Cargando…

Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways

Changes in floral pigmentation can have dramatic effects on angiosperm evolution by making flowers either attractive or inconspicuous to different pollinator groups. Flower color largely depends on the type and abundance of pigments produced in the petals, but it is still unclear whether similar col...

Descripción completa

Detalles Bibliográficos
Autores principales: Ogutcen, Ezgi, Durand, Karine, Wolowski, Marina, Clavijo, Laura, Graham, Catherine, Glauser, Gaétan, Perret, Mathieu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7767864/
https://www.ncbi.nlm.nih.gov/pubmed/33381138
http://dx.doi.org/10.3389/fpls.2020.604389
_version_ 1783629055844679680
author Ogutcen, Ezgi
Durand, Karine
Wolowski, Marina
Clavijo, Laura
Graham, Catherine
Glauser, Gaétan
Perret, Mathieu
author_facet Ogutcen, Ezgi
Durand, Karine
Wolowski, Marina
Clavijo, Laura
Graham, Catherine
Glauser, Gaétan
Perret, Mathieu
author_sort Ogutcen, Ezgi
collection PubMed
description Changes in floral pigmentation can have dramatic effects on angiosperm evolution by making flowers either attractive or inconspicuous to different pollinator groups. Flower color largely depends on the type and abundance of pigments produced in the petals, but it is still unclear whether similar color signals rely on same biosynthetic pathways and to which extent the activation of certain pathways influences the course of floral color evolution. To address these questions, we investigated the physical and chemical aspects of floral color in the Neotropical Gesnerioideae (ca. 1,200 spp.), in which two types of anthocyanins, hydroxyanthocyanins, and deoxyanthocyanins, have been recorded as floral pigments. Using spectrophotometry, we measured flower reflectance for over 150 species representing different clades and pollination syndromes. We analyzed these reflectance data to estimate how the Gesnerioideae flowers are perceived by bees and hummingbirds using the visual system models of these pollinators. Floral anthocyanins were further identified using high performance liquid chromatography coupled to mass spectrometry. We found that orange/red floral colors in Gesnerioideae are produced either by deoxyanthocyanins (e.g., apigenidin, luteolinidin) or hydroxyanthocyanins (e.g., pelargonidin). The presence of deoxyanthocyanins in several lineages suggests that the activation of the deoxyanthocyanin pathway has evolved multiple times in the Gesnerioideae. The hydroxyanthocyanin-producing flowers span a wide range of colors, which enables them to be discriminated by hummingbirds or bees. By contrast, color diversity among the deoxyanthocyanin-producing species is lower and mainly represented at longer wavelengths, which is in line with the hue discrimination optima for hummingbirds. These results indicate that Gesnerioideae have evolved two different biochemical mechanisms to generate orange/red flowers, which is associated with hummingbird pollination. Our findings also suggest that the activation of the deoxyanthocyanin pathway has restricted flower color diversification to orange/red hues, supporting the potential constraining role of this alternative biosynthetic pathway on the evolutionary outcome of phenotypical and ecological diversification.
format Online
Article
Text
id pubmed-7767864
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-77678642020-12-29 Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways Ogutcen, Ezgi Durand, Karine Wolowski, Marina Clavijo, Laura Graham, Catherine Glauser, Gaétan Perret, Mathieu Front Plant Sci Plant Science Changes in floral pigmentation can have dramatic effects on angiosperm evolution by making flowers either attractive or inconspicuous to different pollinator groups. Flower color largely depends on the type and abundance of pigments produced in the petals, but it is still unclear whether similar color signals rely on same biosynthetic pathways and to which extent the activation of certain pathways influences the course of floral color evolution. To address these questions, we investigated the physical and chemical aspects of floral color in the Neotropical Gesnerioideae (ca. 1,200 spp.), in which two types of anthocyanins, hydroxyanthocyanins, and deoxyanthocyanins, have been recorded as floral pigments. Using spectrophotometry, we measured flower reflectance for over 150 species representing different clades and pollination syndromes. We analyzed these reflectance data to estimate how the Gesnerioideae flowers are perceived by bees and hummingbirds using the visual system models of these pollinators. Floral anthocyanins were further identified using high performance liquid chromatography coupled to mass spectrometry. We found that orange/red floral colors in Gesnerioideae are produced either by deoxyanthocyanins (e.g., apigenidin, luteolinidin) or hydroxyanthocyanins (e.g., pelargonidin). The presence of deoxyanthocyanins in several lineages suggests that the activation of the deoxyanthocyanin pathway has evolved multiple times in the Gesnerioideae. The hydroxyanthocyanin-producing flowers span a wide range of colors, which enables them to be discriminated by hummingbirds or bees. By contrast, color diversity among the deoxyanthocyanin-producing species is lower and mainly represented at longer wavelengths, which is in line with the hue discrimination optima for hummingbirds. These results indicate that Gesnerioideae have evolved two different biochemical mechanisms to generate orange/red flowers, which is associated with hummingbird pollination. Our findings also suggest that the activation of the deoxyanthocyanin pathway has restricted flower color diversification to orange/red hues, supporting the potential constraining role of this alternative biosynthetic pathway on the evolutionary outcome of phenotypical and ecological diversification. Frontiers Media S.A. 2020-12-14 /pmc/articles/PMC7767864/ /pubmed/33381138 http://dx.doi.org/10.3389/fpls.2020.604389 Text en Copyright © 2020 Ogutcen, Durand, Wolowski, Clavijo, Graham, Glauser and Perret. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Ogutcen, Ezgi
Durand, Karine
Wolowski, Marina
Clavijo, Laura
Graham, Catherine
Glauser, Gaétan
Perret, Mathieu
Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways
title Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways
title_full Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways
title_fullStr Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways
title_full_unstemmed Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways
title_short Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways
title_sort chemical basis of floral color signals in gesneriaceae: the effect of alternative anthocyanin pathways
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7767864/
https://www.ncbi.nlm.nih.gov/pubmed/33381138
http://dx.doi.org/10.3389/fpls.2020.604389
work_keys_str_mv AT ogutcenezgi chemicalbasisoffloralcolorsignalsingesneriaceaetheeffectofalternativeanthocyaninpathways
AT durandkarine chemicalbasisoffloralcolorsignalsingesneriaceaetheeffectofalternativeanthocyaninpathways
AT wolowskimarina chemicalbasisoffloralcolorsignalsingesneriaceaetheeffectofalternativeanthocyaninpathways
AT clavijolaura chemicalbasisoffloralcolorsignalsingesneriaceaetheeffectofalternativeanthocyaninpathways
AT grahamcatherine chemicalbasisoffloralcolorsignalsingesneriaceaetheeffectofalternativeanthocyaninpathways
AT glausergaetan chemicalbasisoffloralcolorsignalsingesneriaceaetheeffectofalternativeanthocyaninpathways
AT perretmathieu chemicalbasisoffloralcolorsignalsingesneriaceaetheeffectofalternativeanthocyaninpathways