Genomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in Camellia

Abstract Background The formation and domestication of ornamental traits are influenced by various aspects, such as the recognition of esthetic values and cultural traditions. Camellia japonica is widely appreciated and domesticated around the world mainly due to its rich variations in ornamental tr...

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Main Authors: Zhikang Hu, Zhengqi Fan, Sijia Li, Minyan Wang, Mingchuan Huang, Xianjin Ma, Weixin Liu, Yupeng Wang, Yifan Yu, Yaxuan Li, Yingkun Sun, Xinlei Li, Jiyuan Li, Hengfu Yin
Format: Article
Language:English
Published: BMC 2024-02-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-024-01851-y
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author Zhikang Hu
Zhengqi Fan
Sijia Li
Minyan Wang
Mingchuan Huang
Xianjin Ma
Weixin Liu
Yupeng Wang
Yifan Yu
Yaxuan Li
Yingkun Sun
Xinlei Li
Jiyuan Li
Hengfu Yin
author_facet Zhikang Hu
Zhengqi Fan
Sijia Li
Minyan Wang
Mingchuan Huang
Xianjin Ma
Weixin Liu
Yupeng Wang
Yifan Yu
Yaxuan Li
Yingkun Sun
Xinlei Li
Jiyuan Li
Hengfu Yin
author_sort Zhikang Hu
collection DOAJ
description Abstract Background The formation and domestication of ornamental traits are influenced by various aspects, such as the recognition of esthetic values and cultural traditions. Camellia japonica is widely appreciated and domesticated around the world mainly due to its rich variations in ornamental traits. Ornamental camellias have a diverse range of resources, including different bud variations from Camellia spp. as well as inter- and intra- specific hybridization. Despite research on the formation of ornamental traits, a basic understanding of their genetics and genomics is still lacking. Results Here, we report the chromosomal-level reference genome of C. japonica through combining multiple DNA-sequencing technologies and obtain a high-density genetic linkage map of 4255 markers by sequencing 98 interspecific F1 hybrids between C. japonica and C. chekiangoleosa. We identify two whole-genome duplication events in C. japonica: one is a shared ancient γ event, and the other is revealed to be specific to genus Camellia. Based on the micro-collinearity analysis, we find large-scale segmental duplication of chromosome 8, resulting to two copies of the AGAMOUS loci, which may play a key role in the domestication of floral shapes. To explore the regulatory mechanisms of seasonal flowering, we have analyzed year-round gene expression patterns of C. japonica and C. azalea—a sister plant of continuous flowering that has been widely used for cross breeding. Through comparative analyses of gene co-expression networks and annual gene expression patterns, we show that annual expression rhythms of some important regulators of seasonal growth and development, including GIGANTEA and CONSTANS of the photoperiod pathway, have been disrupted in C. azalea. Furthermore, we reveal that the distinctive expression patterns of FLOWERING LOCUS T can be correlated with the seasonal activities of flowering and flushing. We demonstrate that the regulatory module involved in GIGANTEA, CONSTANS, and FLOWERING LOCUS T is central to achieve seasonality. Conclusions Through the genomic and comparative genomics characterizations of ornamental Camellia spp., we propose that duplication of chromosomal segments as well as the establishment of gene expression patterns has played a key role in the formation of ornamental traits (e.g., flower shape, flowering time). This work provides a valuable genomic platform for understanding the molecular basis of ornamental traits.
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spelling doaj.art-be54d9be908b43cf93300d016bc91c572024-03-17T12:38:25ZengBMCBMC Biology1741-70072024-02-0122111610.1186/s12915-024-01851-yGenomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in CamelliaZhikang Hu0Zhengqi Fan1Sijia Li2Minyan Wang3Mingchuan Huang4Xianjin Ma5Weixin Liu6Yupeng Wang7Yifan Yu8Yaxuan Li9Yingkun Sun10Xinlei Li11Jiyuan Li12Hengfu Yin13State Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryCollege of Information Science and Technology, Nanjing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryCollege of Horticulture, Qingdao Agricultural UniversityState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryState Key Laboratory of Tree Genetics and Breeding, Research Institute of Subtropical Forestry, Chinese Academy of ForestryAbstract Background The formation and domestication of ornamental traits are influenced by various aspects, such as the recognition of esthetic values and cultural traditions. Camellia japonica is widely appreciated and domesticated around the world mainly due to its rich variations in ornamental traits. Ornamental camellias have a diverse range of resources, including different bud variations from Camellia spp. as well as inter- and intra- specific hybridization. Despite research on the formation of ornamental traits, a basic understanding of their genetics and genomics is still lacking. Results Here, we report the chromosomal-level reference genome of C. japonica through combining multiple DNA-sequencing technologies and obtain a high-density genetic linkage map of 4255 markers by sequencing 98 interspecific F1 hybrids between C. japonica and C. chekiangoleosa. We identify two whole-genome duplication events in C. japonica: one is a shared ancient γ event, and the other is revealed to be specific to genus Camellia. Based on the micro-collinearity analysis, we find large-scale segmental duplication of chromosome 8, resulting to two copies of the AGAMOUS loci, which may play a key role in the domestication of floral shapes. To explore the regulatory mechanisms of seasonal flowering, we have analyzed year-round gene expression patterns of C. japonica and C. azalea—a sister plant of continuous flowering that has been widely used for cross breeding. Through comparative analyses of gene co-expression networks and annual gene expression patterns, we show that annual expression rhythms of some important regulators of seasonal growth and development, including GIGANTEA and CONSTANS of the photoperiod pathway, have been disrupted in C. azalea. Furthermore, we reveal that the distinctive expression patterns of FLOWERING LOCUS T can be correlated with the seasonal activities of flowering and flushing. We demonstrate that the regulatory module involved in GIGANTEA, CONSTANS, and FLOWERING LOCUS T is central to achieve seasonality. Conclusions Through the genomic and comparative genomics characterizations of ornamental Camellia spp., we propose that duplication of chromosomal segments as well as the establishment of gene expression patterns has played a key role in the formation of ornamental traits (e.g., flower shape, flowering time). This work provides a valuable genomic platform for understanding the molecular basis of ornamental traits.https://doi.org/10.1186/s12915-024-01851-yCamellia japonicaGenomeOrnamental traitsAnnual gene expressionGenome duplication
spellingShingle Zhikang Hu
Zhengqi Fan
Sijia Li
Minyan Wang
Mingchuan Huang
Xianjin Ma
Weixin Liu
Yupeng Wang
Yifan Yu
Yaxuan Li
Yingkun Sun
Xinlei Li
Jiyuan Li
Hengfu Yin
Genomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in Camellia
BMC Biology
Camellia japonica
Genome
Ornamental traits
Annual gene expression
Genome duplication
title Genomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in Camellia
title_full Genomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in Camellia
title_fullStr Genomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in Camellia
title_full_unstemmed Genomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in Camellia
title_short Genomics insights into flowering and floral pattern formation: regional duplication and seasonal pattern of gene expression in Camellia
title_sort genomics insights into flowering and floral pattern formation regional duplication and seasonal pattern of gene expression in camellia
topic Camellia japonica
Genome
Ornamental traits
Annual gene expression
Genome duplication
url https://doi.org/10.1186/s12915-024-01851-y
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