Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (12): 2771-2785    DOI: 10.1016/S2095-3119(19)62716-4
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Deciphering codon usage patterns and evolutionary forces in chloroplast genes of Camellia sinensis var. assamica and Camellia sinensis var. sinensis in comparison to Camellia pubicosta
Sophiarani Yengkhom1, Arif Uddin2, Supriyo Chakraborty
1 Department of Biotechnology, Assam University, Silchar 788011, Assam, India
2 Department of Zoology, Moinul Hoque Choudhury Memorial Science College, Algapur, Hailakandi 788150, Assam, India
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  
Codon usage bias (CUB) is a unique property of genome which refers to non-random usage of synonymous codons in coding sequences.  The present study makes an attempt to find out the pattern of CUB in chloroplast (cp) genes among three tea species, i.e., Camellia sinensis var. assamica (Assam tea), Camellia sinensis var. sinensis (Chinese tea) and Camellia pubicosta (wild tea species) as no work on CUB was reported earlier.  To understand the patterns of codon usage among the cp genes of three tea groups, we used bioinformatic tools to investigate the protein coding sequences of cp genes.  In our present study, the mean nucleobase T was the highest whereas C was the lowest in all the three tea groups.  The overall AT content was more than GC content, i.e., genes were AT rich.  The scaled chi-square (SCS) value indicated that the CUB of cp genes was low.  The codon CGT (Arg) was over-represented in C. sinensis var. sinensis whereas GGA (Pro) was over-represented in C. pubicosta species.  Heatmap study revealed that most of the GC ending codons showed positive correlations between codon usage and GC3 while AT ending codons exhibited negative correlations.  From neutrality plot analysis, it was evident that natural selection had played a major role, while mutation pressure exerted a minor effect in the CUB of cp genes in three tea groups.  Highly significant (P<0.01) positive correlation was found between SCS and synonymous codon usage order (SCUO) of cp genes which suggested that high expression of cp genes was associated with high degree of CUB.
Keywords:  Camellia sinensis var. assamica       Camellia sinensis var. sinensis       Camellia pubicosta        chloroplast genes       codon usage bias       mutation        natural selection  
Received: 14 January 2019   Accepted:
Corresponding Authors:  Correspondence Supriyo Chakraborty, E-mail: supriyoch_2008@rediffmail.com   

Cite this article: 

Sophiarani Yengkhom, Arif Uddin, Supriyo Chakraborty. 2019. Deciphering codon usage patterns and evolutionary forces in chloroplast genes of Camellia sinensis var. assamica and Camellia sinensis var. sinensis in comparison to Camellia pubicosta. Journal of Integrative Agriculture, 18(12): 2771-2785.

Akashi H. 2003. Translational selection and yeast proteome evolution. Genetics, 164, 1291–1303.
Behura S K, Severson D W. 2012. Comparative analysis of codon usage bias and codon context patterns between dipteran and hymenopteran sequenced genomes. PLoS ONE, 7, e43111.
Butt A M, Nasrullah I, Tong Y. 2014. Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS ONE, 9, e90905.
Chamary J, Hurst L D. 2005. Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biology, 6, R75.
Chen H, Sun S, Norenburg J L, Sundberg P. 2014. Mutation and selection cause codon usage and bias in mitochondrial genomes of ribbon worms (Nemertea). PLoS ONE, 9, e85631.
Choudhury M, Uddin A, Chakraborty S. 2017. Nucleotide composition and codon usage bias of SRY gene. Andrologia, 50, https://doi.org/10.1111/and.12787
Clement Y, Fustier M A, Nabholz B, Glemin S. 2014. The bimodal distribution of genic GC content is ancestral to monocot species. Genome Biology and Evolution, 7, 336–348.
Das S, Paul S, Dutta C. 2006. Synonymous codon usage in adenoviruses: Influence of mutation, selection and protein hydropathy. Virus Research, 117, 227–236.
Das S, Uddin A, Bhattacharyya D, Chakraborty S. 2018. Transcript free energy positively correlates with codon usage bias in mitochondrial genes of Calypogeia species (Calypogeiaceae, Marchantiophyta). Mitochondrial DNA (Part A), 30, 201–213.
Dillon M M, Sung W, Lynch M, Cooper V S. 2015. The rate and molecular spectrum of spontaneous mutations in the GC-rich multi-chromosome genome of Burkholderia cenocepacia. Genetics, 200, 935–946.
Duret L, Galtier N. 2009. Biased gene conversion and the evolution of mammalian genomic landscapes. Annual Review of Genomics and Human Genetics, 10, 285–311.
Dutta P, Reddy S, Borthakur B. 2013. Effect of neem kernal aqueous extract (NKAE) in Tea Mosquito Bug, Helopeltis theivora (Waterhouse, 1886) (Heteroptera: Miridae). Munis Entomology & Zoology, 8, 213–218.
Frank A, Lobry J. 1999. Asymmetric substitution patterns: A review of possible underlying mutational or selective mechanisms. Gene, 238, 65–77.
Galtier N, Lobry J. 1997. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. Journal of Molecular Evolution, 44, 632–636.
Gossmann T I, Song B H, Windsor A J, Mitchell-Olds T, Dixon C J, Kapralov M V, Filatov D A, Eyre-Walker A. 2010. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Molecular Biology and Evolution, 27, 1822–1832.
James F C, McCulloch C E. 1990. Multivariate analysis in ecology and systematics: Panacea or Pandora’s box? Annual Review of Ecology and Systematics, 21, 129–166.
Jia X, Liu S, Zheng H, Li B, Qi Q, Wei L, Zhao T, He J, Sun J. 2015. Non-uniqueness of factors constraint on the codon usage in Bombyx mori. BMC Genomics, 16, 356.
Kawabe A, Miyashita N T. 2003. Patterns of codon usage bias in three dicot and four monocot plant species. Genes & Genetic Systems, 78, 343–352.
Kimchi-Sarfaty C, Oh J M, Kim I W, Sauna Z E, Calcagno A M, Ambudkar S V, Gottesman M M. 2007. A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science, 315, 525–528.
Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers O P, Leer R, Tarchini R, Peters S A, Sandbrink H M, Fiers M W. 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proceedings of the National Academy of Sciences of the United States of America, 100, 1990–1995.
Leffler E M, Bullaughey K, Matute D R, Meyer W K, Segurel L, Venkat A, Andolfatto P, Przeworski M. 2012. Revisiting an old riddle: What determines genetic diversity levels within species? PLoS Biology, 10, e1001388.
Li W H, Wu C I, Luo C C. 1985. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Molecular Biology and Evolution, 2, 150–174.
Li X, Song H, Kuang Y, Chen S, Tian P, Li C, Nan Z. 2016. Genome-wide analysis of codon usage bias in Epichloe festucae. International Journal of Molecular Sciences, 17, 1138.
Liu Q. 2012. Mutational bias and translational selection shaping the codon usage pattern of tissue-specific genes in rice. PLoS ONE, 7, e48295.
Liu Q, Hu H, Wang H. 2015. Mutational bias is the driving force for shaping the synonymous codon usage pattern of alternatively spliced genes in rice (Oryza sativa L.). Molecular Genetics and Genomics, 290, 649–660.
Liu Q, Xue Q. 2005. Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. Journal of Genetics, 84, 55–62.
Mazumdar P, Binti Othman R, Mebus K, Ramakrishnan N, Ann Harikrishna J. 2017. Codon usage and codon pair patterns in non-grass monocot genomes. Annals of Botany, 120, 893–909.
Mazumder T H, Chakraborty S. 2015. Gaining insights into the codon usage patterns of TP53 gene across eight mammalian species. PLoS ONE, 10, e0121709.
Mooers A Ø, Holmes E C. 2000. The evolution of base composition and phylogenetic inference. Trends in Ecology & Evolution, 15, 365–369.
Morton B R. 1999. Strand asymmetry and codon usage bias in the chloroplast genome of Euglena gracilis. Proceedings of the National Academy of Sciences of the United States of America, 96, 5123–5128.
Morton B R. 2003. The role of context-dependent mutations in generating compositional and codon usage bias in grass chloroplast DNA. Journal of Molecular Evolution, 56, 616–629.
Mugal C F, Arndt P F, Holm L, Ellegren H. 2015. Evolutionary consequences of DNA methylation on the GC content in vertebrate genomes. G3 (Bethesda), 5, 441–447.
Mukhopadhyay P, Basak S, Ghosh T C. 2008. Differential selective constraints shaping codon usage pattern of housekeeping and tissue-specific homologous genes of rice and Arabidopsis. DNA Research, 15, 347–356.
Muyle A, Serres-Giardi L, Ressayre A, Escobar J, Glémin S. 2011. GC-biased gene conversion and selection affect GC content in the Oryza genus (rice). Molecular Biology and Evolution, 28, 2695–2706.
Nie X, Deng P, Feng K, Liu P, Du X, You F M, Weining S. 2014. Comparative analysis of codon usage patterns in chloroplast genomes of the Asteraceae family. Plant Molecular Biology Reporter, 32, 828–840.
Palmer J D. 1987. Chloroplast DNA evolution and biosystematic uses of chloroplast DNA variation. The American Naturalist, 130, S6–S29.
Plotkin J B, Kudla G. 2011. Synonymous but not the same: The causes and consequences of codon bias. Nature Reviews Genetics, 12, 32–42.
Raiford D W. 2005. Multivariate analysis of prokaryotic amino acid usage bias: A computational method for understanding protein building block selection in primitive organisms. MSc thesis, Wright State University, USA.
Roth A, Anisimova M, Cannarozzi G M. 2012. Measuring codon usage bias. In: Cannarozzi G M, Schneider A, eds. Codon Evolution: Mechanisms and Models. Oxford University Press Inc., New York. pp. 189–217.
Sablok G, Nayak K C, Vazquez F, Tatarinova T V. 2011. Synonymous codon usage, GC3, and evolutionary patterns across plastomes of three pooid model species: Emerging grass genome models for monocots. Molecular Biotechnology, 49, 116–128.
Shackelton L A, Parrish C R, Holmes E C. 2006. Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. Journal of Molecular Evolution, 62, 551–563.
Sharp P M, Li W H. 1986. An evolutionary perspective on synonymous codon usage in unicellular organisms. Journal of Molecular Evolution, 24, 28–38.
Sharp P M, Li W H. 1987. The codon adaptation index - A measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research, 15, 1281–1295.
Shields D C, Sharp P M, Higgins D G, Wright F. 1988. “Silent” sites in Drosophila genes are not neutral: Evidence of selection among synonymous codons. Molecular Biology and Evolution, 5, 704–716.
Singh R, Ming R, Yu Q. 2016. Comparative analysis of GC content variations in plant genomes. Tropical Plant Biology, 9, 136–149.
Spencer C. 2006. Human polymorphism around recombination hotspots. Biochemical Society Transactions, 34, 535–536.
Sueoka N. 1988. Directional mutation pressure and neutral molecular evolution. Proceedings of the National Academy of Sciences of the United States of America, 85, 2653–2657.
Sueoka N. 1995. Intrastrand parity rules of DNA base composition and usage biases of synonymous codons. Journal of Molecular Evolution, 40, 318–325.
Sugiura M. 1992. The chloroplast genome. Plant Molecular Biology, 19, 149–168.
Suzuki H, Morton B R. 2016. Codon adaptation of plastid genes. PLoS ONE, 11, e0154306.
Uddin A, Chakraborty S. 2015. Synonymous codon usage pattern in mitochondrial CYB gene in pisces, aves, and mammals. Mitochondrial DNA, 28, 187–196.
Uddin A, Chakraborty S. 2016. Codon usage trend in mitochondrial CYB gene. Gene, 586, 105–114.
Wachira F N, Waugh R, Powell W, Hackett C. 1995. Detection of genetic diversity in tea (Camellia sinensis) using RAPD markers. Genome, 38, 201–210.
Wan X, Xu D, Zhou J. 2003. A new informatics method for measuring synonymous codon usage bias. Intelligent Engineering Systems Through Artificial Neural Networks, 13, 1–8.
Wood-Mason J. 1884. Report on the Tea-mite and the Tea-bug of Assam. Taylor & Francis, UK.
Wright F. 1990. The ‘effective number of codons’ used in a gene. Gene, 87, 23–29.
Wright F, Bibb M J. 1992. Codon usage in the G+C-rich Streptomyces genome. Gene, 113, 55–65.
Zhang W J, Zhou J, Li Z F, Wang L, Gu X, Zhong Y. 2007. Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L. Journal of Integrative Plant Biology, 49, 246–254.
Zhang Y, Nie X, Jia X, Zhao C, Biradar S S, Wang L, Du X, Weining S. 2012. Analysis of codon usage patterns of the chloroplast genomes in the Poaceae family. Australian Journal of Botany, 60, 461–470.
Zhang Z, Dai W, Wang Y, Lu C, Fan H. 2013. Analysis of synonymous codon usage patterns in torque teno sus virus 1
(TTSuV1). Archives of Virology, 158, 145–154.
Zhou H, Wang H, Huang L, Naylor M, Clifford P. 2005. Heterogeneity in codon usages of sobemovirus genes. Archives of Virology, 150, 1591–1605.
Zhou M, Li X. 2009. Analysis of synonymous codon usage patterns in different plant mitochondrial genomes. Molecular Biology Reports, 36, 2039–2046.
Zhou T, Gu W, Ma J, Sun X, Lu Z. 2005. Analysis of synonymous codon usage in H5N1 virus and other influenza A viruses. Biosystems, 81, 77–86.
[1] WANG Yan, GUO Zhen-ru, CHEN Qing, LI Yang, ZHAO Kan, WAN Yong-fang, Malcolm J. HAWKESFORD, JIANG Yun-feng, KONG Li, PU Zhi-en, DENG Mei, JIANG Qian-tao, LAN Xiu-jin, WANG Ji-rui, CHEN Guo-yue, MA Jian, ZHENG You-liang, WEI Yu-ming, QI Peng-fei. Effect of high-molecular-weight glutenin subunit Dy10 on wheat dough properties and end-use quality[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1609-1617.
[2] ZHAO Yi-ran, ZHAO Yu-zhong, LIU Si-dang, XIAO Yi-hong, LI Ning, LIU Kui-hao, MENG Fan-liang, ZHAO Jun, LIU Meng-da, LI Bao-quan.

Phylogenetic and epidemiological characteristics of H9N2 avian influenza viruses in Shandong Province, China from 2019 to 2021 [J]. >Journal of Integrative Agriculture, 2023, 22(3): 881-896.

[3] HAN Rui-cai, LI Chen-yan, Adnan Rasheed, PAN Xiao-hua, SHI Qing-hua, WU Zi-ming. Reducing phosphorylation of nitrate reductase improves nitrate assimilation in rice[J]. >Journal of Integrative Agriculture, 2022, 21(1): 15-25.
[4] GUAN Hai-ying, DONG Yong-bin, LU Shou-ping, LIU Tie-shan, HE Chun-mei, LIU Chun-xiao, LIU Qiang, DONG Rui, WANG Juan, LI Yu-ling, QI Shi-jun, WANG Li-ming. Characterization and map-based cloning of miniature2-m1, a gene controlling kernel size in maize[J]. >Journal of Integrative Agriculture, 2020, 19(8): 1961-1973.
[5] ZOU Yun-long, LI Zhi-yuan, ZOU Yun-jing, HAO Hai-yang, HU Jia-xiang, LI Ning, LI Qiu-yan. Generation of pigs with a Belgian Blue mutation in MSTN using CRISPR/ Cpf1-assisted ssODN-mediated homologous recombination[J]. >Journal of Integrative Agriculture, 2019, 18(6): 1329-1336.
[6] GUO Liu-ming, HE Jing, LI Jing, CHEN Jian-ping, ZHANG Heng-mu. Chinese wheat mosaic virus: A long-term threat to wheat in China[J]. >Journal of Integrative Agriculture, 2019, 18(4): 821-829.
[7] LIU Hui, LIU Chang, ZHAO Yu-hang, HAN Xue-jie, ZHOU Zheng-wei, WANG Chen, LI Rong-feng, LI Xue-ling . Comparing successful gene knock-in efficiencies of CRISPR/Cas9 with ZFNs and TALENs gene editing systems in bovine and dairy goat fetal fibroblasts[J]. >Journal of Integrative Agriculture, 2018, 17(2): 406-414.
[8] WANG Jing-jing, LI Xiang-ju, LI Dan, HAN Yu-jiao, LI Zheng, YU Hui-lin, CUI Hai-lan. Non-target-site and target-site resistance to AHAS inhibitors in American sloughgrass (Beckmannia syzigachne)[J]. >Journal of Integrative Agriculture, 2018, 17(12): 2714-2723.
[9] SONG Hui, LIU Jing, CHEN Tao, NAN Zhi-biao. Synonymous codon usage pattern in model legume Medicago truncatula[J]. >Journal of Integrative Agriculture, 2018, 17(09): 2074-2081.
[10] HAN Yong-chao, ZENG Xiang-guo, XIANG Fa-yun, ZHANG Qing-hua, GUO Cong, CHEN Feng-ying, GU Yu-chen. Carbendazim sensitivity in populations of Colletotrichum gloeosporioides complex infecting strawberry and yams in Hubei Province of China[J]. >Journal of Integrative Agriculture, 2018, 17(06): 1391-1400.
[11] WU Yan-qing, LI Zhi-yuan, ZHAO Da-qiu, TAO Jun. Comparative analysis of flower-meristem-identity gene APETALA2 (AP2) codon in different plant species[J]. >Journal of Integrative Agriculture, 2018, 17(04): 867-877.
[12] HU Mao-long, PU Hui-ming, GAO Jian-qin, LONG Wei-hua, CHEN Feng, ZHOU Xiao-ying, ZHANG Wei, PENG Qi, CHEN Song, ZHANG Jie-fu. Inheritance and molecular characterization of resistance to AHAS-inhibiting herbicides in rapeseed[J]. >Journal of Integrative Agriculture, 2017, 16(11): 2421-2433.
[13] YUAN Guo-hui, GUO Wen-lei, DU Long, LIU Wei-tang, LI Qi, LI Ling-xu, WANG Jin-xin. Alleles contributing to acetyl coenzyme A carboxylase (ACCase) resistance in keng stiffgrass (Pseudosclerochloa kengiana) populations from China[J]. >Journal of Integrative Agriculture, 2017, 16(01): 125-134.
[14] DENG Wei, YANG Qian, JIAO Hong-tao, ZHANG Yong-zhi, LI Xue-feng, ZHENG Ming-qi. Cross-resistance pattern to four AHAS-inhibiting herbicides of tribenuron-methyl-resistant flixweed (Descurainia sophia) conferred by Asp-376-Glu mutation in AHAS[J]. >Journal of Integrative Agriculture, 2016, 15(11): 2563-2570.
[15] QIAN Li-li, MA De-zun, GAO Peng-fei, JIANG Sheng-wang, WANG Qing-qing, CAI Chun-bo, XIAO Gao-jun, AN Xiao-rong, CUI Wen-tao. Muscle hypertrophy in transgenic mice due to over-expression of porcine myostatin mutated at its cleavage site[J]. >Journal of Integrative Agriculture, 2016, 15(11): 2571-2577.
No Suggested Reading articles found!