Engineered reduction of S-adenosylmethionine alters lignin in sorghum

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

doi:10.1186/s13068-024-02572-8

Engineered reduction of S-adenosylmethionine alters lignin in sorghum

Biotechnol Biofuels Bioprod. 2024 Oct 15;17(1):128. doi: 10.1186/s13068-024-02572-8.

Authors

Yang Tian^{1

2}, Yu Gao^{1

2}, Halbay Turumtay^{1

2

3}, Emine Akyuz Turumtay^{1

2

4}, Yen Ning Chai^{1

2}, Hemant Choudhary^{1

5}, Joon-Hyun Park⁶, Chuan-Yin Wu⁶, Christopher M De Ben⁷, Jutta Dalton^{1

2}, Katherine B Louie^{2

8}, Thomas Harwood^{2

8}, Dylan Chin^{1

9}, Khanh M Vuu^{1

2}, Benjamin P Bowen^{2

8}, Patrick M Shih^{1

2

10}, Edward E K Baidoo^{1

11}, Trent R Northen^{1

2

8}, Blake A Simmons^{1

11}, Robert Hutmacher^{1

12}, Jackie Atim^{1

12}, Daniel H Putnam^{1

7}, Corinne D Scown^{1

11

13

14}, Jenny C Mortimer^{1

2

15}, Henrik V Scheller^{1

2

10}, Aymerick Eudes^{16

17}

Affiliations

¹ Joint BioEnergy Institute, Emeryville, CA, 94608, USA.
² Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, One Cyclotron Road, MS 978R4468, Berkeley, CA, 94720, USA.
³ Department of Energy System Engineering, Karadeniz Technical University, 61830, Trabzon, Turkey.
⁴ Department of Chemistry, Recep Tayyip Erdogan University, 53100, Rize, Turkey.
⁵ Department of Bioresource and Environmental Security, Sandia National Laboratories, Livermore, CA, 94550, USA.
⁶ Forage Genetics International, West Salem, WI, 54669, USA.
⁷ Department of Plant Sciences, University of California-Davis, Davis, CA, 95616, USA.
⁸ Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA.
⁹ Rausser College of Natural Resources, University of California-Berkeley, Berkeley, CA, 94720, USA.
¹⁰ Department of Plant and Microbial Biology, University of California-Berkeley, Berkeley, CA, 94720, USA.
¹¹ Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA.
¹² University of California, Agriculture and Natural Resources, Kearney Agricultural Research and Extension Center, Parlier, CA, 93648, USA.
¹³ Energy & Biosciences Institute, University of California-Berkeley, Berkeley, CA, 94720, USA.
¹⁴ Energy Analysis and Environmental Impacts Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA.
¹⁵ School of Agriculture, Food, and Wine, University of Adelaide, Glen Osmond, South Australia, Australia.
¹⁶ Joint BioEnergy Institute, Emeryville, CA, 94608, USA. [email protected].
¹⁷ Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, One Cyclotron Road, MS 978R4468, Berkeley, CA, 94720, USA. [email protected].

Abstract

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.

Keywords: O-methyltransferases; Bioenergy crop; Cell wall; Monolignols; Saccharification.