Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild types

The potential of whole genome duplication to increase plant biomass yield is well-known. In Arabidopsis tetraploids, an increase in biomass yield was accompanied by a reduction in lignin content and, as a result, a higher saccharification efficiency was achieved compared with diploid controls. Here,...

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Main Authors: Marlies Wouters, Sander Corneillie, Angelo Dewitte, Jan Van Doorsselaere, Jan Van den Bulcke, Joris Van Acker, Bartel Vanholme, Wout Boerjan
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.995402/full
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author Marlies Wouters
Marlies Wouters
Sander Corneillie
Sander Corneillie
Angelo Dewitte
Jan Van Doorsselaere
Jan Van den Bulcke
Joris Van Acker
Bartel Vanholme
Bartel Vanholme
Wout Boerjan
Wout Boerjan
author_facet Marlies Wouters
Marlies Wouters
Sander Corneillie
Sander Corneillie
Angelo Dewitte
Jan Van Doorsselaere
Jan Van den Bulcke
Joris Van Acker
Bartel Vanholme
Bartel Vanholme
Wout Boerjan
Wout Boerjan
author_sort Marlies Wouters
collection DOAJ
description The potential of whole genome duplication to increase plant biomass yield is well-known. In Arabidopsis tetraploids, an increase in biomass yield was accompanied by a reduction in lignin content and, as a result, a higher saccharification efficiency was achieved compared with diploid controls. Here, we evaluated whether the results obtained in Arabidopsis could be translated into poplar and whether the enhanced saccharification yield upon alkaline pretreatment of hairpin-downregulated CINNAMYL ALCOHOL DEHYDROGENASE1 (hpCAD) transgenic poplar could be further improved upon a whole genome duplication. Using a colchicine treatment, wild-type (WT) Populus tremula x P. alba cv. INRA 717-1B4, a commonly used model clone in tree biotechnology research, and hpCAD tetraploids were generated and grown in the greenhouse. In parallel, WT tetraploid poplars were grown in the field. In contrast to Arabidopsis, a whole genome duplication of poplar had a negative impact on the biomass yield of both greenhouse- and field-grown trees. Strikingly, field-grown WT tetraploids developed a brittle apex phenotype, i.e., their tip broke off just below the apex. In addition, the chromosome doubling altered the biomass composition of field-grown, but not of greenhouse-grown tetraploid poplars. More specifically, the lignin content of field-grown tetraploid poplars was increased at the expense of matrix polysaccharides. This increase in lignin deposition in biomass is likely the cause of the observed brittle apex phenotype, though no major differences in stem anatomy or in mechanical properties could be found between di- and tetraploid WT poplars grown in the field. Finally, without biomass pretreatment, the saccharification efficiency of greenhouse- and field-grown WT diploids was not different from that of tetraploids, whereas that of greenhouse-grown hpCAD tetraploids was higher than that of greenhouse-grown diploids. Upon alkaline pretreatment, the saccharification yield of diploids was similar to that of tetraploids for all genotypes and growth conditions tested. This study showed that a whole genome duplication in hybrid WT and hpCAD poplar did neither result in further improvements in biomass yield, nor in improved biomass composition and, hence, saccharification performance.
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spelling doaj.art-68d23e4a4a4e44ba879858c34ebdce152022-12-22T04:24:42ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-09-011310.3389/fpls.2022.995402995402Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild typesMarlies Wouters0Marlies Wouters1Sander Corneillie2Sander Corneillie3Angelo Dewitte4Jan Van Doorsselaere5Jan Van den Bulcke6Joris Van Acker7Bartel Vanholme8Bartel Vanholme9Wout Boerjan10Wout Boerjan11Department 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, BelgiumExpertisecentrum Agro- en Biotechnologie, VIVES, Roeselare, BelgiumExpertisecentrum Agro- en Biotechnologie, VIVES, Roeselare, BelgiumLaboratory of Wood Technology, Department of Environment, Faculty of Bioscience Engineering, Ghent University, Ghent, BelgiumLaboratory of Wood Technology, Department of Environment, Faculty of Bioscience Engineering, Ghent University, 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, BelgiumThe potential of whole genome duplication to increase plant biomass yield is well-known. In Arabidopsis tetraploids, an increase in biomass yield was accompanied by a reduction in lignin content and, as a result, a higher saccharification efficiency was achieved compared with diploid controls. Here, we evaluated whether the results obtained in Arabidopsis could be translated into poplar and whether the enhanced saccharification yield upon alkaline pretreatment of hairpin-downregulated CINNAMYL ALCOHOL DEHYDROGENASE1 (hpCAD) transgenic poplar could be further improved upon a whole genome duplication. Using a colchicine treatment, wild-type (WT) Populus tremula x P. alba cv. INRA 717-1B4, a commonly used model clone in tree biotechnology research, and hpCAD tetraploids were generated and grown in the greenhouse. In parallel, WT tetraploid poplars were grown in the field. In contrast to Arabidopsis, a whole genome duplication of poplar had a negative impact on the biomass yield of both greenhouse- and field-grown trees. Strikingly, field-grown WT tetraploids developed a brittle apex phenotype, i.e., their tip broke off just below the apex. In addition, the chromosome doubling altered the biomass composition of field-grown, but not of greenhouse-grown tetraploid poplars. More specifically, the lignin content of field-grown tetraploid poplars was increased at the expense of matrix polysaccharides. This increase in lignin deposition in biomass is likely the cause of the observed brittle apex phenotype, though no major differences in stem anatomy or in mechanical properties could be found between di- and tetraploid WT poplars grown in the field. Finally, without biomass pretreatment, the saccharification efficiency of greenhouse- and field-grown WT diploids was not different from that of tetraploids, whereas that of greenhouse-grown hpCAD tetraploids was higher than that of greenhouse-grown diploids. Upon alkaline pretreatment, the saccharification yield of diploids was similar to that of tetraploids for all genotypes and growth conditions tested. This study showed that a whole genome duplication in hybrid WT and hpCAD poplar did neither result in further improvements in biomass yield, nor in improved biomass composition and, hence, saccharification performance.https://www.frontiersin.org/articles/10.3389/fpls.2022.995402/fullpolyploidyfield trialCADligninsaccharification
spellingShingle Marlies Wouters
Marlies Wouters
Sander Corneillie
Sander Corneillie
Angelo Dewitte
Jan Van Doorsselaere
Jan Van den Bulcke
Joris Van Acker
Bartel Vanholme
Bartel Vanholme
Wout Boerjan
Wout Boerjan
Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild types
Frontiers in Plant Science
polyploidy
field trial
CAD
lignin
saccharification
title Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild types
title_full Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild types
title_fullStr Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild types
title_full_unstemmed Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild types
title_short Whole genome duplication of wild-type and CINNAMYL ALCOHOL DEHYDROGENASE1-downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field-grown wild types
title_sort whole genome duplication of wild type and cinnamyl alcohol dehydrogenase1 downregulated hybrid poplar reduces biomass yield and causes a brittle apex phenotype in field grown wild types
topic polyploidy
field trial
CAD
lignin
saccharification
url https://www.frontiersin.org/articles/10.3389/fpls.2022.995402/full
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