Abstract
Main conclusion
The codon usage bias in chloroplast genes of Oryza species was low and AT rich. The pattern of codon usage was different among Oryza species and mainly influenced by mutation pressure and natural selection.
Abstract
Codon usage bias (CUB) is the unequal usage of synonymous codons in which some codons are more preferred to others in the coding sequences of genes. It shows a species-specific property. We studied the patterns of codon usage and the factors that influenced the CUB of protein-coding chloroplast (cp) genes in 18 Oryza species as no work was yet reported. The nucleotide composition analysis revealed that the overall GC content of cp genes in different species of Oryza was lower than 50%, i.e., Oryza cp genes were AT rich. Synonymous codon usage order (SCUO) suggested that CUB was weak in the cp genes of different Oryza species. A highly significant correlation was observed between overall nucleotides and its constituents at the third codon position suggesting that both, mutation pressure and natural selection, might influence the CUB. Correspondence analysis (COA) revealed that codon usage pattern differed across Oryza species. In the neutrality plot, a narrow range of GC3 distribution was recorded and some points were diagonally distributed in all the plots, suggesting that natural selection and mutation pressure might have influenced the CUB. The slope of the regression line was < 0.5, augmenting our inference that natural selection might have played a major role, while mutation pressure had a minor role in sha** the CUB of cp genes. The magnitudes of mutation pressure and natural selection on cp genes varied across Oryza species.
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Abbreviations
- COA:
-
Correspondence analysis
- cp:
-
Chloroplast
- CUB:
-
Codon usage bias
- MILC:
-
Measure independent of length and composition
- PR2:
-
Parity rule 2
- RSCU:
-
Relative synonymous codon usage
- SCUO:
-
Synonymous codon usage order
References
Angellotti MC, Bhuiyan SB, Chen G, Wan X-F (2007) CodonO: codon usage bias analysis within and across genomes. Nucleic Acids Res 35(Suppl_2):W132–W136
Baker A, Leaver CJ (1985) Isolation and sequence analysis of a cDNA encoding the ATP/ADP translocator of Zea mays L. Nucleic Acids Res 13(16):5857–5867
Bhattacharyya D, Uddin A, Das S, Chakraborty S (2019) Mutation pressure and natural selection on codon usage in chloroplast genes of two species in Pisum L. (Fabaceae: Faboideae). Mitochondrial DNA Part A 30(4):664–673
Brugler MR, France SC (2008) The mitochondrial genome of a deep-sea bamboo coral (Cnidaria, Anthozoa, Octocorallia, Isididae): genome structure and putative origins of replication are not conserved among octocorals. J Mol Evol 67(2):125
Bungard RA (2004) Photosynthetic evolution in parasitic plants: insight from the chloroplast genome. BioEssays 26(3):235–247
Butt AM, Nasrullah I, Qamar R, Tong Y (2016) Evolution of codon usage in Zika virus genomes is host and vector specific. Emerg Microbes Infec 5(1):1–14
Butt AM, Nasrullah I, Tong Y (2014) Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS ONE 9(3):e90905
Chrispeels MJ, Sadava DE (2003) Plants, genes, and crop biotechnology. Jones & Bartlett Publishers, Massachusetts
Das S, Paul S, Dutta C (2006) Synonymous codon usage in adenoviruses: influence of mutation, selection and protein hydropathy. Virus Res 117(2):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. doi: 10.1080/24701394.2018.1472772
Dos Reis M, Wernisch L, Savva R (2003) Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome. Nucleic Acids Res 31(23):6976–6985
Edelman GM, Gally JA (2001) Degeneracy and complexity in biological systems. Proc Natl Acad Sci USA 98(24):13763–13768
Frank A, Lobry J (1999) Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene 238(1):65–77
Galtier N, Lobry J (1997) Relationships between genomic G+ C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol 44(6):632–636
Garcia-Vallvé S, Romeu A, Palau J (2000) Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res 10(11):1719–1725
Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10(22):7055–7074
Grantham R, Perrin P, Mouchiroud D (1986) Patterns in codon usage of different kinds of species. Oxford Surv Evol Biol 3:48–81
Hatfield GW, Roth DA (2007) Optimizing scaleup yield for protein production: computationally optimized DNA assembly (CODA) and translation engineering™. Biotechnol Annu Rev 13:27–42
He B, Dong H, Jiang C, Cao F, Tao S, Xu L-a (2016) Analysis of codon usage patterns in Ginkgo biloba reveals codon usage tendency from A/U-ending to G/C-ending. Sci Rep 6:35927
Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ et al (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406(6795):477–483
Hershberg R, Petrov DA (2008) Selection on codon bias. Annu Rev Genetics 42:287–299
Howe N, Strauss W (2003) Millennials go to college: Strategies for a new generation on campus: recruiting and admissions, campus life, and the classroom. American Association of Collegiate Registrars and Admissions Officers, Washington
Hsiao Y-Y, Lin C-H, Liu J-K, Wong T-Y, Kuo J (2010) Analysis of codon usage patterns in toxic dinoflagellate Alexandrium tamarense through expressed sequence tag data. Comp Funct Genomics 2010:138538. https://doi.org/10.1155/2010/138538
James FC, McCulloch CE (1990) Multivariate analysis in ecology and systematics: panacea or Pandora’s box? Annu Rev Ecol Syst 21(1):129–166
Jensen PE, Leister D (2014) Chloroplast evolution, structure and functions. F1000prime Reports 6:40. https://doi.org/10.12703/P6-40
Jia J, Xue Q (2009) Codon usage biases of transposable elements and host nuclear genes in Arabidopsis thaliana and Oryza sativa. Genomics Proteomics Bioinf 7(4):175–184
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(1):356
Kawabe A, Miyashita NT (2003) Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genetic Syst 78(5):343–352
Kelley PM, Tolan DR (1986) The complete amino acid sequence for the anaerobically induced aldolase from maize derived from cDNA clones. Plant Physiol 82(4):1076–1080
Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60:115–138
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinf 5(2):150–163
Leffler EM, Bullaughey K, Matute DR, Meyer WK, Segurel L, Venkat A, Andolfatto P, Przeworski M (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10(9):e1001388
Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11(12):2453–2465
Liu H, He R, Zhang H, Huang Y, Tian M, Zhang J (2010) Analysis of synonymous codon usage in Zea mays. Mol Biol Rep 37(2):677
Liu Q, Xue Q (2005) Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. J Genetics 84(1):55–62
Maclean J (ed) (2013) GRiSP Rice Almanac: source book for one of the most important economic activities on earth, vol 4. IRRI, Los Banos, Philippines
Murray EE, Lotzer J, Eberle M (1989) Codon usage in plant genes. Nucleic Acids Res 17(2):477–498
Nie X, Deng P, Feng K, Liu P, Du X, You FM, Weining S (2014) Comparative analysis of codon usage patterns in chloroplast genomes of the Asteraceae family. Plant Mol Biol Rep 32(4):828–840
Paul P, Malakar AK, Chakraborty S (2018) Codon usage and amino acid usage influence genes expression level. Genetica 146(1):53–63
Prat S, Cortadas J, Puigdomènech P, Palau J (1985) Nucleic acid (cDNA) and amino acid sequences of the maize endosperm protein glutelin-2. Nucleic Acids Res 13(5):1493–1504
Sablok G, Nayak KC, Vazquez F, Tatarinova TV (2011) Synonymous codon usage, GC3, and evolutionary patterns across plastomes of three pooid model species: emerging grass genome models for monocots. Mol Biotechnol 49(2):116–128
Sanchez PL, Wing RA, Brar DS (2013) The wild relative of rice: genomes and genomics. In: Zhang Q, Wing RA (eds) Genetics and genomics of rice. Springer, New York, pp 9–25
Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE (2005) Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res 33(4):1141–1153
Sharp PM, Emery LR, Zeng K (2010) Forces that influence the evolution of codon bias. Philos T R Soc B 365(1544):1203–1212
Sharp PM, Li W-H (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24(1–2):28–38
Sharp PM, Li W-H (1987) The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15(3):1281–1295
Shields DC, Sharp PM, Higgins DG, Wright F (1988) “Silent” sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 5(6):704–716
Sueoka N (1995) Intrastrand parity rules of DNA base composition and usage biases of synonymous codons. JMol Evol 40(3):318–325
Sueoka N (1999) Two aspects of DNA base composition: G+ C content and translation-coupled deviation from intra-strand rule of A= T and G= C. J Mol Evol 49(1):49–62
Supek F, Vlahoviček K (2005) Comparison of codon usage measures and their applicability in prediction of microbial gene expressivity. BMC Bioinf 6(1):182
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526
Tamura M, Tao R, Sugiura A (1992) Highly stable regeneration from long-term cultures of Japanese persimmon callus. Hort Sci 27(9):1048–1048
Tatarinova TV, Alexandrov NN, Bouck JB, Feldmann KA (2010) GC 3 biology in corn, rice, sorghum and other grasses. BMC Genomics 11(1):308
Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, Zaborske J, Pan T, Dahan O, Furman I, Pilpel Y (2010) An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141(2):344–354
Vaughan DA (1994) The wild relatives of rice: a genetic resources handbook. IRRI, Los Banos
Wan X-F, Xu D, Kleinhofs A, Zhou J (2004) Quantitative relationship between synonymous codon usage bias and GC composition across unicellular genomes. BMC Evol Biol 4(1):19
Wan X, Xu D, Zhou J (2003) A new informatics method for measuring synonymous codon usage bias. In: Dagli CH, et al. (eds) Intelligent engineering systems through artificial neural networks, vol 13. ASME Press., New York, pp 1101–1018
Wang B, Yuan J, Liu J, ** L, Chen JQ (2011) Codon usage bias and determining forces in green plant mitochondrial genomes. J Integr Plant Biol 53(4):324–334
Wei L, He J, Jia X, Qi Q, Liang Z, Zheng H, ** Y, Liu S, Sun J (2014) Analysis of codon usage bias of mitochondrial genome in Bombyx mori and its relation to evolution. BMC Evol Biol 14(1):262
Williams E, Place A, Bachvaroff T (2017) Transcriptome analysis of core dinoflagellates reveals a universal bias towards “GC” rich codons. Marine Drugs 15(5):125
Williams KC, Page RA, Petrosky AR (2014) Green sustainability and new social media. J Strategic Innov Sustain 9:11–33
Wright F, Bibb MJ (1992) Codon usage in the G+ C-rich Streptomyces genome. Gene 113:55–65
Yadav MK, Swati D (2012) Comparative genome analysis of six malarial parasites using codon usage bias based tools. Bioinformation 8(24):1230–1239
Zhang L, Yong G, Ling L, Yue-** W, Zhi-Min D, Shou-Hong S, Li-Juan Q (2011) Analysis of nuclear gene codon bias on soybean genome and transcriptome. Acta Agron Sinica 37(6):965–974
Zhang WJ, Zhou J, Li ZF, Wang L, Gu X, Zhong Y (2007) Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L. J Integr Plant Biol 49(2):246–254
Zhang Y, Nie X, Jia X, Zhao C, Biradar SS, Wang L, Du X, Weining S (2012) Analysis of codon usage patterns of the chloroplast genomes in the Poaceae family. Austr J Bot 60(5):461–470
Zhang Z, Dai W, Dai D (2013a) Synonymous codon usage in TTSuV2: analysis and comparison with TTSuV1. PLoS ONE 8(11):e81469
Zhang Z, Dai W, Wang Y, Lu C, Fan H (2013b) Analysis of synonymous codon usage patterns in torque teno sus virus 1 (TTSuV1). Arch Virol 158(1):145–154
Zhao Y, Zheng H, Xu A, Yan D, Jiang Z, Qi Q, Sun J (2016) Analysis of codon usage bias of envelope glycoprotein genes in nuclear polyhedrosis virus (NPV) and its relation to evolution. BMC Genomics 17(1):677
Zhou J-h, Ding Y-z, He Y, Chu Y-f, Zhao P, Ma L-y, Wang X-j, Li X-r, Liu Y-s (2014) The effect of multiple evolutionary selections on synonymous codon usage of genes in the Mycoplasma bovis genome. PLoS ONE 9(10):e108949
Zhou M, Li X (2009) Analysis of synonymous codon usage patterns in different plant mitochondrial genomes. Mol Biol Rep 36(8):2039–2046
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The authors are thankful to Assam University, Silchar, India for providing the necessary facilities. The work was not funded by any agency.
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Chakraborty, S., Yengkhom, S. & Uddin, A. Analysis of codon usage bias of chloroplast genes in Oryza species. Planta 252, 67 (2020). https://doi.org/10.1007/s00425-020-03470-7
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DOI: https://doi.org/10.1007/s00425-020-03470-7