Novel insight into anthocyanin metabolism and molecular characterization of its key regulators in Camellia sasanqua

Abstract

Flower color is a trait that affects the ornamental value of a plant. Camellia sasanqua is a horticultural plant with rich flower color, but little is known about the regulatory mechanism of color diversity in this plant. Here, the anthocyanin profile of 20 C. sasanqua cultivars revealed and quantified 11 anthocyanin derivatives (five delphinidin-based and six cyanidin-based anthocyanins) for the first time. Cyanidin-3-O-(6-O-(E)-p-coumaroyl)-glucoside was the main contributor to flower base color, and the accumulation of cyanidin and delphinidin derivatives differed in the petals. To further explore the molecular mechanism of color divergence, a transcriptome analysis was performed using C. sasanqua cultivars ‘YingYueYe’, ‘WanXia’, ‘XueYueHua’, and’XiaoMeiGui’. The co-expression network related to differences in delphinidin and cyanidin derivatives accumulation was identified. Eleven candidate genes encoding key enzymes (e.g., F3H, F3′H, and ANS) were involved in anthocyanin biosynthesis. Moreover, 27 transcription factors were screened as regulators of the two types of accumulating anthocyanins. The association was suggested by correlation analysis between the expression levels of the candidate genes and the different camellia cultivars. We concluded that cyanidin and delphinidin derivatives are the major drivers of color diversity in C. sasanqua. This finding provides valuable resources for the study of flower color in C. sasanqua and lays a foundation for genetic modification of anthocyanin biosynthesis.

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Plant Molecular Biology (2023) 111:249–262
https://doi.org/10.1007/s11103-022-01324-2
Novel insight intoanthocyanin metabolism andmolecular
characterization ofits key regulators inCamellia sasanqua
MenglongFan1· XinLeiLi1 · YingZhang1· MeiyingYang1· SiWu1· HengFuYin1· WeiXinLiu1· ZhengQiFan1·
JiYuanLi1
Received: 24 April 2022 / Accepted: 28 October 2022 / Published online: 13 November 2022
© The Author(s), under exclusive licence to Springer Nature B.V. 2022
Abstract
Flower color is a trait that affects the ornamental value of a plant. Camellia sasanqua is a horticultural plant with rich flower
color, but little is known about the regulatory mechanism of color diversity in this plant. Here, the anthocyanin profile of
20 C. sasanqua cultivars revealed and quantified 11 anthocyanin derivatives (five delphinidin-based and six cyanidin-based
anthocyanins) for the first time. Cyanidin-3-O-(6-O-(E)-p-coumaroyl)-glucoside was the main contributor to flower base
color, and the accumulation of cyanidin and delphinidin derivatives differed in the petals. To further explore the molecular
mechanism of color divergence, a transcriptome analysis was performed using C. sasanqua cultivars ‘YingYueYe’, ‘WanXia’,
‘XueYueHua’, and’XiaoMeiGui’. The co-expression network related to differences in delphinidin and cyanidin derivatives
accumulation was identified. Eleven candidate genes encoding key enzymes (e.g., F3H, F3′H, and ANS) were involved in
anthocyanin biosynthesis. Moreover, 27 transcription factors were screened as regulators of the two types of accumulating
anthocyanins. The association was suggested by correlation analysis between the expression levels of the candidate genes
and the different camellia cultivars. We concluded that cyanidin and delphinidin derivatives are the major drivers of color
diversity in C. sasanqua. This finding provides valuable resources for the study of flower color in C. sasanqua and lays a
foundation for genetic modification of anthocyanin biosynthesis.
Keywords Camellia sasanqua· Flower color· Delphinidin· Coexpression· Transcriptome
Introduction
The diversity of flower color contributes to the ornamen-
tal value of horticultural plants and regulates plant repro-
duction by attracting pollinators (Martins etal. 2021). The
evolution of flower color is consistent with the evolution
of color vision in pollinator (Rausher 2006), resulting in
a limited number of flower colors in wild species. Flower
color is primarily controlled by pigment compounds (e.g.,
anthocyanins, betalains, and carotenoids) (Xue etal. 2016).
Anthocyanins are flavonoids, and contribute to colors rang-
ing from orange to blue (Xue etal. 2016). A series of stud-
ies have revealed the roles of anthocyanins in determining
color in plants. For example, cyanidin-based anthocyanins
are responsible for the red color of Paeonia suffruticosa
(Zhao etal. 2016), Salvia miltiorrhiza (Jiang etal. 2020),
and Camellia japonica (Fu etal. 2021), while delphinidin-
based anthocyanins are responsible blue and violet flower
colors (Yoshida etal. 2009). In addition, the proportions of
the anthocyanins regulate flower color. For example, the blu-
ish petals of chrysanthemums are achieved by increasing the
proportion of delphinidin (Brugliera etal. 2013). Therefore,
identifying pigments is vital for the development of novel
flower color varieties, and identifying species containing
delphinidin is of particular interest.
The anthocyanin synthetic pathway and some associ-
ated structural genes have been reported, including PAL,
CHS, CHI, DFR, F3H, and UFGT (Fan etal. 2022). F3′H
catalyzes naringenin to produce dihydroquercetin, result-
ing in the red phenotype, and F3′5′H catalyzes naringenin
to produce pentahydroxyflavone. Subsequently, delphi-
nidin is produced, resulting in blue petals (Noda etal.
2013). F3′H and F3′5′H are cytochrome P450 family pro-
teins (Tanaka and Brugliera. 2013). F3′5′H in Asteraceae
* XinLei Li
lixinlei2020@163.com
1 State Key Laboratory ofTree Genetics andBreeding,
Research Institute ofSubtropical Forestry, Chinese Academy
ofForestry, Hangzhou311400, Zhejiang, China
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