Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in Theaceae
Abstract Background Theaceae, comprising 300 + species, holds significance in biodiversity, economics, and culture, notably including the globally consumed tea plant. Stewartia gemmata, a species of the earliest diverging tribe Stewartieae, is critical to offer insights into Theaceae's origin a...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-024-10016-8 |
| _version_ | 1797340276964982784 |
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| author | Daliang Liu Zhihan Zhang Yanlin Hao Mengge Li Houlin Yu Xingruo Zhang Haoyang Mi Lin Cheng Yiyong Zhao |
| author_facet | Daliang Liu Zhihan Zhang Yanlin Hao Mengge Li Houlin Yu Xingruo Zhang Haoyang Mi Lin Cheng Yiyong Zhao |
| author_sort | Daliang Liu |
| collection | DOAJ |
| description | Abstract Background Theaceae, comprising 300 + species, holds significance in biodiversity, economics, and culture, notably including the globally consumed tea plant. Stewartia gemmata, a species of the earliest diverging tribe Stewartieae, is critical to offer insights into Theaceae's origin and evolutionary history. Result We sequenced the complete organelle genomes of Stewartia gemmata using short/long reads sequencing technologies. The chloroplast genome (158,406 bp) exhibited a quadripartite structure including the large single-copy region (LSC), a small single-copy region (SSC), and a pair of inverted repeat regions (IRs); 114 genes encoded 80 proteins, 30 tRNAs, and four rRNAs. The mitochondrial genome (681,203 bp) exhibited alternative conformations alongside a monocyclic structure: 61 genes encoding 38 proteins, 20 tRNAs, three rRNAs, and RNA editing-impacting genes, including ATP6, RPL16, COX2, NAD4L, NAD5, NAD7, and RPS1. Comparative analyses revealed frequent recombination events and apparent rRNA gene gains and losses in the mitochondrial genome of Theaceae. In organelle genomes, the protein-coding genes exhibited a strong A/U bias at codon endings; ENC-GC3 analysis implies selection-driven codon bias. Transposable elements might facilitate interorganelle sequence transfer. Phylogenetic analysis confirmed Stewartieae's early divergence within Theaceae, shedding light on organelle genome characteristics and evolution in Theaceae. Conclusions We studied the detailed characterization of organelle genomes, including genome structure, composition, and repeated sequences, along with the identification of lateral gene transfer (LGT) events and complexities. The discovery of a large number of repetitive sequences and simple sequence repeats (SSRs) has led to new insights into molecular phylogenetic markers. Decoding the Stewartia gemmata organellar genome provides valuable genomic resources for further studies in tea plant phylogenomics and evolutionary biology. |
| first_indexed | 2024-03-08T10:00:39Z |
| format | Article |
| id | doaj.art-3c75d7f26cfa4c789f3ba65737a848da |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-08T10:00:39Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-3c75d7f26cfa4c789f3ba65737a848da2024-01-29T10:59:33ZengBMCBMC Genomics1471-21642024-01-0125111810.1186/s12864-024-10016-8Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in TheaceaeDaliang Liu0Zhihan Zhang1Yanlin Hao2Mengge Li3Houlin Yu4Xingruo Zhang5Haoyang Mi6Lin Cheng7Yiyong Zhao8Henan International Joint Laboratory of Tea-Oil Tree Biology and High-Value Utilization, College of Life Sciences, Xinyang Normal UniversityKey Laboratory of Functional Agriculture in Higher Education of Guizhou Province, College of Agriculture, Guizhou UniversityHenan International Joint Laboratory of Tea-Oil Tree Biology and High-Value Utilization, College of Life Sciences, Xinyang Normal UniversityHenan International Joint Laboratory of Tea-Oil Tree Biology and High-Value Utilization, College of Life Sciences, Xinyang Normal UniversityDepartment of Biochemistry and Molecular Biology, University of Massachusetts AmherstDepartment of Public Health Sciences, University of ChicagoDepartment of Biomedical Engineering, Johns Hopkins UniversityHenan International Joint Laboratory of Tea-Oil Tree Biology and High-Value Utilization, College of Life Sciences, Xinyang Normal UniversityKey Laboratory of Functional Agriculture in Higher Education of Guizhou Province, College of Agriculture, Guizhou UniversityAbstract Background Theaceae, comprising 300 + species, holds significance in biodiversity, economics, and culture, notably including the globally consumed tea plant. Stewartia gemmata, a species of the earliest diverging tribe Stewartieae, is critical to offer insights into Theaceae's origin and evolutionary history. Result We sequenced the complete organelle genomes of Stewartia gemmata using short/long reads sequencing technologies. The chloroplast genome (158,406 bp) exhibited a quadripartite structure including the large single-copy region (LSC), a small single-copy region (SSC), and a pair of inverted repeat regions (IRs); 114 genes encoded 80 proteins, 30 tRNAs, and four rRNAs. The mitochondrial genome (681,203 bp) exhibited alternative conformations alongside a monocyclic structure: 61 genes encoding 38 proteins, 20 tRNAs, three rRNAs, and RNA editing-impacting genes, including ATP6, RPL16, COX2, NAD4L, NAD5, NAD7, and RPS1. Comparative analyses revealed frequent recombination events and apparent rRNA gene gains and losses in the mitochondrial genome of Theaceae. In organelle genomes, the protein-coding genes exhibited a strong A/U bias at codon endings; ENC-GC3 analysis implies selection-driven codon bias. Transposable elements might facilitate interorganelle sequence transfer. Phylogenetic analysis confirmed Stewartieae's early divergence within Theaceae, shedding light on organelle genome characteristics and evolution in Theaceae. Conclusions We studied the detailed characterization of organelle genomes, including genome structure, composition, and repeated sequences, along with the identification of lateral gene transfer (LGT) events and complexities. The discovery of a large number of repetitive sequences and simple sequence repeats (SSRs) has led to new insights into molecular phylogenetic markers. Decoding the Stewartia gemmata organellar genome provides valuable genomic resources for further studies in tea plant phylogenomics and evolutionary biology.https://doi.org/10.1186/s12864-024-10016-8Stewartia gemmateMitochondrial genomeChloroplast genomePhylogenetics |
| spellingShingle | Daliang Liu Zhihan Zhang Yanlin Hao Mengge Li Houlin Yu Xingruo Zhang Haoyang Mi Lin Cheng Yiyong Zhao Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in Theaceae BMC Genomics Stewartia gemmate Mitochondrial genome Chloroplast genome Phylogenetics |
| title | Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in Theaceae |
| title_full | Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in Theaceae |
| title_fullStr | Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in Theaceae |
| title_full_unstemmed | Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in Theaceae |
| title_short | Decoding the complete organelle genomic architecture of Stewartia gemmata: an early-diverging species in Theaceae |
| title_sort | decoding the complete organelle genomic architecture of stewartia gemmata an early diverging species in theaceae |
| topic | Stewartia gemmate Mitochondrial genome Chloroplast genome Phylogenetics |
| url | https://doi.org/10.1186/s12864-024-10016-8 |
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