Article

Role of bifunctional ammonia-lyase in grass cell wall biosynthesis

  • Nature Plants 2, Article number: 16050 (2016)
  • doi:10.1038/nplants.2016.50
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Abstract

L-Phenylalanine ammonia-lyase (PAL) is the first enzyme in the biosynthesis of phenylpropanoid-derived plant compounds such as flavonoids, coumarins and the cell wall polymer lignin. The cell walls of grasses possess higher proportions of syringyl (S)-rich lignins and high levels of esterified coumaric acid compared with those of dicotyledonous plants, and PAL from grasses can also possess tyrosine ammonia-lyase (TAL) activity, the reason for which has remained unclear. Using phylogenetic, transcriptomic and in vitro biochemical analyses, we identified a single homotetrameric bifunctional ammonia-lyase (PTAL) among eight BdPAL enzymes in the model grass species Brachypodium distachyon. 13C isotope labelling experiments along with BdPTAL1-downregulation in transgenic plants showed that the TAL activity of BdPTAL1 can provide nearly half of the total lignin deposited in Brachypodium, with a preference for S-lignin and wall-bound coumarate biosynthesis, indicating that PTAL function is linked to the characteristic features of grass cell walls. Furthermore, isotope dilution experiments suggest that the pathways to lignin from L-phenylalanine and L-tyrosine are distinct beyond the formation of 4-coumarate, supporting the organization of lignin synthesis enzymes in one or more metabolons.

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Acknowledgements

We thank D. Huhman and the Noble Foundation Analytical Chemistry Facility for the analysis of soluble phenolic compounds, Dr X. Wang for assistance with protein purification, and Dr L. Gallego-Giraldo for critical reading of the manuscript. This work was supported by a Barrie Foundation Fellowship (to J.B.), The University of North Texas and the BioEnergy Science Center (Oak Ridge National Laboratory), a US Department of Energy (DOE) Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science.

Author information

Affiliations

  1. BioDiscovery Institute, University of North Texas, Denton, Texas 76203, USA

    • Jaime Barros
    • , Juan C. Serrani-Yarce
    • , Fang Chen
    • , David Baxter
    • , Barney J. Venables
    •  & Richard A. Dixon
  2. Department of Biological Sciences, University of North Texas, Denton, Texas 76203, USA

    • Jaime Barros
    • , Juan C. Serrani-Yarce
    • , Fang Chen
    •  & Richard A. Dixon
  3. BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA

    • Fang Chen
    •  & Richard A. Dixon

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Contributions

R.A.D. and J.B. conceived the study; J.B., J.S.-Y., F.C. and R.A.D. designed the experiments; J.B, J.S.-Y. and D.B. performed experimental work; J.B., J.S.-Y., D.B., B.V., F.C. and R.A.D. discussed and interpreted results; J.B. and R.A.D. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Richard A. Dixon.

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