Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>

The color of flowers in <i>Osmanthus fragrans</i> is regulated by carotenoid metabolism. The orange-red variety, Dangui, is believed to have evolved from the yellow variety, Jingui, through a natural bud mutation. This study uses the Jingui cultivar ‘Jinqiu Gui’ (JQG) and its bud mutatio...

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Main Authors: Xiangling Zeng, Yunfei Tan, Xin Wen, Qiang He, Hui Wu, Jingjing Zou, Jie Yang, Xuan Cai, Hongguo Chen
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Horticulturae
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Online Access:https://www.mdpi.com/2311-7524/11/7/864
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author Xiangling Zeng
Yunfei Tan
Xin Wen
Qiang He
Hui Wu
Jingjing Zou
Jie Yang
Xuan Cai
Hongguo Chen
author_facet Xiangling Zeng
Yunfei Tan
Xin Wen
Qiang He
Hui Wu
Jingjing Zou
Jie Yang
Xuan Cai
Hongguo Chen
author_sort Xiangling Zeng
collection DOAJ
description The color of flowers in <i>Osmanthus fragrans</i> is regulated by carotenoid metabolism. The orange-red variety, Dangui, is believed to have evolved from the yellow variety, Jingui, through a natural bud mutation. This study uses the Jingui cultivar ‘Jinqiu Gui’ (JQG) and its bud mutation cultivar ‘Huolian Jindan’ (HLJD) as materials, combining genome resequencing, ultrastructural observation, targeted metabolomics, and transcriptomic analysis to elucidate the molecular and cellular mechanisms underlying flower color variation. Phylogenetic analysis confirms that HLJD is a natural bud mutation of JQG. Ultrastructural observations reveal that during petal development, chromoplasts are transformed from proplastids. In HLJD petals, starch granules degrade more slowly and exhibit abnormal morphology, resulting in chromoplasts displaying crystalline, tubular, and fibrous composite structures, in contrast to the typical spherical plastoglobuli found in JQG. Targeted metabolomics identified 34 carotenoids, showing significant increases in the levels of ε-carotene, γ-carotene, α-carotene, and β-carotene in HLJD petals compared to JQG, with these levels continuing to accumulate throughout the flowering process, while the levels of the cleavage products α-ionone and β-ionone decrease. Transcriptomic analysis indicates that carotenoid metabolic pathway genes do not correlate directly with the phenotype; however, 49 candidate genes significantly associated with pigment accumulation were identified. Among these, the expression of genes such as glycoside hydrolases (LYG036752, etc.), sucrose synthase (LYG010191), and glucose-1-phosphate adenylyltransferase (LYG003610) are downregulated in HLJD. This study proposes for the first time the pathway of “starch degradation delay → chromoplast structural abnormalities → carotenoid cleavage inhibition” for deepening flower color, providing a new theoretical model for the metabolic regulation of carotenoids in non-photosynthetic tissues of plants. This research not only identifies key target genes (such as glycoside hydrolases) for the color breeding of <i>O. fragrans</i> but also establishes a theoretical foundation for the color enhancement of other ornamental plants.
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series Horticulturae
spelling doaj-art-3199afea79ec49fca0c8a41793d5fc5b2025-08-20T03:58:26ZengMDPI AGHorticulturae2311-75242025-07-0111786410.3390/horticulturae11070864Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>Xiangling Zeng0Yunfei Tan1Xin Wen2Qiang He3Hui Wu4Jingjing Zou5Jie Yang6Xuan Cai7Hongguo Chen8School of Pharmacy, Xianning Medical College, Hubei University of Science and Technology, Xianning 437100, ChinaSchool of Pharmacy, Xianning Medical College, Hubei University of Science and Technology, Xianning 437100, ChinaSchool of Pharmacy, Xianning Medical College, Hubei University of Science and Technology, Xianning 437100, ChinaPublic Inspection and Testing Center, Xianning 437100, ChinaPublic Inspection and Testing Center, Xianning 437100, ChinaNational Forestry and Grassland Administration Engineering Research Center for <i>Osmanthus fragrans</i>, Hubei University of Science and Technology, Xianning 437100, ChinaNational Forestry and Grassland Administration Engineering Research Center for <i>Osmanthus fragrans</i>, Hubei University of Science and Technology, Xianning 437100, ChinaNational Forestry and Grassland Administration Engineering Research Center for <i>Osmanthus fragrans</i>, Hubei University of Science and Technology, Xianning 437100, ChinaNational Forestry and Grassland Administration Engineering Research Center for <i>Osmanthus fragrans</i>, Hubei University of Science and Technology, Xianning 437100, ChinaThe color of flowers in <i>Osmanthus fragrans</i> is regulated by carotenoid metabolism. The orange-red variety, Dangui, is believed to have evolved from the yellow variety, Jingui, through a natural bud mutation. This study uses the Jingui cultivar ‘Jinqiu Gui’ (JQG) and its bud mutation cultivar ‘Huolian Jindan’ (HLJD) as materials, combining genome resequencing, ultrastructural observation, targeted metabolomics, and transcriptomic analysis to elucidate the molecular and cellular mechanisms underlying flower color variation. Phylogenetic analysis confirms that HLJD is a natural bud mutation of JQG. Ultrastructural observations reveal that during petal development, chromoplasts are transformed from proplastids. In HLJD petals, starch granules degrade more slowly and exhibit abnormal morphology, resulting in chromoplasts displaying crystalline, tubular, and fibrous composite structures, in contrast to the typical spherical plastoglobuli found in JQG. Targeted metabolomics identified 34 carotenoids, showing significant increases in the levels of ε-carotene, γ-carotene, α-carotene, and β-carotene in HLJD petals compared to JQG, with these levels continuing to accumulate throughout the flowering process, while the levels of the cleavage products α-ionone and β-ionone decrease. Transcriptomic analysis indicates that carotenoid metabolic pathway genes do not correlate directly with the phenotype; however, 49 candidate genes significantly associated with pigment accumulation were identified. Among these, the expression of genes such as glycoside hydrolases (LYG036752, etc.), sucrose synthase (LYG010191), and glucose-1-phosphate adenylyltransferase (LYG003610) are downregulated in HLJD. This study proposes for the first time the pathway of “starch degradation delay → chromoplast structural abnormalities → carotenoid cleavage inhibition” for deepening flower color, providing a new theoretical model for the metabolic regulation of carotenoids in non-photosynthetic tissues of plants. This research not only identifies key target genes (such as glycoside hydrolases) for the color breeding of <i>O. fragrans</i> but also establishes a theoretical foundation for the color enhancement of other ornamental plants.https://www.mdpi.com/2311-7524/11/7/864<i>Osmanthus fragrans</i>floral colorbud mutationpastidcarotenoidstarch
spellingShingle Xiangling Zeng
Yunfei Tan
Xin Wen
Qiang He
Hui Wu
Jingjing Zou
Jie Yang
Xuan Cai
Hongguo Chen
Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>
Horticulturae
<i>Osmanthus fragrans</i>
floral color
bud mutation
pastid
carotenoid
starch
title Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>
title_full Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>
title_fullStr Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>
title_full_unstemmed Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>
title_short Delayed Starch Degradation Triggers Chromoplast Structural Aberration to Inhibit Carotenoid Cleavage: A Novel Mechanism for Flower Color Deepening in <i>Osmanthus fragrans</i>
title_sort delayed starch degradation triggers chromoplast structural aberration to inhibit carotenoid cleavage a novel mechanism for flower color deepening in i osmanthus fragrans i
topic <i>Osmanthus fragrans</i>
floral color
bud mutation
pastid
carotenoid
starch
url https://www.mdpi.com/2311-7524/11/7/864
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