‘白毫早’叶绿体与线粒体基因组密码子偏好性分析

曾文娟, 刘珊, 文聪, 张其湘, 黄静, 龚意辉, 陈致印

茶叶科学 ›› 2025, Vol. 45 ›› Issue (4) : 587-603.

PDF(1630 KB)
PDF(1630 KB)
茶叶科学 ›› 2025, Vol. 45 ›› Issue (4) : 587-603. DOI: 10.13305/j.cnki.jts.2025.04.005
研究报告

‘白毫早’叶绿体与线粒体基因组密码子偏好性分析

  • 曾文娟1,2,3,4, 刘珊1,2,3,4, 文聪1,2,3,4, 张其湘1,2,3,4, 黄静5, 龚意辉1,2,3,4, 陈致印1,2,3,4,*
作者信息 +

Analysis of Codon Usage Bias in Chloroplast and Mitochondrial Genomes of Camellia sinensis cv. ‘Baihaozao’

  • ZENG Wenjuan1,2,3,4, LIU Shan1,2,3,4, WEN Cong1,2,3,4, ZHANG Qixiang1,2,3,4, HUANG Jing5, GONG Yihui1,2,3,4, CHEN Zhiyin1,2,3,4,*
Author information +
文章历史 +

摘要

密码子使用偏好性作为基因表达调控与分子进化的关键驱动机制,在植物细胞器基因组演化中具有重要生物学意义。以茶树品种‘白毫早’(Camellia sinensis cv. ‘Baihaozao’)为对象,系统解析其叶绿体(52个基因)与线粒体(29个基因)基因组的密码子使用模式及进化驱动力。结果表明:(1)叶绿体基因组平均有效密码子数(ENC=44.57±4.59)显著低于线粒体基因组(ENC=51.87±5.31),两者均呈现弱偏好性特征。中性分析揭示,叶绿体偏好性主要由自然选择主导(GC3s与ENC相关性R2=0.016),而线粒体则受自然选择与突变压力协同调控(R2=0.11),与双子叶植物细胞器基因组的进化约束差异规律一致。(2)相对同义密码子使用度(Relative synonymous codon usage,RSCU)分析表明,两类细胞器基因组均显著偏好以A/U结尾的同义密码子,其中叶绿体高表达基因(如ndhArps14)表现出更强的A/U末端偏好性,暗示翻译选择对高表达基因的优化作用。(3)通过多变量统计筛选,确定18个叶绿体最优密码子(GCA、GCU等)及18个线粒体最优密码子(GCA、AGA等),其中GCA在两类细胞器中均被优选,显示跨细胞器功能基因的适应性趋同。本研究阐明了‘白毫早’细胞器基因组密码子使用特征的异质性及其进化驱动力,为茶树分子育种中外源基因的适配性优化及跨细胞器表达调控网络的构建提供了理论依据。

Abstract

Codon usage bias serves as a critical driving mechanism in gene expression regulation and molecular evolution, holding significant biological importance in the evolution of organelle genomes in plants. This study focused on the economically important tea cultivar ‘Baihaozao’ (Camellia sinensis cv. ‘Baihaozao’) and systematically analyzed the codon usage patterns and evolutionary drivers of its chloroplast (52 genes) and mitochondrial (29 genes) genomes for the first time. The results indicate: (1) the average effective codon number (ENC=44.57±4.59) of the chloroplast genome is significantly lower than that of the mitochondrial genome (ENC=51.87±5.31), with both exhibiting weak preference characteristics. Neutrality analysis reveals that the chloroplast's preference is primarily driven by natural selection (correlation between GC3s and ENC, R2 =-0.016), whereas the mitochondrial genome is regulated by a combination of natural selection and mutational pressure (R² = -0.11), which is consistent with the evolutionary constraints observed in the organelle genomes of dicotyledons. (2) RSCU analysis shows that both types of organelle genomes significantly prefer synonymous codons ending in A/U, with high-expression chloroplast genes (e.g., ndhA, rps14) exhibiting a stronger preference for A/U terminal codons. This suggests that translational selection optimizes highly expressed genes. (3) Through multivariate statistical screening, 18 optimal codons were identified for the chloroplast genome (e.g., GCA, GCU) and 18 optimal codons for the mitochondrial genome (e.g., GCA, AGA). GCA was favored in both organelle types, reflecting the adaptive convergence of functional genes across organelles. This study elucidated the heterogeneity of codon usage characteristics in the organelle genomes of ‘Baihaozao’ and their evolutionary drivers for the first time, providing a theoretical basis for the adaptive optimization of exogenous genes and the construction of cross-organelle expression regulatory networks in molecular tea breeding.

关键词

白毫早 / 密码子使用偏好性 / 线粒体基因组 / 叶绿体基因组 / 最优密码子

Key words

Camellia sinensis cv. ‘Baihaozao’ / chloroplast genome / codon usage bias / mitochondrial genome / optimal codon

引用本文

导出引用
曾文娟, 刘珊, 文聪, 张其湘, 黄静, 龚意辉, 陈致印. ‘白毫早’叶绿体与线粒体基因组密码子偏好性分析[J]. 茶叶科学. 2025, 45(4): 587-603 https://doi.org/10.13305/j.cnki.jts.2025.04.005
ZENG Wenjuan, LIU Shan, WEN Cong, ZHANG Qixiang, HUANG Jing, GONG Yihui, CHEN Zhiyin. Analysis of Codon Usage Bias in Chloroplast and Mitochondrial Genomes of Camellia sinensis cv. ‘Baihaozao’[J]. Journal of Tea Science. 2025, 45(4): 587-603 https://doi.org/10.13305/j.cnki.jts.2025.04.005
中图分类号: S432.41    Q52   

参考文献

[1] Sharp P M, Li W H.The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications[J]. Nucleic Acids Research, 1987, 15(3): 1281-1296.
[2] 舒军霞, 杨林, 周涛, 等. 刺柏属4种药用植物叶绿体基因组密码子偏好性分析[J]. 中草药, 2022, 53(23): 7507-7516.
Shu J X, Yang L, Zhou T, et al.Analysis of codon bias in the chloroplast genome of four medicinal plants of Juniperus[J]. Chinese Traditional and Herbal Drugs, 2022, 53(23): 7507-7516.
[3] 杨国锋, 苏昆龙, 赵怡然, 等. 蒺藜苜蓿叶绿体密码子偏好性分析[J]. 草业学报, 2015, 24(12): 171-179.
Yang G F, Su K L, Zhao Y R, et al.Analysis of codon usage in the chloroplast genome of Medicago truncatula[J]. Acta Prataculturae Sinica, 2015, 24(12): 171-179.
[4] Chandan J, Gupta S, Babu V, et al.Comprehensive analysis of codon usage pattern in Withania somnifera and its associated pathogens: Meloidogyne incognita and Alternaria alternata[J]. Genetica, 2022, 150(2): 129-144.
[5] Chaudhary R, Chand S, Alam B K, et al.Codon usage bias for fatty acid genes FAE1 and FAD2 in oilseed brassica species[J]. Sustainability, 2022, 14(17): 11035. doi:10.3390/su141711035.
[6] Sueoka N.Directional mutation pressure and neutral molecular evolution[J]. PNAS, 1988, 85(8): 2653-2657.
[7] 早浩龙, 李奇, 黄珍华, 等. 人参和三七叶绿体基因组密码子偏好性比较分析[J/OL]. 分子植物育种, 2025: 1-17[2025-04-16]. https://link.cnki.net/urlid/46.1068.S.20240521.1131.005.
Zao H L, Li Q, Huang Z H, et al. Comparative analysis of codon usage bias in chloroplast genome between Panax ginseng and Panax notoginseng [J/OL]. Molecular Plant Breeding, 2025: 1-17[2025-04-16]. https://link.cnki.net/urlid/46.1068.S.20240521.1131.005.
[8] 杨秀玲, 许春梅, 耿晓珊, 等. 独脚金叶绿体基因组密码子偏好性分析[J]. 分子植物育种, 2023, 21(12): 3889-3897.
Yang X L, Xu C M, Geng X S, et al.Codon usage bias analysis of chloroplast genome in Striga asiatica[J]. Molecular Plant Breeding, 2023, 21(12): 3889-3897.
[9] Tyagi S, Kabade P G, Gnanapragasam N, et al.Codon usage provide insights into the adaptation of rice genes under stress condition[J]. International Journal of Molecular Sciences, 2023, 24(2): 1098. doi:10.3390/ijms24021098.
[10] Huang X, Xu J, Chen L, et al.Analysis of transcriptome data reveals multifactor constraint on codon usage in Taenia multiceps[J]. BMC Genomics, 2017, 18(1): 308. doi:10.1186/s12864-017-3704-8.
[11] Jamil Z, Uddin A, Alam S S M, et al. Analysis of the compositional features and codon usage pattern of genes involved in human autophagy[J]. Cells, 2022, 11(20): 3203. doi:10.3390/cells11203203.
[12] Deb B, Uddin A, Chakraborty S.Composition, codon usage pattern, protein properties, and influencing factors in the genomes of members of the family Anelloviridae[J]. Archives of Virology, 2021, 166(2): 461-474.
[13] Si F S, Jiang L, Yu R S, et al.Study on the characteristic codon usage pattern in porcine epidemic diarrhea virus genomes and its host adaptation phenotype[J]. Frontiers in Microbiology, 2021, 12: 738082. doi:10.3389/fmicb.2021.738082.
[14] Shi C, Hu N, Huang H, et al.An improved chloroplast DNA extraction procedure for whole plastid genome sequencing[J]. PLoS ONE, 2012, 7(2): e31468. doi:10.1371/journal.pone.0031468.
[15] Hao W J, Fan S H, Hua W, et al.Effective extraction and assembly methods for simultaneously obtaining plastid and mitochondrial genomes[J]. PLoS ONE, 2014, 9(9): e108291. doi:10.1371/journal.pone.0108291.
[16] Takamatsu T, Baslam M, Inomata T, et al.Optimized method of extracting rice chloroplast dna for high-quality plastome resequencing and de novo assembly[J]. Frontiers in Plant Science, 2018, 9: 266. doi:10.3389/fpls.2018.00266. eCollection 2018.
[17] Wang Y, Chen S J, Chen J J, et al.Characterization and phylogenetic analysis of the complete mitochondrial genome sequence of Photinia serratifolia[J]. Scientific Reports, 2023, 13: 770. doi:10.1038/s41598-022-24327-x.
[18] Cadorna C A E, Pahayo D G, Rey J D. The first mitochondrial genome of Calophyllum soulattri Burm.f.[J]. Scientific Reports, 2024, 14: 5112. doi:10.1038/s41598-024-55016-6.
[19] Twyford A D, Ness R W.Strategies for complete plastid genome sequencing[J]. Molecular Ecology Resources, 2017, 17: 858-868.
[20] 冯瑞云, 梅超, 王慧杰, 等. 籽粒苋叶绿体基因组密码子偏好性分析[J]. 中国草地学报, 2019, 41(4): 8-16.
Feng R Y, Mei C, Wang H J, et al.Analysis of codon usage in the chloroplast genome of grain Amaranth (Amaranthus hypochondriacus L.)[J]. Chinese Journal of Grassland, 2019, 41(4): 8-16.
[21] 刘慧, 王梦醒, 岳文杰, 等. 糜子叶绿体基因组密码子使用偏性的分析[J]. 植物科学学报, 2017, 35(3): 362-371.
Liu H, Wang M X, Yue W J, et al.Analysis of codon usage in the chloroplast genome of Broomcorn millet (Panicum miliaceum L.)[J]. Plant Science Joumal, 2017, 35(3): 362-371.
[22] 赵森, 邓力华, 陈芬. 秋茄叶绿体基因组密码子使用偏好性分析[J]. 森林与环境学报, 2020, 40(5): 534-541.
Zhao S, Deng L H, Chen F.Codon usage bias of chloroplast genome in Kandelia obovata[J]. Journal of Forest and Environment, 2020, 40(5): 534-541.
[23] 原晓龙, 康洪梅, 王毅. 云南蓝果树叶绿体基因组密码子偏好性分析[J]. 西北林学院学报, 2020, 35(4): 26-31.
Yuan X L, Kang H M, Wang Y.Codon usage bias analysis of chloroplast genome in Nyssa yunnanensis[J]. Journal of Northwest Forestry University, 2020, 35(4): 26-31.
[24] Hu Q, Wu J Q, Fan C C, et al.Comparative analysis of codon usage bias in the chloroplast genomes of eighteen Ampelopsideae species (Vitaceae)[J]. BMC Genomic Data, 2024, 25(1): 80. doi:10.1186/s12863-024-01260-8.
[25] 辛雅萱, 黎若竹, 李鑫, 等. 杧果叶绿体基因组密码子使用偏好性分析[J]. 中南林业科技大学学报, 2021, 41(9): 148-156, 165.
Xin Y X, Li R Z, Li X, et al.Analysis on codon usage bias of chloroplast genome in Mangifera indica[J]. Journal of Central South University of Forestry & Technology, 2021, 41(9): 148-156, 165.
[26] 梁湘兰, 郭松. 苦马豆叶绿体基因组密码子偏好性分析[J]. 西北林学院学报, 2022, 37(2): 121-126.
Liang X L, Guo S.Codon usage bias in the chloroplast genome of Sphaerophysa salsula[J]. Journal of Northwest Forestry University, 2022, 37(2): 121-126.
[27] 吴学俊, 梁湘兰, 易子群, 等. 湖北山楂叶绿体基因组密码子偏好性分析[J]. 分子植物育种, 2023, 21(8): 2508-2516.
Wu X J, Liang X L, Yi Z Q, et al.Analysis of codon bias in the chloroplast genome of Crataegus hupehensis Sarg. (Rosaceae)[J]. Molecular Plant Breeding, 2023, 21(8): 2508-2516.
[28] Shen L W, Chen S Q, Liang M, et al.Comparative analysis of codon usage bias in chloroplast genomes of ten medicinal species of Rutaceae[J]. BMC Plant Biology, 2024, 24(1): 424. doi:10.1186/s12870-024-04999-5.
[29] Wu P, Xiao W Q, Luo Y Y, et al.Comprehensive analysis of codon bias in 13 Ganoderma mitochondrial genomes[J]. Frontiers in Microbiology, 2023, 14: 1170790. doi:10.3389/fmicb.2023.1170790. eCollection 2023.
[30] Wei L, He J, Jia X, et al.Analysis of codon usage bias of mitochondrial genome in Bombyx mori and its relation to evolution[J]. BMC Evolutionary Biology, 2014, 14: 262. doi:10.1186/s12862-014-0262-4.
[31] Gao W, Chen X D, He J, et al.Intraspecific and interspecific variations in the synonymous codon usage in mitochondrial genomes of 8 pleurotus strains[J]. BMC Genomics, 2024, 25(1): 456. doi:10.1186/s12864-024-10374-3.
[32] 丁锐, 胡兵, 宗小雁, 等. 杓兰叶绿体基因组密码子偏好性分析[J]. 林业科学研究, 2021, 34(5): 177-185.
Ding R, Hu B, Zong X Y, et al.Analysis of codon usage in the chloroplast genome of Cypripedium calceolus[J]. Forest Research, 2021, 34(5): 177-185.
[33] 赖瑞联, 陈瑾, 冯新, 等. 橄榄叶绿体基因组密码子偏好性特征[J]. 福建农林大学学报(自然科学版), 2022, 51(4): 502-510.
Lai R L, Chen J, Feng X, et al.Codon usage preference of chloroplast genome of Canarium album[J]. Journal of Fujian Agriculture and Forestry University (Natural Science Edition), 2022, 51(4): 502-510.
[34] 陆奇丰, 骆文华, 黄至欢. 两种梧桐叶绿体基因组密码子使用偏性分析[J]. 广西植物, 2020, 40(2): 173-183.
Lu Q F, Luo W H, Huang Z H.Codon usage bias of chloroplast genome from two species of Firmiana Marsili[J]. Guihaia, 2020, 40(2): 173-183.
[35] 王鹏良, 吴双成, 杨利平, 等. 巨桉叶绿体基因组密码子偏好性分析[J]. 广西植物, 2019, 39(12): 1583-1592.
Wang P L, Wu S C, Yang L P, et al.Analysis of codon bias of chloroplast genome in Eucalyptus grandis[J]. Guihaia, 2019, 39(12): 1583-1592.
[36] 王媛媛, 杨美青. 蒙古韭叶绿体基因组密码子使用偏好性分析[J]. 分子植物育种, 2021, 19(4): 1084-1092.
Wang Y Y, Yang M Q.Analysis of the codon usage bias in the chloroplast genome of allium Mongolicum regel[J]. Molecular Plant Breeding, 2021, 19(4): 1084-1092.
[37] 林新茂, 黄家权. 仙人掌科叶绿体与核基因组密码子偏好性分析[J]. 分子植物育种, 2024, 22(22): 7400-7412.
Lin X M, Huang J Q.Codon preference analysis of the chloroplast and nuclear genomes in Cactaceae[J]. Molecular Plant Breeding, 2024, 22(22): 7400-7412.
[38] Sharp P M, Touhy T M F, Mosurski K R. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes[J]. Nucleic Acids Research, 1986, 14(13): 5125-5143.
[39] Antezana M A, King Jordan I.Highly conserved regimes of neighbor-base-dependent mutation generated the background primary-structural heterogeneities along vertebrate chromosomes[J]. PLoS ONE, 2008, 3(5): e2145. doi:10.1371/journal.pone.0002145.
[40] 辛雅萱, 董章宏, 瞿绍宏, 等. 杜梨叶绿体基因组密码子偏好性分析[J]. 河北农业大学学报, 2020, 43(6): 51-60.
Xin Y X, Dong Z H, Qu S H, et al.Analysis on codon usage bias of chloroplast genome in Pyrus betulifolia Bge.[J]. Journal of Hebei Agricultural University, 2020, 43(6): 51-60.
[41] Shen Z N, Gan Z M, Zhang F, et al.Analysis of codon usage patterns in citrus based on coding sequence data[J]. BMC Genomics, 2020, 21(s5): 234. doi:10.1186/s12864-020-6641-x.
[42] 原晓龙, 郝佳波, 王毅, 等. 铁核桃叶绿体基因组密码子偏好性分析[J]. 分子植物育种, 2020, 18(20): 6671-6677.
Yuan X L, Hao J B, Wang Y, et al.Codon usage bias analysis of chloroplast genome in Juglans sigillata[J]. Molecular Plant Breeding, 2020, 18(20): 6671-6677.
[43] Hershberg R, Petrov D A.Codon adaptation of plastid genes[J]. Annual Review of Genetics, 2008, 42: 287-299.
[44] Yin D B, Mu Y T, Li X, et al.Comparison of the complete chloroplast genomes in the Astragalus[J]. Legume Research, 2024, 47(3): 420-427.
[45] 刘庆坡, 薛庆中. 粳稻叶绿体基因组的密码子用法[J]. 作物学报, 2004, 30(12): 1220-1224.
Liu Q P, Xue Q Z.Codon usage in the chloroplast genome of rice (Oryza sativa L.ssp.japonica)[J]. Acta Agronomica Sinica, 2004, 30(12): 1220-1224.
[46] 王婧, 王天翼, 王罗云, 等. 沙枣叶绿体全基因组序列及其使用密码子偏性分析[J]. 西北植物学报, 2019, 39(9): 1559-1572.
Wang J, Wang T Y, Wang L Y, et al.Assembling and analysis of the whole chloroplast genome sequence of Elaeagnus angustifolia and its codon usage bias[J]. Acta Botanica Boreali-Occidentalia Sinica, 2019, 39(9): 1559-1572.
[47] 杨祥燕, 蔡元保, 谭秦亮, 等. 菠萝叶绿体基因组密码子偏好性分析[J]. 热带作物学报, 2022, 43(3): 439-446.
Yang X Y, Cai Y B, Tan Q L, et al.Analysis of codon usage bias in the chloroplast genome of Ananas comosus[J]. Chinese Journal of Tropical Crops, 2022, 43(3): 439-446.
[48] 何亚玲, 彭业军, 李锦, 等. 天山雪莲叶绿体基因组密码子偏好性分析[J]. 石河子大学学报(自然科学版), 2022, 40(1): 84-93.
He Y L, Peng Y J, Li J, et al.Preference analysis of codon usage in the chloroplast genome of Saussurea involucrate[J]. Journal of Shihezi University (Natural Science), 2022, 40(1): 84-93.
[49] 郭媛婷, 张敏, 杨玉洁, 等. 翅果油树叶绿体基因组密码子偏好性分析[J]. 山西农业科学, 2023, 51(3): 233-240.
Guo Y T, Zhang M, Yang Y J, et al.Analysis on codon usage bias in chloroplast genome of Elaeagnus mollis[J]. Journal of Shanxi Agricultural Sciences, 2023, 51(3): 233-240.
[50] 冯展, 江媛, 郑燕, 等. 肉苁蓉属植物叶绿体基因组密码子偏好性分析[J]. 中草药, 2023, 54(5): 1540-1551.
Feng Z, Jiang Y, Zheng Y, et al.Codon use bias analysis of chloroplast genome of Cistanche[J]. Chinese Traditional and Herbal Drugs, 2023, 54(5): 1540-1551.
[51] 张文娟. 基于密码子水平的生物信息学分析及进化研究[D]. 上海: 复旦大学, 2006.
Zhang W J.Codon analysis and its application in bioinformatics and evolutionary studies [D]. Shanghai: Fudan University, 2006.
[52] 尹明华, 张嘉欣, 乐芸, 等. 茶树大面白叶绿体基因组特征、密码子偏好性及其系统发育分析[J]. 茶叶科学, 2024, 44(3): 411-430.
Yin M H, Zhang J X, Le Y, et al.Genomic characteristics, codon preference, and phylogenetic analysis of chloroplasts of Camellia sinensis cv. ‘Damianbai’[J]. Journal of Tea Science, 2024, 44(3): 411-430.
[53] Sun M Y, Zhang J Z. Preferred synonymous codons are translated more accurately: proteomic evidence, among-species variation,mechanistic basis [J]. Science Advances, 2022, 8(27): eabl9812. doi:10.1126/sciadv.abl9812
[54] 佟岩, 黄荟, 王雨华. 森林茶园古茶树大理茶叶绿体基因组密码子偏好性及系统发育研究[J]. 茶叶科学, 2023, 43(3): 297-309.
Tong Y, Huang H, Wang Y H.Analysis of codon usage bias and phylogenesis in the chloroplast genome of ancient tea tree Camellia taliensis in forest-tea garden[J]. Journal of Tea Science, 2023, 43(3): 297-309.
[55] Wei C L, Yang H, Wang S B, et al.Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality[J]. PNAS, 2018, 115(18): E4151-E4158.
[56] Liang H, Qi H, Wang C, et al.Analysis of the complete mitogenomes of three high economic value tea plants (Tea-oil Camellia) provide insights into evolution and phylogeny relationship[J]. Frontiers in Plant Science, 2025, 16: 1549185. doi:10.3389/fpls.2025.1549185.

基金

湖南省自然科学基金(2023JJ50465)、湖南省科技创新计划项目(2024RC8289)、娄底市科技创新计划项目(2023RC3501)、国家级大学生创新训练项目(S202310553022)

PDF(1630 KB)

Accesses

Citation

Detail

段落导航
相关文章

/