title: ZEAXANTHIN EPOXIDASE Activity Potentiates Carotenoid Degradation in Maturing Seed.
abstract: Elucidation of the carotenoid biosynthetic pathway has enabled altering the composition and content of carotenoids in various plants, but to achieve desired nutritional impacts, the genetic components regulating carotenoid homeostasis in seed, the plant organ consumed in greatest abundance, must be elucidated. We used a combination of linkage mapping, genome-wide association studies (GWAS), and pathway-level analysis to identify nine loci that impact the natural variation of seed carotenoids in Arabidopsis (Arabidopsis thaliana). ZEAXANTHIN EPOXIDASE (ZEP) was the major contributor to carotenoid composition, with mutants lacking ZEP activity showing a remarkable 6-fold increase in total seed carotenoids relative to the wild type. Natural variation in ZEP gene expression during seed development was identified as the underlying mechanism for fine-tuning carotenoid composition, stability, and ultimately content in Arabidopsis seed. We previously showed that two CAROTENOID CLEAVAGE DIOXYGENASE enzymes, CCD1 and CCD4, are the primary mediators of seed carotenoid degradation, and here we demonstrate that ZEP acts as an upstream control point of carotenoid homeostasis, with ZEP-mediated epoxidation targeting carotenoids for degradation by CCD enzymes. Finally, four of the nine loci/enzymatic activities identified as underlying natural variation in Arabidopsis seed carotenoids also were identified in a recent GWAS of maize (Zea mays) kernel carotenoid variation. This first comparison of the natural variation in seed carotenoids in monocots and dicots suggests a surprising overlap in the genetic architecture of these traits between the two lineages and provides a list of likely candidates to target for selecting seed carotenoid variation in other species.
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.G.-J., P.M., M.M.-L., R.A., D.D.P.);Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA United Kingdom (S.G.-J., P.M.);Department of Crop Sciences, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois, Urbana-Champaign, Illinois 61801 (A.E.L.);Division of Biological Sciences, University of Missouri, Columbia, Missouri 65201 (R.A.); andPlant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (M.A.G.).
authors.forename: Sabrina
authors.identifier: 0000-0002-0783-1929
authors.initials: S
authors.lastname: Gonzalez-Jorge
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.G.-J., P.M., M.M.-L., R.A., D.D.P.);Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA United Kingdom (S.G.-J., P.M.);Department of Crop Sciences, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois, Urbana-Champaign, Illinois 61801 (A.E.L.);Division of Biological Sciences, University of Missouri, Columbia, Missouri 65201 (R.A.); andPlant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (M.A.G.).
authors.forename: Payam
authors.identifier: 0000-0002-7192-0942
authors.initials: P
authors.lastname: Mehrshahi
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.G.-J., P.M., M.M.-L., R.A., D.D.P.);Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA United Kingdom (S.G.-J., P.M.);Department of Crop Sciences, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois, Urbana-Champaign, Illinois 61801 (A.E.L.);Division of Biological Sciences, University of Missouri, Columbia, Missouri 65201 (R.A.); andPlant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (M.A.G.).
authors.forename: Maria
authors.initials: M
authors.lastname: Magallanes-Lundback
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.G.-J., P.M., M.M.-L., R.A., D.D.P.);Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA United Kingdom (S.G.-J., P.M.);Department of Crop Sciences, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois, Urbana-Champaign, Illinois 61801 (A.E.L.);Division of Biological Sciences, University of Missouri, Columbia, Missouri 65201 (R.A.); andPlant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (M.A.G.).
authors.forename: Alexander E
authors.initials: AE
authors.lastname: Lipka
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.G.-J., P.M., M.M.-L., R.A., D.D.P.);Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA United Kingdom (S.G.-J., P.M.);Department of Crop Sciences, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois, Urbana-Champaign, Illinois 61801 (A.E.L.);Division of Biological Sciences, University of Missouri, Columbia, Missouri 65201 (R.A.); andPlant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (M.A.G.).
authors.forename: Ruthie
authors.initials: R
authors.lastname: Angelovici
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.G.-J., P.M., M.M.-L., R.A., D.D.P.);Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA United Kingdom (S.G.-J., P.M.);Department of Crop Sciences, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois, Urbana-Champaign, Illinois 61801 (A.E.L.);Division of Biological Sciences, University of Missouri, Columbia, Missouri 65201 (R.A.); andPlant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (M.A.G.).
authors.forename: Michael A
authors.identifier: 0000-0001-6896-8024
authors.initials: MA
authors.lastname: Gore
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (S.G.-J., P.M., M.M.-L., R.A., D.D.P.);Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA United Kingdom (S.G.-J., P.M.);Department of Crop Sciences, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois, Urbana-Champaign, Illinois 61801 (A.E.L.);Division of Biological Sciences, University of Missouri, Columbia, Missouri 65201 (R.A.); andPlant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (M.A.G.) dellapen@msu.edu.
authors.forename: Dean
authors.initials: D
authors.lastname: DellaPenna
mesh_terms: D017360:Arabidopsis / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002338:Carotenoids / Q000235:genetics / Q000378:metabolism*; D049308:Dioxygenases / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D055106:Genome-Wide Association Study; D006239:Haplotypes; D009154:Mutation; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism*; D040641:Quantitative Trait Loci; D012639:Seeds / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D024341:Xanthophylls / Q000235:genetics / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D024341:Xanthophylls; D002338:Carotenoids; C000592331:CCD4 protein, Arabidopsis; D010088:Oxidoreductases; C097153:zeaxanthin epoxidase; D049308:Dioxygenases