Journal Article

Engineered reduction of S-adenosylmethionine alters lignin in sorghum

Chin, Dylan, Atim, Jackie, Wu, Chuan-Yin, Shih, Patrick M., Putnam, Daniel H., Hutmacher, Robert, De Ben, Christopher M., Bowen, Benjamin P., Harwood, Thomas, Chai, Yen Ning, Simmons, Blake A., Dalton, Jutta, Mortimer, Jenny C., Scheller, Henrik V., Turumtay, Halbay, Choudhary, Hemant, Vuu, Khanh M., Louie, Katherine B., Northen, Trent R., Gao, Yu, Park, Joon-Hyun, Turumtay, Emine Akyuz, Baidoo, Edward E. K., Eudes, Aymerick, Tian, Yang, Scown, Corinne D.

2024

Overview

Background Lignin is an aromatic polymer deposited in secondary cell walls of higher plants to provide strength, rigidity, and hydrophobicity to vascular tissues. Due to its interconnections with cell wall polysaccharides, lignin plays important roles during plant growth and defense, but also has a negative impact on industrial processes aimed at obtaining monosaccharides from plant biomass. Engineering lignin offers a solution to this issue. For example, previous work showed that heterologous expression of a coliphage S -adenosylmethionine hydrolase (AdoMetase) was an effective approach to reduce lignin in the model plant Arabidopsis. The efficacy of this engineering strategy remains to be evaluated in bioenergy crops. Results We studied the impact of expressing AdoMetase on lignin synthesis in sorghum ( Sorghum bicolor L. Moench). Lignin content, monomer composition, and size, as well as biomass saccharification efficiency were determined in transgenic sorghum lines. The transcriptome and metabolome were analyzed in stems at three developmental stages. Plant growth and biomass composition was further evaluated under field conditions. Results evidenced that lignin was reduced by 18% in the best transgenic line, presumably due to reduced activity of the S -adenosylmethionine-dependent O -methyltransferases involved in lignin synthesis. The modified sorghum features altered lignin monomer composition and increased lignin molecular weights. The degree of methylation of glucuronic acid on xylan was reduced. These changes enabled a ~20% increase in glucose yield after biomass pretreatment and saccharification compared to wild type. RNA-seq and untargeted metabolomic analyses evidenced some pleiotropic effects associated with AdoMetase expression. The transgenic sorghum showed developmental delay and reduced biomass yields at harvest, especially under field growing conditions. Conclusions The expression of AdoMetase represents an effective lignin engineering approach in sorghum. However, considering that this strategy potentially impacts multiple S -adenosylmethionine-dependent methyltransferases, adequate promoters for fine-tuning AdoMetase expression will be needed to mitigate yield penalty.

• Publisher: BioMed Central,BioMed Central Ltd,Nature Publishing Group,Springer Science + Business Media,BMC
• Subject: Acids / Adenosylmethionine hydrolase / Agricultural production / Alcohol / Alternative energy sources / Amino acids / Analysis / Arabidopsis / Arabidopsis thaliana / Bioenergy crop / biofuels / Biomass / Biomass energy / Biosynthesis / Biotechnology / Carbon / Cell wall / Cell walls / Cellulose / Chemistry / Chemistry and Materials Science / coliphages / Composition / Corn / Developmental stages / Effectiveness / Energy crops / Environmental aspects / Environmental Engineering/Biotechnology / Enzymes / Flowers & plants / Genes / Genetic engineering / genetically modified organisms / Glucose / glucuronic acid / heterologous gene expression / Hydrolases / Hydrophobicity / Lignin / lignin content / Lignocellulose / Management / Metabolism / Metabolites / metabolome / Metabolomics / Methylation / Methyltransferases / Microbiology / Molecular weight / Monolignols / Monomers / Monosaccharides / Mutation / O-methyltransferases / phytomass / Plant biomass / Plant Breeding/Biotechnology / Plant growth / Plant tissues / Polyamines / Polymerization / Polymers / Polysaccharides / Production management / Renewable and Green Energy / Rigidity / RNA / S-Adenosylmethionine / Saccharides / Saccharification / sequence analysis / Sorghum / Sorghum bicolor / Sugars / Synthesis / transcriptome / Transcriptomes / Vascular tissue / Xylan