Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen. (14th March 2022)

• Record Type: Journal Article
• Authors: Hu, Shi; Kamimura, Naofumi; Sakamoto, Shingo; Nagano, Soichiro; Takata, Naoki; Liu, Sarah; Goeminne, Geert; Vanholme, Ruben; Uesugi, Mikiko; Yamamoto, Masanobu; Hishiyama, Shojiro; Kim, Hoon; Boerjan, Wout; Ralph, John; Masai, Eiji; Mitsuda, Nobutaka; Kajita, Shinya
• Is Part Of: Plant journal. Volume 110:Number 2(2022)
• Page Start: 358
• Page End: 376
• Publication Date: 2022-03-14
• Subjects: heterologous expression -- lignocellulose -- metabolome -- phenolic metabolites -- RNA‐seq -- shikimate pathway -- saccharification efficiency; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15674
• Languages: English
• ISSNs: 0960-7412

Abstract

SUMMARY: Lignin is a phenolic polymer deposited in the plant cell wall, and is mainly polymerized from three canonical monomers (monolignols), i.e. p ‐coumaryl, coniferyl and sinapyl alcohols. After polymerization, these alcohols form different lignin substructures. In dicotyledons, monolignols are biosynthesized from phenylalanine, an aromatic amino acid. Shikimate acts at two positions in the route to the lignin building blocks. It is part of the shikimate pathway that provides the precursor for the biosynthesis of phenylalanine, and is involved in the transesterification of p ‐coumaroyl‐CoA to p ‐coumaroyl shikimate, one of the key steps in the biosynthesis of coniferyl and sinapyl alcohols. The shikimate residue in p ‐coumaroyl shikimate is released in later steps, and the resulting shikimate becomes available again for the biosynthesis of new p ‐coumaroyl shikimate molecules. In this study, we inhibited cytosolic shikimate recycling in transgenic hybrid aspen by accelerated phosphorylation of shikimate in the cytosol through expression of a bacterial shikimate kinase (SK). This expression elicited an increase in p ‐hydroxyphenyl units of lignin and, by contrast, a decrease in guaiacyl and syringyl units. Transgenic plants with high SK activity produced a lignin content comparable to that in wild‐type plants, and had an increased processability via enzymatic saccharification. Although expression of many genes was altered in the transgenic plants, elevated SK activity did not exert a significant effect on the expression of the majority of genes responsible for lignin biosynthesis. The present results indicate that cytosolic shikimate recycling is crucial to the monomeric composition of lignin rather than for lignin content. Significance Statement: To investigate the role of shikimate recycling in lignin biosynthesis, cytosolic shikimate availability was reduced by overexpression of a bacterial shikimate kinase in hybrid aspen. The transgenic trees showed an increase in p ‐hydroxyphenyl units of lignin without alteration of lignin level, and the change in the structure led to reduced biomass recalcitrance with higher delignification and improved cell wall digestibility.