunnerås 9, Alexander Erban 10, Ines Fehrle 10, Michel Petit-Conil 11, Joachim Kopka 10, Andrea Polle 4, Eric Messens 2, Björn Sundberg 9, Shawn D. Mansfield 5, John Ralph 12, Gilles Pilate 13, and Wout Boerjan 2*

1 Department of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Gent, Belgium; Department of Molecular Genetics, Ghent University, 9052 Gent, Belgium; Unité Amélioration Génétique et Physiologie Forestières, Institut National de la Recherche Agronomique, 45166 Olivet cedex, France
2 Department of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Gent, Belgium; Department of Molecular Genetics, Ghent University, 9052 Gent, Belgium
3 Unité de Chimie Biologique, Unité Mixte de Recherche 206 AgroParisTech/Institut National de la Recherche Agronomique, AgroParisTech Centre de Grignon, 78850 Thiverval-Grignon, France
4 Institut fur Forstbotanik, Universität Göttingen, 37077 Göttingen, Germany
5 Department of Wood Science, University of British Columbia, Vancouver, BC, Canada V6T 1Z4
6 U.S. Dairy Forage Research Center, Agricultural Research Service, Department of Horticulture, University of Wisconsin, Madison, Wisconsin 53706
7 Centre de Recherche sur les Macromolécules Végétales, Unité Propre de Recherche 5301, Centre National de la Recherche Scientifique, 38041 Grenoble Cedex 09, France
8 Pôle de Biotechnologies Végétales, Unité Mixte de Recherche/Unité Propre de Service 5546, Centre National de la Recherche Scientifique, 31326 Castanet Tolosan, France
9 Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden
10 Max-Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany
11 Centre Technique du Papier, 38044 Grenoble Cedex 9, France; Department of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Gent, Belgium
12 U.S. Dairy Forage Research Center, Agricultural Research Service, U.S. Department of Agriculture and Department of Biological Systems Engineering, University of Wisconsin, Madison, Wisconsin 53706
13 Unité Amélioration Génétique et Physiologie Forestières, Institut National de la Recherche Agronomique, 45166 Olivet cedex, France

* To whom correspondence should be addressed. E-mail: wout.boerjan{at}psb.ugent.be.

Cinnamoyl-CoA reductase (CCR) catalyzes the penultimate step in monolignol biosynthesis. We show that downregulation of CCR in transgenic poplar (Populus tremula x Populus alba) was associated with up to 50% reduced lignin content and an orange-brown, often patchy, coloration of the outer xylem. Thioacidolysis, nuclear magnetic resonance (NMR), immunocytochemistry of lignin epitopes, and oligolignol profiling indicated that lignin was relatively more reduced in syringyl than in guaiacyl units. The cohesion of the walls was affected, particularly at sites that are generally richer in syringyl units in wild-type poplar. Ferulic acid was incorporated into the lignin via ether bonds, as evidenced independently by thioacidolysis and by NMR. A synthetic lignin incorporating ferulic acid had a red-brown coloration, suggesting that the xylem coloration was due to the presence of ferulic acid during lignification. Elevated ferulic acid levels were also observed in the form of esters. Transcript and metabolite profiling were used as comprehensive phenotyping tools to investigate how CCR downregulation impacted metabolism and the biosynthesis of other cell wall polymers. Both methods suggested reduced biosynthesis and increased breakdown or remodeling of noncellulosic cell wall polymers, which was further supported by Fourier transform infrared spectroscopy and wet chemistry analysis. The reduced levels of lignin and hemicellulose were associated with an increased proportion of cellulose. Furthermore, the transcript and metabolite profiling data pointed toward a stress response induced by the altered cell wall structure. Finally, chemical pulping of wood derived from 5-year-old, field-grown transgenic lines revealed improved pulping characteristics, but growth was affected in all transgenic lines tested.






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