Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield

Lignocellulosic biomass is recalcitrant toward deconstruction into simple sugars mainly due to the presence of lignin. By engineering plants to partially replace traditional lignin monomers with alternative ones, lignin degradability and extractability can be enhanced. Previously, the alternative mo...

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Main Authors: Barbara De Meester, Paula Oyarce, Ruben Vanholme, Rebecca Van Acker, Yukiko Tsuji, Thijs Vangeel, Sander Van den Bosch, Jan Van Doorsselaere, Bert Sels, John Ralph, Wout Boerjan
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.943349/full
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author Barbara De Meester
Barbara De Meester
Paula Oyarce
Paula Oyarce
Ruben Vanholme
Ruben Vanholme
Rebecca Van Acker
Rebecca Van Acker
Yukiko Tsuji
Yukiko Tsuji
Thijs Vangeel
Sander Van den Bosch
Jan Van Doorsselaere
Bert Sels
John Ralph
John Ralph
Wout Boerjan
Wout Boerjan
author_facet Barbara De Meester
Barbara De Meester
Paula Oyarce
Paula Oyarce
Ruben Vanholme
Ruben Vanholme
Rebecca Van Acker
Rebecca Van Acker
Yukiko Tsuji
Yukiko Tsuji
Thijs Vangeel
Sander Van den Bosch
Jan Van Doorsselaere
Bert Sels
John Ralph
John Ralph
Wout Boerjan
Wout Boerjan
author_sort Barbara De Meester
collection DOAJ
description Lignocellulosic biomass is recalcitrant toward deconstruction into simple sugars mainly due to the presence of lignin. By engineering plants to partially replace traditional lignin monomers with alternative ones, lignin degradability and extractability can be enhanced. Previously, the alternative monomer curcumin has been successfully produced and incorporated into lignified cell walls of Arabidopsis by the heterologous expression of DIKETIDE-CoA SYNTHASE (DCS) and CURCUMIN SYNTHASE2 (CURS2). The resulting transgenic plants did not suffer from yield penalties and had an increased saccharification yield after alkaline pretreatment. Here, we translated this strategy into the bio-energy crop poplar. Via the heterologous expression of DCS and CURS2 under the control of the secondary cell wall CELLULOSE SYNTHASE A8-B promoter (ProCesA8-B), curcumin was also produced and incorporated into the lignified cell walls of poplar. ProCesA8-B:DCS_CURS2 transgenic poplars, however, suffered from shoot-tip necrosis and yield penalties. Compared to that of the wild-type (WT), the wood of transgenic poplars had 21% less cellulose, 28% more matrix polysaccharides, 23% more lignin and a significantly altered lignin composition. More specifically, ProCesA8-B:DCS_CURS2 lignin had a reduced syringyl/guaiacyl unit (S/G) ratio, an increased frequency of p-hydroxyphenyl (H) units, a decreased frequency of p-hydroxybenzoates and a higher fraction of phenylcoumaran units. Without, or with alkaline or hot water pretreatment, the saccharification efficiency of the transgenic lines was equal to that of the WT. These differences in (growth) phenotype illustrate that translational research in crops is essential to assess the value of an engineering strategy for applications. Further fine-tuning of this research strategy (e.g., by using more specific promoters or by translating this strategy to other crops such as maize) might lead to transgenic bio-energy crops with cell walls more amenable to deconstruction without settling in yield.
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spelling doaj.art-fe170f1c3a804e268a53dcfc4d9e29c32022-12-22T01:20:53ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-07-011310.3389/fpls.2022.943349943349Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass YieldBarbara De Meester0Barbara De Meester1Paula Oyarce2Paula Oyarce3Ruben Vanholme4Ruben Vanholme5Rebecca Van Acker6Rebecca Van Acker7Yukiko Tsuji8Yukiko Tsuji9Thijs Vangeel10Sander Van den Bosch11Jan Van Doorsselaere12Bert Sels13John Ralph14John Ralph15Wout Boerjan16Wout Boerjan17Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Biochemistry, University of Wisconsin, Madison, WI, United StatesUS Department of Energy, Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, WI, United StatesCenter for Sustainable Catalysis and Engineering, KU Leuven, Leuven, BelgiumCenter for Sustainable Catalysis and Engineering, KU Leuven, Leuven, BelgiumVIVES, Roeselare, BelgiumCenter for Sustainable Catalysis and Engineering, KU Leuven, Leuven, BelgiumDepartment of Biochemistry, University of Wisconsin, Madison, WI, United StatesUS Department of Energy, Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, WI, United StatesDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumLignocellulosic biomass is recalcitrant toward deconstruction into simple sugars mainly due to the presence of lignin. By engineering plants to partially replace traditional lignin monomers with alternative ones, lignin degradability and extractability can be enhanced. Previously, the alternative monomer curcumin has been successfully produced and incorporated into lignified cell walls of Arabidopsis by the heterologous expression of DIKETIDE-CoA SYNTHASE (DCS) and CURCUMIN SYNTHASE2 (CURS2). The resulting transgenic plants did not suffer from yield penalties and had an increased saccharification yield after alkaline pretreatment. Here, we translated this strategy into the bio-energy crop poplar. Via the heterologous expression of DCS and CURS2 under the control of the secondary cell wall CELLULOSE SYNTHASE A8-B promoter (ProCesA8-B), curcumin was also produced and incorporated into the lignified cell walls of poplar. ProCesA8-B:DCS_CURS2 transgenic poplars, however, suffered from shoot-tip necrosis and yield penalties. Compared to that of the wild-type (WT), the wood of transgenic poplars had 21% less cellulose, 28% more matrix polysaccharides, 23% more lignin and a significantly altered lignin composition. More specifically, ProCesA8-B:DCS_CURS2 lignin had a reduced syringyl/guaiacyl unit (S/G) ratio, an increased frequency of p-hydroxyphenyl (H) units, a decreased frequency of p-hydroxybenzoates and a higher fraction of phenylcoumaran units. Without, or with alkaline or hot water pretreatment, the saccharification efficiency of the transgenic lines was equal to that of the WT. These differences in (growth) phenotype illustrate that translational research in crops is essential to assess the value of an engineering strategy for applications. Further fine-tuning of this research strategy (e.g., by using more specific promoters or by translating this strategy to other crops such as maize) might lead to transgenic bio-energy crops with cell walls more amenable to deconstruction without settling in yield.https://www.frontiersin.org/articles/10.3389/fpls.2022.943349/fullligninlignin engineeringalternative lignin monomerspoplarcurcumintranslational research
spellingShingle Barbara De Meester
Barbara De Meester
Paula Oyarce
Paula Oyarce
Ruben Vanholme
Ruben Vanholme
Rebecca Van Acker
Rebecca Van Acker
Yukiko Tsuji
Yukiko Tsuji
Thijs Vangeel
Sander Van den Bosch
Jan Van Doorsselaere
Bert Sels
John Ralph
John Ralph
Wout Boerjan
Wout Boerjan
Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield
Frontiers in Plant Science
lignin
lignin engineering
alternative lignin monomers
poplar
curcumin
translational research
title Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield
title_full Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield
title_fullStr Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield
title_full_unstemmed Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield
title_short Engineering Curcumin Biosynthesis in Poplar Affects Lignification and Biomass Yield
title_sort engineering curcumin biosynthesis in poplar affects lignification and biomass yield
topic lignin
lignin engineering
alternative lignin monomers
poplar
curcumin
translational research
url https://www.frontiersin.org/articles/10.3389/fpls.2022.943349/full
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