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Title: Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen

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 processabilitymore » 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.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4]; ORCiD logo [4];  [5];  [6];  [6];  [1];  [1];  [4];  [5];  [6];  [5];  [2];  [3]; ORCiD logo [1]
  1. Tokyo Univ. of Agriculture and Technology (Japan)
  2. Nagaoka Univ. of Technology (Japan)
  3. National Inst. of Advanced Industrial Science and Technology (AIST), Tsukuba (Japan)
  4. Forest Research and Management Organization, Ibaraki (Japan)
  5. Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
  6. Ghent Univ. (Belgium); VIB Center for Plant Systems Biology, Ghent (Belgium)
Publication Date:
Research Org.:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Japan Science and Technology Agency
OSTI Identifier:
1846175
Alternate Identifier(s):
OSTI ID: 1854981
Grant/Contract Number:  
SC0018409; JPMJAL1107
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 110; Journal Issue: 2; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; heterologous expression; lignocellulose; metabolome; phenolic metabolites; RNAseq; shikimate pathway; saccharification efficiency

Citation Formats

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, and Kajita, Shinya. Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen. United States: N. p., 2022. Web. doi:10.1111/tpj.15674.
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. Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen. United States. https://doi.org/10.1111/tpj.15674
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, and Kajita, Shinya. Wed . "Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen". United States. https://doi.org/10.1111/tpj.15674. https://www.osti.gov/servlets/purl/1846175.
@article{osti_1846175,
title = {Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen},
author = {Hu, Shi and Kamimura, Naofumi and Sakamoto, Shingo and Nagano, Soichiro and Takata, Naoki and Liu, Sarah and Goeminne, Geert and Vanholme, Ruben and Uesugi, Mikiko and Yamamoto, Masanobu and Hishiyama, Shojiro and Kim, Hoon and Boerjan, Wout and Ralph, John and Masai, Eiji and Mitsuda, Nobutaka and Kajita, Shinya},
abstractNote = {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.},
doi = {10.1111/tpj.15674},
journal = {The Plant Journal},
number = 2,
volume = 110,
place = {United States},
year = {Wed Jan 19 00:00:00 EST 2022},
month = {Wed Jan 19 00:00:00 EST 2022}
}

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