Abstract
Lignin biosynthesis begins with the deamination of phenylalanine and tyrosine (Tyr) as a key branch point between primary and secondary metabolism in land plants. Here, we used a systems biology approach to investigate the global metabolic responses to lignin pathway perturbations in the model grass Brachypodium distachyon. We identified the lignin biosynthetic protein families and found that ammonia-lyases (ALs) are among the most abundant proteins in lignifying tissues in grasses. Integrated metabolomic and proteomic data support a link between lignin biosynthesis and primary metabolism mediated by the ammonia released from ALs that is recycled for the synthesis of amino acids via glutamine. RNA interference knockdown of lignin genes confirmed that the route of the canonical pathway using shikimate ester intermediates is not essential for lignin formation in Brachypodium, and there is an alternative pathway from Tyr via sinapic acid for the synthesis of syringyl lignin involving yet uncharacterized enzymatic steps. Our findings support a model in which plant ALs play a central role in coordinating the allocation of carbon for lignin synthesis and the nitrogen available for plant growth. Collectively, these data also emphasize the value of integrative multiomic analyses to advance our understanding of plant metabolism.
| Original language | English |
|---|---|
| Pages (from-to) | 3339-3363 |
| Number of pages | 25 |
| Journal | Plant Cell |
| Volume | 34 |
| Issue number | 9 |
| DOIs | |
| State | Published - Sep 2022 |
Funding
We thank the BioAnalytical Facility at the University of North Texas for support with MS and 13C-isotopic labeling analyses, and the three anonymous reviewers for their helpful suggestions. This work was supported by the BioEnergy Science Center and the Center for Bioenergy Innovation (Oak Ridge National Laboratory), US Department of Energy (DOE) Bioenergy Research Centers supported by the Office of Biological and Environmental Research in the DOE Office of Science, and the University of North Texas. This manuscript has been co-authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the US Department of Energy. J.B. is also indebted to the Fundacion Barrie and the Spanish Foundation for Science and Technology for postdoctoral training fellowships, and acknowledges a CBI-Early Career Research Fellowship received as a Visiting Fellow at Oak Ridge National Laboratory, during which period the proteomics data were generated.