Engineered reduction of S-adenosylmethionine alters lignin in sorghum
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 al...
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2024-10-01
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| Series: | Biotechnology for Biofuels and Bioproducts |
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| Online Access: | https://doi.org/10.1186/s13068-024-02572-8 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Yang Tian |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-0ca54f0577224f1fabb4d3ef015fb5ed |
| institution | OA Journals |
| issn | 2731-3654 |
| language | English |
| publishDate | 2024-10-01 |
| publisher | BMC |
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| series | Biotechnology for Biofuels and Bioproducts |
| spelling | doaj-art-0ca54f0577224f1fabb4d3ef015fb5ed2025-08-20T02:17:37ZengBMCBiotechnology for Biofuels and Bioproducts2731-36542024-10-0117111610.1186/s13068-024-02572-8Engineered reduction of S-adenosylmethionine alters lignin in sorghumYang Tian0Yu Gao1Halbay Turumtay2Emine Akyuz Turumtay3Yen Ning Chai4Hemant Choudhary5Joon-Hyun Park6Chuan-Yin Wu7Christopher M. De Ben8Jutta Dalton9Katherine B. Louie10Thomas Harwood11Dylan Chin12Khanh M. Vuu13Benjamin P. Bowen14Patrick M. Shih15Edward E. K. Baidoo16Trent R. Northen17Blake A. Simmons18Robert Hutmacher19Jackie Atim20Daniel H. Putnam21Corinne D. Scown22Jenny C. Mortimer23Henrik V. Scheller24Aymerick Eudes25Joint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteForage Genetics InternationalForage Genetics InternationalDepartment of Plant Sciences, University of California-DavisJoint BioEnergy InstituteEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National LaboratoryEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National LaboratoryJoint BioEnergy InstituteJoint BioEnergy InstituteEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National LaboratoryJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteJoint BioEnergy InstituteAbstract 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.https://doi.org/10.1186/s13068-024-02572-8Cell wallMonolignolsSaccharificationO-methyltransferasesBioenergy crop |
| spellingShingle | 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 Engineered reduction of S-adenosylmethionine alters lignin in sorghum Biotechnology for Biofuels and Bioproducts Cell wall Monolignols Saccharification O-methyltransferases Bioenergy crop |
| title | Engineered reduction of S-adenosylmethionine alters lignin in sorghum |
| title_full | Engineered reduction of S-adenosylmethionine alters lignin in sorghum |
| title_fullStr | Engineered reduction of S-adenosylmethionine alters lignin in sorghum |
| title_full_unstemmed | Engineered reduction of S-adenosylmethionine alters lignin in sorghum |
| title_short | Engineered reduction of S-adenosylmethionine alters lignin in sorghum |
| title_sort | engineered reduction of s adenosylmethionine alters lignin in sorghum |
| topic | Cell wall Monolignols Saccharification O-methyltransferases Bioenergy crop |
| url | https://doi.org/10.1186/s13068-024-02572-8 |
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