QT–GWAS: A novel method for unveiling biosynthetic loci affecting qualitative metabolic traits
Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining bio...
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| Published in | Molecular plant Vol. 16; no. 7; pp. 1212 - 1227 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Elsevier Inc
03.07.2023
Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted method designated as qualitative trait GWAS (QT–GWAS) that subjects qualitative metabolic traits to a genome-wide association study, while the conventional metabolite GWAS (mGWAS) mainly considers the quantitative variation of metabolites. As a proof of the validity of QT-GWAS, 23 and 15 of the retrieved associations identified in Arabidopsis thaliana by QT-GWAS and mGWAS, respectively, were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT–GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or in vitro enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UDP-GLYCOSYLTRANSFERASE 76C3 (UGT76C3) is able to hexosylate guanine in vitro and in planta, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans in vitro. Collectively, our study demonstrates that the untargeted QT–GWAS method can retrieve valid gene–metabolite associations at the level of enzyme-encoding genes, even new associations that cannot be found by the conventional mGWAS, providing a new approach for dissecting qualitative metabolic traits.
A novel genome-wide association method to uncover biosynthetic loci underlying qualitative metabolic traits (designated as QT–GWAS) was developed and compared with a conventional quantitative metabolite GWAS (mGWAS). At least 23 of the associations identified by QT-GWAS were supported by previous research, and 7 associations involving three metabolic enzyme-encoding genes (CYP706A5, UGT76C3, and SULT202B1) were newly confirmed, illustrating the power of QT–GWAS. |
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| AbstractList | Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remains unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted system-wide method in
Arabidopsis thaliana
, subjecting qualitative metabolic traits to a genome-wide association study (designated as Qualitative Trait GWAS or QT-GWAS), along with the more conventional metabolite GWAS (mGWAS) that considers the quantitative variation of metabolites. As proof of the validity of the QT-GWAS and mGWAS, 23 and 15 of the retrieved associations were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT-GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or
in vitro
enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UGT76C3 is able to hexosylate guanine
in vitro
and
in planta
, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans
in vitro
. Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted method designated as qualitative trait GWAS (QT–GWAS) that subjects qualitative metabolic traits to a genome-wide association study, while the conventional metabolite GWAS (mGWAS) mainly considers the quantitative variation of metabolites. As a proof of the validity of QT-GWAS, 23 and 15 of the retrieved associations identified in Arabidopsis thaliana by QT-GWAS and mGWAS, respectively, were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT–GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or in vitro enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UDP-GLYCOSYLTRANSFERASE 76C3 (UGT76C3) is able to hexosylate guanine in vitro and in planta, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans in vitro. Collectively, our study demonstrates that the untargeted QT–GWAS method can retrieve valid gene–metabolite associations at the level of enzyme-encoding genes, even new associations that cannot be found by the conventional mGWAS, providing a new approach for dissecting qualitative metabolic traits. A novel genome-wide association method to uncover biosynthetic loci underlying qualitative metabolic traits (designated as QT–GWAS) was developed and compared with a conventional quantitative metabolite GWAS (mGWAS). At least 23 of the associations identified by QT-GWAS were supported by previous research, and 7 associations involving three metabolic enzyme-encoding genes (CYP706A5, UGT76C3, and SULT202B1) were newly confirmed, illustrating the power of QT–GWAS. Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted method designated as qualitative trait GWAS (QT-GWAS) that subjects qualitative metabolic traits to a genome-wide association study, while the conventional metabolite GWAS (mGWAS) mainly considers the quantitative variation of metabolites. As a proof of the validity of QT-GWAS, 23 and 15 of the retrieved associations identified in Arabidopsis thaliana by QT-GWAS and mGWAS, respectively, were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT-GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or in vitro enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UDP-GLYCOSYLTRANSFERASE 76C3 (UGT76C3) is able to hexosylate guanine in vitro and in planta, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans in vitro. Collectively, our study demonstrates that the untargeted QT-GWAS method can retrieve valid gene-metabolite associations at the level of enzyme-encoding genes, even new associations that cannot be found by the conventional mGWAS, providing a new approach for dissecting qualitative metabolic traits.Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted method designated as qualitative trait GWAS (QT-GWAS) that subjects qualitative metabolic traits to a genome-wide association study, while the conventional metabolite GWAS (mGWAS) mainly considers the quantitative variation of metabolites. As a proof of the validity of QT-GWAS, 23 and 15 of the retrieved associations identified in Arabidopsis thaliana by QT-GWAS and mGWAS, respectively, were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT-GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or in vitro enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UDP-GLYCOSYLTRANSFERASE 76C3 (UGT76C3) is able to hexosylate guanine in vitro and in planta, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans in vitro. Collectively, our study demonstrates that the untargeted QT-GWAS method can retrieve valid gene-metabolite associations at the level of enzyme-encoding genes, even new associations that cannot be found by the conventional mGWAS, providing a new approach for dissecting qualitative metabolic traits. Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted method designated as qualitative trait GWAS (QT–GWAS) that subjects qualitative metabolic traits to a genome-wide association study, while the conventional metabolite GWAS (mGWAS) mainly considers the quantitative variation of metabolites. As a proof of the validity of QT-GWAS, 23 and 15 of the retrieved associations identified in Arabidopsis thaliana by QT-GWAS and mGWAS, respectively, were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT–GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or in vitro enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UDP-GLYCOSYLTRANSFERASE 76C3 (UGT76C3) is able to hexosylate guanine in vitro and in planta, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans in vitro. Collectively, our study demonstrates that the untargeted QT–GWAS method can retrieve valid gene–metabolite associations at the level of enzyme-encoding genes, even new associations that cannot be found by the conventional mGWAS, providing a new approach for dissecting qualitative metabolic traits. Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted method designated as qualitative trait GWAS (QT-GWAS) that subjects qualitative metabolic traits to a genome-wide association study, while the conventional metabolite GWAS (mGWAS) mainly considers the quantitative variation of metabolites. As a proof of the validity of QT-GWAS, 23 and 15 of the retrieved associations identified in Arabidopsis thaliana by QT-GWAS and mGWAS, respectively, were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT-GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or in vitro enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UDP-GLYCOSYLTRANSFERASE 76C3 (UGT76C3) is able to hexosylate guanine in vitro and in planta, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans in vitro. Collectively, our study demonstrates that the untargeted QT-GWAS method can retrieve valid gene-metabolite associations at the level of enzyme-encoding genes, even new associations that cannot be found by the conventional mGWAS, providing a new approach for dissecting qualitative metabolic traits. |
| Author | Morreel, Kris Peng, Meng Höfer, René Vanholme, Ruben Storme, Véronique Darrah, Chiarina Ralph, John Goeminne, Geert Brouckaert, Marlies Saeys, Yvan Boerjan, Wout Timokhin, Vitaliy I. El Houari, llias |
| AuthorAffiliation | 6 Ghent University Department of Applied Mathematics, Computer Science and Statistics, Ghent, Belgium 2 VIB Center for Plant Systems Biology, Ghent, Belgium 9 Department of Biochemistry, and U.S. Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, USA 1 Ghent University, Department of Plant Biotechnology and Bioinformatics, Ghent, Belgium 7 VIB Center for Inflammation Research, Ghent, Belgium 8 VIB Metabolomics Core, Ghent, Belgium |
| AuthorAffiliation_xml | – name: 1 Ghent University, Department of Plant Biotechnology and Bioinformatics, Ghent, Belgium – name: 7 VIB Center for Inflammation Research, Ghent, Belgium – name: 2 VIB Center for Plant Systems Biology, Ghent, Belgium – name: 6 Ghent University Department of Applied Mathematics, Computer Science and Statistics, Ghent, Belgium – name: 9 Department of Biochemistry, and U.S. Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, USA – name: 8 VIB Metabolomics Core, Ghent, Belgium |
| Author_xml | – sequence: 1 givenname: Marlies orcidid: 0000-0002-5893-3175 surname: Brouckaert fullname: Brouckaert, Marlies organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 2 givenname: Meng surname: Peng fullname: Peng, Meng organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 3 givenname: René surname: Höfer fullname: Höfer, René organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 4 givenname: llias surname: El Houari fullname: El Houari, llias organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 5 givenname: Chiarina surname: Darrah fullname: Darrah, Chiarina organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 6 givenname: Véronique surname: Storme fullname: Storme, Véronique organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 7 givenname: Yvan surname: Saeys fullname: Saeys, Yvan organization: Ghent University, Department of Applied Mathematics, Computer Science and Statistics, 9000 Ghent, Belgium – sequence: 8 givenname: Ruben surname: Vanholme fullname: Vanholme, Ruben organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 9 givenname: Geert surname: Goeminne fullname: Goeminne, Geert organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 10 givenname: Vitaliy I. surname: Timokhin fullname: Timokhin, Vitaliy I. organization: Department of Biochemistry, and US Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI 53706, USA – sequence: 11 givenname: John surname: Ralph fullname: Ralph, John organization: Department of Biochemistry, and US Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI 53706, USA – sequence: 12 givenname: Kris surname: Morreel fullname: Morreel, Kris organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium – sequence: 13 givenname: Wout orcidid: 0000-0003-1495-510X surname: Boerjan fullname: Boerjan, Wout email: wout.boerjan@psb.vib-ugent.be organization: Ghent University, Department of Plant Biotechnology and Bioinformatics, 9000 Ghent, Belgium |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37349988$$D View this record in MEDLINE/PubMed https://www.osti.gov/biblio/1989747$$D View this record in Osti.gov |
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| CitedBy_id | crossref_primary_10_1016_j_ijbiomac_2024_138821 crossref_primary_10_1093_plphys_kiad596 crossref_primary_10_1016_j_copbio_2024_103147 crossref_primary_10_3390_plants14040629 crossref_primary_10_3390_agronomy14102214 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 USDOE SC0018409 current address: VIB Agro-incubator, Nevele, Belgium current address: Research Institute for Chromatography, Kortrijk, Belgium current address: BioNTech SE, Mainz, Rhineland-Palatinate, Germany current address: Eunomia Research & Consulting, Bristol, United Kingdom current addresses are 6,7 |
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| SubjectTerms | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis thaliana biosynthesis cytochrome P-450 enzymes Genome-Wide Association Study guanine kingdom lignans metabolites metabolomics Metabolomics - methods Phenotype Polymorphism, Single Nucleotide Quantitative Trait Loci - genetics reverse genetics |
| Title | QT–GWAS: A novel method for unveiling biosynthetic loci affecting qualitative metabolic traits |
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