Downregulation of cinnamoyl-coenzyme a reductase in poplar: Multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure

Jean Charles Leplé, Rebecca Dauwe, Kris Morreel, Véronique Storme, Catherine Lapierre, Brigitte Pollet, Annette Naumann, Kyu Young Kang, Hoon Kim, Katia Ruel, Andrée Lefèbvre, Jean Paul Joseleau, Jacqueline Grima-Pettenati, Riet De Rycke, Sara Andersson-Gunnerås, Alexander Erban, Ines Fehrle, Michel Petit-Conil, Joachim Kopka, Andrea PolleEric Messens, Björn Sundberg, Shawn D. Mansfield, John Ralph, Gilles Pilate, Wout Boerjan

Research output: Contribution to journalArticlepeer-review

347 Scopus citations

Abstract

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.

Original languageEnglish
Pages (from-to)3669-3691
Number of pages23
JournalPlant Cell
Volume19
Issue number11
DOIs
StatePublished - Nov 2007

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