Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues

Abstract Background Anthocyanins are the primary source of colour in flowers and also accumulate in vegetative tissues, where they have multiple protective roles traditionally attributed to early compounds of the metabolic pathway (flavonols, flavones, etc.). Petal-specific loss of anthocyanins in p...

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Main Authors: José Carlos Del Valle, Cristina Alcalde-Eon, Mª. Teresa Escribano-Bailón, Mª. Luisa Buide, Justen B. Whittall, Eduardo Narbona
Format: Article
Language:English
Published: BMC 2019-11-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-019-2082-6
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author José Carlos Del Valle
Cristina Alcalde-Eon
Mª. Teresa Escribano-Bailón
Mª. Luisa Buide
Justen B. Whittall
Eduardo Narbona
author_facet José Carlos Del Valle
Cristina Alcalde-Eon
Mª. Teresa Escribano-Bailón
Mª. Luisa Buide
Justen B. Whittall
Eduardo Narbona
author_sort José Carlos Del Valle
collection DOAJ
description Abstract Background Anthocyanins are the primary source of colour in flowers and also accumulate in vegetative tissues, where they have multiple protective roles traditionally attributed to early compounds of the metabolic pathway (flavonols, flavones, etc.). Petal-specific loss of anthocyanins in petals allows plants to escape from the negative pleiotropic effects of flavonoid and anthocyanins loss in vegetative organs, where they perform a plethora of essential functions. Herein, we investigate the degree of pleiotropy at the biochemical scale in a pink-white flower colour polymorphism in the shore campion, Silene littorea. We report the frequencies of pink and white individuals across 21 populations and underlying biochemical profiles of three flower colour variants: anthocyanins present in all tissues (pink petals), petal-specific loss of anthocyanins (white petals), and loss of anthocyanins in all tissues (white petals). Results Individuals lacking anthocyanins only in petals represent a stable polymorphism in two populations at the northern edge of the species range (mean frequency 8–21%). Whereas, individuals lacking anthocyanins in the whole plant were found across the species range, yet always at very low frequencies (< 1%). Biochemically, the flavonoids detected were anthocyanins and flavones; in pigmented individuals, concentrations of flavones were 14–56× higher than anthocyanins across tissues with differences of > 100× detected in leaves. Loss of anthocyanin pigmentation, either in petals or in the whole plant, does not influence the ability of these phenotypes to synthesize flavones, and this pattern was congruent among all sampled populations. Conclusions We found that all colour variants showed similar flavone profiles, either in petals or in the whole plant, and only the flower colour variant with anthocyanins in photosynthetic tissues persists as a stable flower colour polymorphism. These findings suggest that anthocyanins in photosynthetic tissues, not flavonoid intermediates, are the targets of non-pollinator mediated selection.
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spelling doaj.art-b80049a250ac4a87a8948b7d8d90fc012022-12-21T19:51:32ZengBMCBMC Plant Biology1471-22292019-11-0119111310.1186/s12870-019-2082-6Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissuesJosé Carlos Del Valle0Cristina Alcalde-Eon1Mª. Teresa Escribano-Bailón2Mª. Luisa Buide3Justen B. Whittall4Eduardo Narbona5Department of Molecular Biology and Biochemical Engineering, Pablo de Olavide UniversityGrupo de Investigación en Polifenoles (GIP), University of SalamancaGrupo de Investigación en Polifenoles (GIP), University of SalamancaDepartment of Molecular Biology and Biochemical Engineering, Pablo de Olavide UniversityDepartment of Biology, Santa Clara UniversityDepartment of Molecular Biology and Biochemical Engineering, Pablo de Olavide UniversityAbstract Background Anthocyanins are the primary source of colour in flowers and also accumulate in vegetative tissues, where they have multiple protective roles traditionally attributed to early compounds of the metabolic pathway (flavonols, flavones, etc.). Petal-specific loss of anthocyanins in petals allows plants to escape from the negative pleiotropic effects of flavonoid and anthocyanins loss in vegetative organs, where they perform a plethora of essential functions. Herein, we investigate the degree of pleiotropy at the biochemical scale in a pink-white flower colour polymorphism in the shore campion, Silene littorea. We report the frequencies of pink and white individuals across 21 populations and underlying biochemical profiles of three flower colour variants: anthocyanins present in all tissues (pink petals), petal-specific loss of anthocyanins (white petals), and loss of anthocyanins in all tissues (white petals). Results Individuals lacking anthocyanins only in petals represent a stable polymorphism in two populations at the northern edge of the species range (mean frequency 8–21%). Whereas, individuals lacking anthocyanins in the whole plant were found across the species range, yet always at very low frequencies (< 1%). Biochemically, the flavonoids detected were anthocyanins and flavones; in pigmented individuals, concentrations of flavones were 14–56× higher than anthocyanins across tissues with differences of > 100× detected in leaves. Loss of anthocyanin pigmentation, either in petals or in the whole plant, does not influence the ability of these phenotypes to synthesize flavones, and this pattern was congruent among all sampled populations. Conclusions We found that all colour variants showed similar flavone profiles, either in petals or in the whole plant, and only the flower colour variant with anthocyanins in photosynthetic tissues persists as a stable flower colour polymorphism. These findings suggest that anthocyanins in photosynthetic tissues, not flavonoid intermediates, are the targets of non-pollinator mediated selection.http://link.springer.com/article/10.1186/s12870-019-2082-6AnthocyaninsFlavonoidsFlower color polymorphismLoss of pigmentationNon-pollinator mediated selectionPlant secondary metabolites
spellingShingle José Carlos Del Valle
Cristina Alcalde-Eon
Mª. Teresa Escribano-Bailón
Mª. Luisa Buide
Justen B. Whittall
Eduardo Narbona
Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues
BMC Plant Biology
Anthocyanins
Flavonoids
Flower color polymorphism
Loss of pigmentation
Non-pollinator mediated selection
Plant secondary metabolites
title Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues
title_full Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues
title_fullStr Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues
title_full_unstemmed Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues
title_short Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues
title_sort stability of petal color polymorphism the significance of anthocyanin accumulation in photosynthetic tissues
topic Anthocyanins
Flavonoids
Flower color polymorphism
Loss of pigmentation
Non-pollinator mediated selection
Plant secondary metabolites
url http://link.springer.com/article/10.1186/s12870-019-2082-6
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