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Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.)

BACKGROUND: Lignin deposited in plant cell walls negatively affects biomass conversion into advanced bioproducts. There is therefore a strong interest in developing bioenergy crops with reduced lignin content or altered lignin structures. Another desired trait for bioenergy crops is the ability to a...

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Autores principales: Hao, Zhangying, Yogiswara, Sasha, Wei, Tong, Benites, Veronica Teixeira, Sinha, Anagh, Wang, George, Baidoo, Edward E. K., Ronald, Pamela C., Scheller, Henrik V., Loqué, Dominique, Eudes, Aymerick
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7819203/
https://www.ncbi.nlm.nih.gov/pubmed/33478381
http://dx.doi.org/10.1186/s12870-021-02842-9
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author Hao, Zhangying
Yogiswara, Sasha
Wei, Tong
Benites, Veronica Teixeira
Sinha, Anagh
Wang, George
Baidoo, Edward E. K.
Ronald, Pamela C.
Scheller, Henrik V.
Loqué, Dominique
Eudes, Aymerick
author_facet Hao, Zhangying
Yogiswara, Sasha
Wei, Tong
Benites, Veronica Teixeira
Sinha, Anagh
Wang, George
Baidoo, Edward E. K.
Ronald, Pamela C.
Scheller, Henrik V.
Loqué, Dominique
Eudes, Aymerick
author_sort Hao, Zhangying
collection PubMed
description BACKGROUND: Lignin deposited in plant cell walls negatively affects biomass conversion into advanced bioproducts. There is therefore a strong interest in developing bioenergy crops with reduced lignin content or altered lignin structures. Another desired trait for bioenergy crops is the ability to accumulate novel bioproducts, which would enhance the development of economically sustainable biorefineries. As previously demonstrated in the model plant Arabidopsis, expression of a 3-dehydroshikimate dehydratase in plants offers the potential for decreasing lignin content and overproducing a value-added metabolic coproduct (i.e., protocatechuate) suitable for biological upgrading. RESULTS: The 3-dehydroshikimate dehydratase QsuB from Corynebacterium glutamicum was expressed in the bioenergy crop switchgrass (Panicum virgatum L.) using the stem-specific promoter of an O-methyltransferase gene (pShOMT) from sugarcane. The activity of pShOMT was validated in switchgrass after observation in-situ of beta-glucuronidase (GUS) activity in stem nodes of plants carrying a pShOMT::GUS fusion construct. Under controlled growth conditions, engineered switchgrass lines containing a pShOMT::QsuB construct showed reductions of lignin content, improvements of biomass saccharification efficiency, and accumulated higher amount of protocatechuate compared to control plants. Attempts to generate transgenic switchgrass lines carrying the QsuB gene under the control of the constitutive promoter pZmUbi-1 were unsuccessful, suggesting possible toxicity issues associated with ectopic QsuB expression during the plant regeneration process. CONCLUSION: This study validates the transfer of the QsuB engineering approach from a model plant to switchgrass. We have demonstrated altered expression of two important traits: lignin content and accumulation of a co-product. We found that the choice of promoter to drive QsuB expression should be carefully considered when deploying this strategy to other bioenergy crops. Field-testing of engineered QsuB switchgrass are in progress to assess the performance of the introduced traits and agronomic performances of the transgenic plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02842-9.
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spelling pubmed-78192032021-01-22 Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.) Hao, Zhangying Yogiswara, Sasha Wei, Tong Benites, Veronica Teixeira Sinha, Anagh Wang, George Baidoo, Edward E. K. Ronald, Pamela C. Scheller, Henrik V. Loqué, Dominique Eudes, Aymerick BMC Plant Biol Research Article BACKGROUND: Lignin deposited in plant cell walls negatively affects biomass conversion into advanced bioproducts. There is therefore a strong interest in developing bioenergy crops with reduced lignin content or altered lignin structures. Another desired trait for bioenergy crops is the ability to accumulate novel bioproducts, which would enhance the development of economically sustainable biorefineries. As previously demonstrated in the model plant Arabidopsis, expression of a 3-dehydroshikimate dehydratase in plants offers the potential for decreasing lignin content and overproducing a value-added metabolic coproduct (i.e., protocatechuate) suitable for biological upgrading. RESULTS: The 3-dehydroshikimate dehydratase QsuB from Corynebacterium glutamicum was expressed in the bioenergy crop switchgrass (Panicum virgatum L.) using the stem-specific promoter of an O-methyltransferase gene (pShOMT) from sugarcane. The activity of pShOMT was validated in switchgrass after observation in-situ of beta-glucuronidase (GUS) activity in stem nodes of plants carrying a pShOMT::GUS fusion construct. Under controlled growth conditions, engineered switchgrass lines containing a pShOMT::QsuB construct showed reductions of lignin content, improvements of biomass saccharification efficiency, and accumulated higher amount of protocatechuate compared to control plants. Attempts to generate transgenic switchgrass lines carrying the QsuB gene under the control of the constitutive promoter pZmUbi-1 were unsuccessful, suggesting possible toxicity issues associated with ectopic QsuB expression during the plant regeneration process. CONCLUSION: This study validates the transfer of the QsuB engineering approach from a model plant to switchgrass. We have demonstrated altered expression of two important traits: lignin content and accumulation of a co-product. We found that the choice of promoter to drive QsuB expression should be carefully considered when deploying this strategy to other bioenergy crops. Field-testing of engineered QsuB switchgrass are in progress to assess the performance of the introduced traits and agronomic performances of the transgenic plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02842-9. BioMed Central 2021-01-21 /pmc/articles/PMC7819203/ /pubmed/33478381 http://dx.doi.org/10.1186/s12870-021-02842-9 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Hao, Zhangying
Yogiswara, Sasha
Wei, Tong
Benites, Veronica Teixeira
Sinha, Anagh
Wang, George
Baidoo, Edward E. K.
Ronald, Pamela C.
Scheller, Henrik V.
Loqué, Dominique
Eudes, Aymerick
Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.)
title Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.)
title_full Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.)
title_fullStr Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.)
title_full_unstemmed Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.)
title_short Expression of a bacterial 3-dehydroshikimate dehydratase (QsuB) reduces lignin and improves biomass saccharification efficiency in switchgrass (Panicum virgatum L.)
title_sort expression of a bacterial 3-dehydroshikimate dehydratase (qsub) reduces lignin and improves biomass saccharification efficiency in switchgrass (panicum virgatum l.)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7819203/
https://www.ncbi.nlm.nih.gov/pubmed/33478381
http://dx.doi.org/10.1186/s12870-021-02842-9
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