Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensis
Anthocyanins are the primary pigments contributing to the variety of flower colors among angiosperms and are considered essential for survival and reproduction. Anthocyanins are members of the flavonoids, a broader class of secondary metabolites, of which there are numerous structural genes and regu...
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| Format: | Article |
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Frontiers Media S.A.
2021-02-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.633979/full |
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| author | Mercedes Sánchez-Cabrera Francisco Javier Jiménez-López Eduardo Narbona Montserrat Arista Pedro L. Ortiz Francisco J. Romero-Campero Francisco J. Romero-Campero Karolis Ramanauskas Boris Igić Amelia A. Fuller Justen B. Whittall |
| author_facet | Mercedes Sánchez-Cabrera Francisco Javier Jiménez-López Eduardo Narbona Montserrat Arista Pedro L. Ortiz Francisco J. Romero-Campero Francisco J. Romero-Campero Karolis Ramanauskas Boris Igić Amelia A. Fuller Justen B. Whittall |
| author_sort | Mercedes Sánchez-Cabrera |
| collection | DOAJ |
| description | Anthocyanins are the primary pigments contributing to the variety of flower colors among angiosperms and are considered essential for survival and reproduction. Anthocyanins are members of the flavonoids, a broader class of secondary metabolites, of which there are numerous structural genes and regulators thereof. In western European populations of Lysimachia arvensis, there are blue- and orange-petaled individuals. The proportion of blue-flowered plants increases with temperature and daylength yet decreases with precipitation. Here, we performed a transcriptome analysis to characterize the coding sequences of a large group of flavonoid biosynthetic genes, examine their expression and compare our results to flavonoid biochemical analysis for blue and orange petals. Among a set of 140 structural and regulatory genes broadly representing the flavonoid biosynthetic pathway, we found 39 genes with significant differential expression including some that have previously been reported to be involved in similar flower color transitions. In particular, F3′5′H and DFR, two genes at a critical branchpoint in the ABP for determining flower color, showed differential expression. The expression results were complemented by careful examination of the SNPs that differentiate the two color types for these two critical genes. The decreased expression of F3′5′H in orange petals and differential expression of two distinct copies of DFR, which also exhibit amino acid changes in the color-determining substrate specificity region, strongly correlate with the blue to orange transition. Our biochemical analysis was consistent with the transcriptome data indicating that the shift from blue to orange petals is caused by a change from primarily malvidin to largely pelargonidin forms of anthocyanins. Overall, we have identified several flavonoid biosynthetic pathway loci likely involved in the shift in flower color in L. arvensis and even more loci that may represent the complex network of genetic and physiological consequences of this flower color polymorphism. |
| first_indexed | 2024-12-24T01:44:36Z |
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| id | doaj.art-8fedb9c2f5184abc99d74665b4c61bca |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-24T01:44:36Z |
| publishDate | 2021-02-01 |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-8fedb9c2f5184abc99d74665b4c61bca2022-12-21T17:21:54ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-02-011210.3389/fpls.2021.633979633979Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensisMercedes Sánchez-Cabrera0Francisco Javier Jiménez-López1Eduardo Narbona2Montserrat Arista3Pedro L. Ortiz4Francisco J. Romero-Campero5Francisco J. Romero-Campero6Karolis Ramanauskas7Boris Igić8Amelia A. Fuller9Justen B. Whittall10Department of Plant Biology and Ecology, Faculty of Biology, University of Seville, Seville, SpainDepartment of Plant Biology and Ecology, Faculty of Biology, University of Seville, Seville, SpainDepartment of Molecular Biology and Biochemical Engineering, Pablo de Olavide University, Seville, SpainDepartment of Plant Biology and Ecology, Faculty of Biology, University of Seville, Seville, SpainDepartment of Plant Biology and Ecology, Faculty of Biology, University of Seville, Seville, SpainInstitute for Plant Biochemistry and Photosynthesis, University of Seville – Centro Superior de Investigación Científica, Seville, SpainDepartment of Computer Science and Artificial Intelligence, University of Seville, Seville, SpainDepartment of Biological Science, University of Illinois at Chicago, Chicago, IL, United StatesDepartment of Biological Science, University of Illinois at Chicago, Chicago, IL, United StatesDepartment of Chemistry and Biochemistry, Santa Clara University, Santa Clara, CA, United StatesDepartment of Biology, College of Arts and Sciences, Santa Clara University, Santa Clara, CA, United StatesAnthocyanins are the primary pigments contributing to the variety of flower colors among angiosperms and are considered essential for survival and reproduction. Anthocyanins are members of the flavonoids, a broader class of secondary metabolites, of which there are numerous structural genes and regulators thereof. In western European populations of Lysimachia arvensis, there are blue- and orange-petaled individuals. The proportion of blue-flowered plants increases with temperature and daylength yet decreases with precipitation. Here, we performed a transcriptome analysis to characterize the coding sequences of a large group of flavonoid biosynthetic genes, examine their expression and compare our results to flavonoid biochemical analysis for blue and orange petals. Among a set of 140 structural and regulatory genes broadly representing the flavonoid biosynthetic pathway, we found 39 genes with significant differential expression including some that have previously been reported to be involved in similar flower color transitions. In particular, F3′5′H and DFR, two genes at a critical branchpoint in the ABP for determining flower color, showed differential expression. The expression results were complemented by careful examination of the SNPs that differentiate the two color types for these two critical genes. The decreased expression of F3′5′H in orange petals and differential expression of two distinct copies of DFR, which also exhibit amino acid changes in the color-determining substrate specificity region, strongly correlate with the blue to orange transition. Our biochemical analysis was consistent with the transcriptome data indicating that the shift from blue to orange petals is caused by a change from primarily malvidin to largely pelargonidin forms of anthocyanins. Overall, we have identified several flavonoid biosynthetic pathway loci likely involved in the shift in flower color in L. arvensis and even more loci that may represent the complex network of genetic and physiological consequences of this flower color polymorphism.https://www.frontiersin.org/articles/10.3389/fpls.2021.633979/fullDFRF3′5′Hflavonoid biosynthetic pathwaymalvidinpelargonidinRNA-Seq |
| spellingShingle | Mercedes Sánchez-Cabrera Francisco Javier Jiménez-López Eduardo Narbona Montserrat Arista Pedro L. Ortiz Francisco J. Romero-Campero Francisco J. Romero-Campero Karolis Ramanauskas Boris Igić Amelia A. Fuller Justen B. Whittall Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensis Frontiers in Plant Science DFR F3′5′H flavonoid biosynthetic pathway malvidin pelargonidin RNA-Seq |
| title | Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensis |
| title_full | Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensis |
| title_fullStr | Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensis |
| title_full_unstemmed | Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensis |
| title_short | Changes at a Critical Branchpoint in the Anthocyanin Biosynthetic Pathway Underlie the Blue to Orange Flower Color Transition in Lysimachia arvensis |
| title_sort | changes at a critical branchpoint in the anthocyanin biosynthetic pathway underlie the blue to orange flower color transition in lysimachia arvensis |
| topic | DFR F3′5′H flavonoid biosynthetic pathway malvidin pelargonidin RNA-Seq |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.633979/full |
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