Expression of dehydroshikimate dehydratase in poplar induces transcriptional and metabolic changes in the phenylpropanoid pathway

Author:

Akyuz Turumtay Emine123,Turumtay Halbay124,Tian Yang12ORCID,Lin Chien-Yuan12,Chai Yen Ning12,Louie Katherine B25,Chen Yan16,Lipzen Anna5,Harwood Thomas25,Satish Kumar Kavitha12,Bowen Benjamin P25,Wang Qian78,Mansfield Shawn D789ORCID,Blow Matthew J5,Petzold Christopher J16,Northen Trent R25ORCID,Mortimer Jenny C1210,Scheller Henrik V1211ORCID,Eudes Aymerick12ORCID

Affiliation:

1. Feedstocks Division, Joint BioEnergy Institute , Emeryville, CA , USA

2. Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory , Berkeley, CA , USA

3. Recep Tayyip Erdogan University, Department of Chemistry , 53100, Rize , Turkiye

4. Karadeniz Technical University, Department of Energy System Engineering , 61830, Trabzon , Turkiye

5. Joint Genome Institute, Lawrence Berkeley National Laboratory , Berkeley, CA , USA

6. Biological Systems & Engineering Division, Lawrence Berkeley National Laboratory , Berkeley, CA , USA

7. Department of Wood Science, University of British Columbia , Vancouver, BC , Canada

8. Department of Botany, University of British Columbia , Vancouver, BC , Canada

9. DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute , Madison, WI 53726 , USA

10. School of Agriculture, Food and Wine & Waite Research Institute, University of Adelaide , Glen Osmond, SA , Australia

11. Department of Plant and Microbial Biology, University of California, Berkeley , Berkeley, CA , USA

Abstract

Abstract Modification of lignin in feedstocks via genetic engineering aims to reduce biomass recalcitrance to facilitate efficient conversion processes. These improvements can be achieved by expressing exogenous enzymes that interfere with native biosynthetic pathways responsible for the production of the lignin precursors. In planta expression of a bacterial 3-dehydroshikimate dehydratase in poplar trees reduced lignin content and altered the monomer composition, which enabled higher yields of sugars after cell wall polysaccharide hydrolysis. Understanding how plants respond to such genetic modifications at the transcriptional and metabolic levels is needed to facilitate further improvement and field deployment. In this work, we acquired fundamental knowledge on lignin-modified poplar expressing 3-dehydroshikimate dehydratase using RNA-seq and metabolomics. The data clearly demonstrate that changes in gene expression and metabolite abundance can occur in a strict spatiotemporal fashion, revealing tissue-specific responses in the xylem, phloem, or periderm. In the poplar line that exhibited the strongest reduction in lignin, we found that 3% of the transcripts had altered expression levels and ~19% of the detected metabolites had differential abundance in the xylem from older stems. The changes affected predominantly the shikimate and phenylpropanoid pathways as well as secondary cell wall metabolism, and resulted in significant accumulation of hydroxybenzoates derived from protocatechuate and salicylate.

Funder

Lawrence Berkeley National Laboratory

U.S. Department of Energy

Publisher

Oxford University Press (OUP)

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