Please wait a minute...
Journal of Integrative Agriculture  2018, Vol. 17 Issue (09): 2074-2081    DOI: 10.1016/S2095-3119(18)61961-6
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
Synonymous codon usage pattern in model legume Medicago truncatula
SONG Hui1, 2, LIU Jing1, CHEN Tao1, NAN Zhi-biao1#br#  
1 State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, P.R.China
2 Grassland Agri-husbandry Research Center, Qingdao Agricultural University, Qingdao 266109, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  
Synonymous codon usage pattern presumably reflects gene expression optimization as a result of molecular evolution.  Though much attention has been paid to various model organisms ranging from prokaryotes to eukaryotes, codon usage has yet been extensively investigated for model legume Medicago truncatula.  In present study, 39 531 available coding sequences (CDSs) from M. truncatula were examined for codon usage bias (CUB).  Based on analyses including neutrality plots, effective number of codons plots, and correlations between optimal codons frequency and codon adaptation index, we conclude that natural selection is a major driving force in M. truncatula CUB.  We have identified 30 optimal codons encoding 18 amino acids based on relative synonymous codon usage.  These optimal codons characteristically end with A or T, except for AGG and TTG encoding arginine and leucine respectively.  Optimal codon usage is positively correlated with the GC content at three nucleotide positions of codons and the GC content of CDSs.  The abundance of expressed sequence tag is a proxy for gene expression intensity in the legume, but has no relatedness with either CDS length or GC content.  Collectively, we unravel the synonymous codon usage pattern in M. truncatula, which may serve as the valuable information on genetic engineering of the model legume and forage crop.
 
Keywords:  codon usage        gene expression        Medicago truncatula        natural selection        optimal codon  
Received: 05 September 2017   Accepted:
Fund: This study was supported by the National Basic Research Program of China (2014CB138702) and the National Natural Science Foundation of China (31502001).
Corresponding Authors:  Correspondence SONG Hui, E-mail: biosonghui@outlook.com; NAN Zhi-biao, E-mail: zhibiao@lzu.edu.cn   

Cite this article: 

SONG Hui, LIU Jing, CHEN Tao, NAN Zhi-biao. 2018. Synonymous codon usage pattern in model legume Medicago truncatula. Journal of Integrative Agriculture, 17(09): 2074-2081.

Agris P F, Vendeix F A P, Graham W D. 2007. tRNA’s wobble decoding of the genome: 40 years of modification. Journal of Molecular Biology, 366, 1–13.
Akashi H. 2001. Gene expression and molecular evolution. Current Opinion in Genetics and Development, 11, 660–666.
Altschul S, Madden T, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman D. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.
Camiolo S, Farina L, Porceddu A. 2012. The relation of codon bias to tissue-specific gene expression in Arabidopsis thaliana. Genetics, 192, 641–649.
Camiolo S, Melito S, Porceddu A. 2015. New insights into the interplay between codon bias determinants in plants. DNA Research, 22, 461–470.
Chaney J, Clark P L. 2015. Roles for synonymous codon usage in protein biogenesis. Annual Review of Biophysics, 44, 143–166.
Duret L. 2000. tRNA gene number and codon usage in the
C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends in Genetics, 16, 287–289.
Fennoy S L, Bailey-Serres J. 1993. Synonymous codon usage in Zea mays L. nuclear genes is varied by levels of C- and G-ending codons. Nucleic Acids Research, 21, 5294–5300.
Hershberg R, Petrov D A. 2008. Selection on codon bias. Annual Review of Genetics, 42, 287–299.
Hershberg R, Petrov D A. 2009. General rules for optimal codon choice. PLoS Genetics, 5, e1000556.
Ikemura T. 1985. Codon usage and tRNA content in unicellular and multicellular organisms. Molecular Biology and Evolution, 2, 13–34.
Ingvarsson P K. 2007. Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Molecular Biology and Evolution, 24, 836–844.
Ingvarsson P K. 2008. Molecular evolution of synonymous codon usage in Populus. BMC Evolutionary Biology, 8, 307.
Ingvarsson P K. 2010. Natural selection on synonymous and nonsynonymous mutations shaps patterns of polymorphism in Populus tremula. Molecular Biology and Evolution, 27, 650–660.
Kawabe A, Miyashita N T. 2003. Patterns of codon usage bias in three dicot and four monocot plant species. Genes and Genetic Systems, 78, 343–352.
Li X, Song H, Kuang Y, Chen S, Tian P, Li C, Nan Z. 2016. Genome-wide analysis of codon usage bias in Epichloë festucae. International Journal of Molecular Sciences, 17, E1138.
Liu Q, Feng Y, Zhao X, Dong H, Xue Q. 2004. Synonymous codon usage bias in Oryza sativa. Plant Science, 167, 101–105.
Liu Q, Hu H, Wang H. 2015. Mutational bias is the driving force for shaping the synonymous codon usage pattern of alternatively spliced in rice (Oryza sativa L.). Molecular Genetics and Genomics, 290, 649–660.
Morton B R, Wright S I. 2007. Selective constraints on codon usage of nuclear genes from Arabidopsis thaliana. Molecular Biology and Evolution, 24, 122–129.
Novoa E M, de Pouplana L R. 2012. Speeding with control: Codon usage, tRNAs, and ribosomes. Trends in Genetics, 28, 574–581.
Ohlrogge J, Benning C. 2000. Unraveling plant metabolism by EST analysis. Current Opinion in Plant Biology, 3, 224–228.
Ometto L, Li M, Bresadola L, Varotto C. 2012. Rates of evolution in stress-related genes are associated with habitat preference in two Cardamine lineages. BMC Evolutionary Biology, 12, 7.
Plotkin J B. 2011. Synonymous but not the same: The causes and consequences of codon bias. Nature Reviews Genetics, 12, 32–42.
Qian W, Yang J R, Pearson N M, Maclean C, Zhang J. 2012. Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genetics, 8, e1002603.
Qiu S, Bergero R, Zeng K, Charlesworth D. 2011a. Patterns of codon usage bias in Silene latifolia. Molecular Biology and Evolution, 28, 771–780.
Qiu S, Zeng K, Slotte T, Wright S, Charlesworth D. 2011b. Reduced efficacy of natural selection on codon usage bias in selfing Arabidopsis and Capsella species. Genome Biology and Evolution, 3, 868–880.
Rao Y, Wu G, Wang Z, Chai X, Nie Q, Zhang X. 2011. Mutation bias is the driving force of codon usage in the Gallus gallus genome. DNA Research, 18, 499–512.
Shah P, Gilchrist M A. 2010. Effect of correlated tRNA abundances on translation errors and evolution of codon usage bias. PLoS Genetics, 6, e1001128.
Sharp P M, Li W H. 1987. The codon adaption index - A measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research, 15, 1281–1295.
Song H, Gao H, Liu J, Tian P, Nan Z. 2017a. Comprehensive analysis of correlations among codon usage bias, gene expression, and substitution rate in Arachis duranensis and Arachis ipaënsis orthologs. Scientific Reports, 7, 14853.
Song H, Liu J, Song Q, Zhang Q, Tian P, Nan Z. 2017b. Comprehensive analysis of codon usage bias in seven Epichloë species and their peramine-coding genes. Frontiers in Microbiology, 8, 1419.
Song H, Nan Z. 2014. Genome-wide analysis of nucleotide-binding site disease resistance genes in Medicago truncatula. Chinese Science Bulletin, 59, 1129–1138.
Song H, Wang P F, Li T T, Xia H, Zhao S Z, Hou L, Zhao C Z. 2015. Genome-wide identification and evolutionary analysis of nucleotide-binding site-encoding resistance genes in Lotus japonicus (Fabaceae). Genetics and Molecular Research, 14, 16024–16040.
Song H, Zhang Q, Tian P, Nan Z. 2017c. Differential evolutionary patterns and expression levels between sex-specific and somatic tissue-specific genes in peanut. Scientific Reports, 7, 9016.
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.
De La Torre A R, Lin Y C, Van de Peer Y, Ingvarsson P K. 2015. Genome-wide analysis reveals diverged pattern of codon bias, gene expression, and rates of sequence evolution in Picea gene families. Genome Biology and Evolution, 7, 1002–1015.
Wang B, Shao Z Q, Xu Y, Liu J, Liu Y, Hang Y Y, Chen J Q. 2011. Optimal codon identities in bacteria: Implications from the conflicting results of two different method. PLoS ONE, 6, e22714.
Wang H C, Hickey D A. 2007. Rapid divergence of codon usage patterns within the rice genome. BMC Evolutionary Biology, 7, S6.
Whittle C A, Extavour C G. 2015. Codon and amino acid usage are shaped by selection across divergent model organisms of the Pancrustacea. G3: Genes Genomes Genetics, 5, 2307–2321.
Whittle C A, Malik M R, Krochko J E. 2007. Gender-specific selection on codon usage in plant genomes. BMC Genomics, 8, 169.
Whittle C A, Sun Y, Johannesson H. 2011. Evolution of synonymous codon usage in Neurospora tetrasperma and Neurospora discreta. Genome Biology and Evolution, 3, 332–343.
Williford A, Demuth J P. 2012. Gene expression levels are correlated with synonymous codon usage, amino acid composition, and gene architecture in the red flour beetle, Tribolium castaneum. Molecular Biology and Evolution, 29, 3755–3766.
Wright F. 1990. The ‘effective number of codons’ used in a gene. Gene, 87, 23–29.
Wright S I, Yan C B, Looseley M, Meyers B C. 2004. Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Molecular Biology and Evolution, 21, 1719–1726.
Yang H. 2009. In plants, expression breadth and expression level distinctly and non-linearly correlate with gene structure. Biology Direct, 4, 45.
Young N D, Debellé F, Oldroyd G E, Geurts R, Cannon S B, Udvardi M K, Benedito V A, Mayer K F, Gouzy J, Schoof H, Van de Peer Y, Proost S, Cook D R, Meyers B C, Spannagl M, Cheung F, De Mita S, Krishnakumar V, Gundlach H, Zhou S, et al. 2011. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature, 480, 520–524.
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.
Zhou M, Guo J, Cha J, Chae M, Chen S, Barral J M, Sachs M S, Liu Y. 2013. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature, 495, 111–115.
[1] ZHANG Yan-mei, AO De, LEI Kai-wen, XI Lin, Jerry W SPEARS, SHI Hai-tao, HUANG Yan-ling, YANG Fa-long. Dietary copper supplementation modulates performance and lipid metabolism in meat goat kids[J]. >Journal of Integrative Agriculture, 2023, 22(1): 214-221.
[2] JIANG Yong, MA Xin-yan, XIE Ming, ZHOU Zheng-kui, TANG Jing, CHANG Guo-bin, CHEN Guo-hong, HOU Shui-sheng. Dietary threonine deficiency affects expression of genes involved in lipid metabolism in adipose tissues of Pekin ducks in a genotype-dependent manner[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2691-2699.
[3] RONG Hao, YANG Wen-jing, XIE Tao, WANG Yue, WANG Xia-qin, JIANG Jin-jin, WANG You-ping. Transcriptional profiling between yellow- and black-seeded Brassica napus reveals molecular modulations on flavonoid and fatty acid content[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2211-2226.
[4] LIU Cong, LI De-xiong, HUANG Xian-biao, Zhang Fu-qiong, Xie Zong-zhou, Zhang Hong-yan, Liu Ji-hong. Manual thinning increases fruit size and sugar content of Citrus reticulata Blanco and affects hormone synthesis and sugar transporter activity[J]. >Journal of Integrative Agriculture, 2022, 21(3): 725-735.
[5] GUO Bing-bing, LI Jia-ming, LIU Xing, QIAO Xin, Musana Rwalinda FABRICE, WANG Peng, ZHANG Shao-ling, WU Ju-you. Identification and expression analysis of the PbrMLO gene family in pear, and functional verification of PbrMLO23[J]. >Journal of Integrative Agriculture, 2021, 20(9): 2410-2423.
[6] JI Xiao-hao, WANG Bao-liang, WANG Xiao-di, WANG Xiao-long, LIU Feng-zhi, WANG Hai-bo. Differences of aroma development and metabolic pathway gene expression between Kyoho and 87-1 grapes[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1525-1539.
[7] CHEN Chang-long, YUAN Fang, LI Xiao-ying, MA Rong-cai, XIE Hua. Jasmonic acid and ethylene signaling pathways participate in the defense response of Chinese cabbage to Pectobacterium carotovorum infection[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1314-1326.
[8] WANG Lu-lu, ZHAO Chun-fang, LIU Chang-jun, ZHANG Hao, LIAN Ling. Analysis of DNA methylation of CD79B in MDV-infected chicken spleen[J]. >Journal of Integrative Agriculture, 2021, 20(11): 2995-3002.
[9] WANG Xi-cheng, WU Wei-min, ZHOU Bei-bei, WANG Zhuang-wei, QIAN Ya-ming, WANG Bo, YAN Li-chun. Genome-wide analysis of the SCPL gene family in grape (Vitis vinifera L.)[J]. >Journal of Integrative Agriculture, 2021, 20(10): 2666-2679.
[10] CHI Zhuo-heng, WANG Yong-qing, DENG Qun-xian, ZHANG Hui, PAN Cui-ping, YANG Zhi-wu. Endogenous phytohormones and the expression of flowering genes synergistically induce flowering in loquat[J]. >Journal of Integrative Agriculture, 2020, 19(9): 2247-2256.
[11] LIU Xiang, KANG Zhi-wei, YU Xing-lin, LI Fan, LIU Tong-xian, LI Qiang . Role of TRP channels and HSPs in thermal stress response in the aphid parasitoid Aphelinus asychis (Hymenoptera: Aphelinidae)[J]. >Journal of Integrative Agriculture, 2020, 19(6): 1530-1542.
[12] ZHANG Zhen, LIU Qiang, WANG Cong, GUO Gang, HUO Wen-jie, ZHANG Yan-li, PEI Cai-xia, ZHANG Shuan-lin. Effects of palm fat powder and coated folic acid on growth performance, ruminal fermentation, nutrient digestibility and hepatic fat accumulation of Holstein dairy bulls[J]. >Journal of Integrative Agriculture, 2020, 19(4): 1074-1084.
[13] WANG Zi-yu, bAO Yu-fang, PEI Tong, WU Tai-ru, DU Xu, HE Meng-xi, WANG Yue, LIU Qi-feng, YANG Huan-huan, JIANG Jing-bin, ZHANG He, LI Jing-fu, ZHAO Ting-ting, XU Xiang-yang. Silencing the SLB3 transcription factor gene decreases drought stress tolerance in tomato[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2699-2708.
[14] WENG Bo, RAN Mao-liang, Cao Rong, PENG Fu-zhi, LUO Hui, GAO Hu, TANG Xiang-wei, Yang An-qi, CHEN Bin.
miR-10b promotes porcine immature Sertoli cell proliferation by targeting the DAZAP1 gene  
[J]. >Journal of Integrative Agriculture, 2019, 18(8): 1924-1935.
[15] WANG Shao-xi, SHI Feng-yan, DONG Xiang-xiang, LI Yu-xiang, ZHANG Zhi-hong, LI He. Genome-wide identification and expression analysis of auxin response factor (ARF) gene family in strawberry (Fragaria vesca)[J]. >Journal of Integrative Agriculture, 2019, 18(7): 1587-1603.
No Suggested Reading articles found!