Analysis of codon usage bias in the genome of Epichloё gansuensis

doi:10.11686/cyxb2019335

Abstract

Abstract: The sequence of multiple sets of triplet adjacent DNA or RNA nucleotides (codon) determines amino acid sequence. In the long process of adaptive evolution, the codon usage of organisms has developed certain biases. Two major factors affect codon usage bias. The species ‘Epichloё gansuensis’ is an important endophytic fungus. E. gansuensis infection can improve the host resistance to biotic and abiotic stress, but the fungus produces secondary alkaloid metabolites that may poison livestock. This study aimed to analyze the basic composition of the genome of E. gansuensis and the pattern of codon usage, and to determine the optimal codon. Correlation of each codon index with gene length, amino acid usage frequency and other indicators was analyzed, to identify the main factors affecting codon usage. We found that the GC3 is mainly distributed between 40%-60%, the effective codon number of 62.7% genes distributed between 0-0.1, 95.4% effective codon numbers are lower than the expected and lie to the lower right of the expectation curve. These results suggest that mutation pressure is one of the main influencing factors on codon usage of E. gansuensis. However, the neutral analysis showed a significant positive correlation between GC12 and GC3 (r=0.110, P<0.01), with a slope of the regression line 0.2729. It suggests that the effect of mutation on codon usage was only 27.29%, 82.71% for other factors. Correlation analysis also showed that hydrophobic amino acids had the greatest effect on the codon usage of E. gansuensis, greater than that of aromatic amino acids. In addition, 26 optimal codon that end with a G or C residue from E. gansuensis were identified, indicating that codon usage in E. gansuensis may relate to the presence of a GC residue at the third position of the triplet codon. These optimal codon are significantly correlated with transcription level, and may help in the design of degenerative primers, for tracing the evolutionary origin of endophytic fungi.

Key words: Epichloë, gansuensis, codon usage bias, mutation, natural selection, amino acid

LI Xiu-zhang, SONG Hui, ZHANG Zong-hao, XU Hai-feng, LIU Xin, LI Yu-ling, LI Chun-jie. Analysis of codon usage bias in the genome of Epichloё gansuensis[J]. Acta Prataculturae Sinica, 2020, 29(5): 67-77.

References

[1] Grantham R, Gautier C, Gouy M, et al. Codon catalog usage and the genome hypothesis. Nucleic Acids Research, 1980, 8(1): 197.
[2] Martin A, Bertranpetit J, Oliver J, et al. Variation in G+C content and codon choice: Differences among synonymous codon groups in vertebrate genes. Nucleic Acids Research, 1989, 17(15): 6181-6189.
[3] Sharp P M, Li W H. Codon usage in regulatory genes in Escherichia coli does not reflect selection for ‘rare’ codons. Nucleic Acids Research, 1986, 14(19): 7737-7749.
[4] Duret L, Mouchiroud D. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(8): 4482-4487.
[5] Gu W, Zhou T, Ma J, et al. Analysis of synonymous codon usage in SARS coronavirus and other viruses in the nidovirales. Virus Research, 2004, 101(2): 155-161.
[6] Linden V D, Marx G, de Farias S T. Correlation between codon usage and thermostability. Extremophiles, 2006, 10(5): 479-481.
[7] Sharp P M, Cowe E, Higgins D G, et al. Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Research, 1988, 16(17): 8207-8211.
[8] Chiapello H, Lisacek F, Caboche M, et al. Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene, 1998, 209(1): 1-38.
[9] Moriyama E N, Powell J R. Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Research, 1998, 26(13): 3188-3193.
[10] Sueoka N, Kawanishi Y. DNA G+C content of the third codon position and codon usage biases of human genes. Gene, 2000, 261(1): 53-62.
[11] Marais G, Mouchiroud D, Duret L. Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98(10): 5688-5692.
[12] Zhou T, Gu W, Ma J, et al. Analysis of synonymous codon usage in H5N1 virus and other influenza a viruses. Biosystems, 2005, 81(1): 77-86.
[13] Chen H T, Gu Y X, Liu Y S. Analysis of synonymous codon usage in dengue viruses. Journal of Animal & Veterinary Advances, 2013, 12(1): 88-98.
[14] Butt A M, Nasrullah I, Tong Y. Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS One, 2014, 9(3): e90905.
[15] Schardl C L, Scott B, Florea S, et al. Epichloё endophytes: Clavicipitaceous symbionts of grasses//Plant relationships. Berlin Heidelberg: Springer, 2009: 275-306.
[16] Leuchtmann A, Bacon C W, Schardl C L, et al. Nomenclatural realignment of Neotyphodium species with genus Epichloё. Mycologia, 2014, 106(2): 202-215.
[17] Tanaka A, Takemoto D, Chujo T, et al. Fungal endophytes of grasses. Current Opinion in Plant Biology, 2012, 15(4): 462-468.
[18] Latch G. An overview of Neotyphodium-grass interactions, in Neotyphodium/grass interactions. Boston: Springer, 1997: 1-11.
[19] Li C J, Nan Z B, Paul V H, et al. A new Neotyphodium species symbiotic with drunken horse grass (Achnatherum inebrians) in China. Mycotaxon, 2004, 90(1): 141-147.
[20] Nan Z B, Li C J. Roles of the grass-Neotyphodiuem association in pastoral agriculture systems. Acta Ecologica Sinica, 2004, 24(3): 605-616.
南志标, 李春杰. 禾草内生真菌共生体在草地农业系统中的作用. 生态学报, 2004, 24(3): 605-616.
[21] Li X Z, Fang A G, Li C J, et al. Advances in the researches on the effects of grass endophytes on other microbes. Acta Ecologica Sinica, 2015, 35(6): 1660-1671.
李秀璋, 方爱国, 李春杰, 等. 禾草内生真菌对其他微生物影响的研究进展. 生态学报, 2015, 35(6): 1660-1671.
[22] Li C J, Yao X, Nan Z B. Advances in research of Achnatherum inebrians-Epichloё endophyte symbionts. Chinese Journal of Plant Ecology, 2018, 42(8): 793-805.
李春杰, 姚祥, 南志标. 醉马草内生真菌共生体研究进展. 植物生态学报, 2018, 42(8): 793-805.
[23] Liu J, Chen Z J, Li X Z, et al. Interaction effects of exogenous salicylic acid, abscisic acid and Epichloё on Achnatherum inebrians symbiosis under low temperature stress. Acta Prataculturae Sinica, 2018, 27(1): 142-151.
刘静, 陈振江, 李秀璋, 等. 低温处理下外源水杨酸和脱落酸与内生真菌互作对醉马草共生体的影响. 草业学报, 2018, 27(1): 142-151.
[24] Guo C H, Li X Z, Liu L, et al. Effect of the Epichloё endophyte on the soil nematode community in the rhizosphere of Achnatherum inebrians. Acta Prataculturae Sinica, 2016, 25(4): 140-148.
郭长辉, 李秀璋, 柳莉, 等. 内生真菌对醉马草根际土壤线虫群落的影响. 草业学报, 2016, 25(4): 140-148.
[25] Schardl C L, Young C A, Pan J, et al. Currencies of mutualisms: Sources of alkaloid genes in vertically transmitted epichloae. Toxins, 2013, 5(6): 1064-1088.
[26] Jansen R, Bussemaker H J, Gerstein M. Revisiting the codon adaptation index from a whole-genome perspective: Analyzing the relationship between gene expression and codon occurrence in yeast using a variety of models. Nucleic Acids Research, 2003, 31(8): 2242-2251.
[27] Wright F. The ‘effective number of codons’ used in a gene. Gene, 1990, 87(1): 23-29.
[28] Sharp P M, Li W H. The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research, 1987, 15(3): 1281-1295.
[29] Drews O, Reil G, Parlar H, et al. Setting up standards and a reference map for the alkaline proteome of the Gram-positive bacterium Lactococcus lactis. Proteomics, 2004, 4(5): 1293-1304.
[30] Huang X, Xu J, Chen L, et al. Analysis of transcriptome data reveals multifactor constraint on codon usage in Taenia multiceps. BMC Genomics, 2017, 18(1): 308.
[31] Chen H X, Sun S C, Norenburg J L, et al. Mutation and selection cause codon usage and bias in mitochondrial genomes of ribbon worms (Nemertea). PLoS One, 2014, 9(1): e85631.
[32] Zhang W J, Zhou J, Li Z F, et al. Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L. Journal of Integrative Plant Biology, 2007, 49(2): 246-254.
[33] Liu Q P, Feng Y, Zhao X A, et al. Synonymous codon usage bias in Oryza sativa. Plant Science, 2004, 167(1): 101-105.
[34] Jia X, Liu S Y, Zheng H, et al. Non-uniqueness of factors constraint on the codon usage in Bombyx mori. BMC Genomics, 2015, 16(1): 1.
[35] Kramer C Y. Extension of multiple range tests to group means with unequal numbers of replications. Biometrics, 1956, 12(3): 307-310.
[36] Bulmer M. The selection-mutation-drift theory of synonymous codon usage. Genetics, 1991, 129(3): 897.
[37] Nakamura Y, Gojobori T, Ikemura T. Codon usage tabulated from the international DNA sequence databases. Nucleic Acids Research, 1999, 27(1): 292.
[38] Fuglsang A. The ‘effective number of codons’ revisited. Biochemical and Biophysical Research Communications, 2004, 317(3): 957-964.
[39] Shields D C, Sharp P M. Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Research, 1987, 15(19): 8023-8040.
[40] Song H, Gao H, Jing L, et al. Comprehensive analysis of correlations among codon usage bias, gene expression, and substitution rate in Arachis duranensis and Arachis ipaёnsis orthologs. Scientific Reports, 2017, 7(1): 14853.
[41] Song H, Wang P F, Ma D C, et al. Analysis of codon usage bias of WRKY transcription factors in Medicago truncatula. Journal of Agricultural Biotechnology, 2015, 23(2): 203-212.
宋辉, 王鹏飞, 马登超, 等. 蒺藜苜蓿WRKY转录因子密码子使用偏好性分析. 农业生物技术学报, 2015, 23(2): 203-212.
[42] Li X Z, Song H, Kuang Y, et al. Genome-wide analysis of codon usage bias in Epichloё festucae. International Journal of Molecular Sciences, 2016, 17(7): 1138.
[43] Song H, Liu J, Song Q, et al. Comprehensive analysis of codon usage bias in seven Epichloё species and their peramine-coding genes. Frontiers in Microbiology, 2017, 8(7): 1419.
[44] Li X Z, Song H, Li C J. Analysis of codon usage bias in mitochondria genome of Fusarium solani. Genomics and Applied Biology, 2015, 34(11): 2465-2472.
李秀璋, 宋辉, 李春杰. 茄腐镰孢(Fusarium solani)线粒体基因组密码子偏好性分析. 基因组学与应用生物学, 2015, 34(11): 2465-2472.
[45] Li H, Luo L F. The relations of gene expression level with codon usage and its prediction. Journal of Inner Mongolia University (Nature Science Edition), 1995, 26(5): 544-561.
李宏, 罗辽复. 基因表达水平与密码子使用的关系及其预测. 内蒙古大学学报(自然科学版), 1995, 26(5): 544-561.
[46] Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. Journal of Molecular Biology, 1981, 146(1): 1-21.
[47] Varenne S, Baty D, Verheij H, et al. The maximum rate of gene expression is dependent in the downstream context of unfavourable codons. Biochimie, 1989, 71(11): 1221-1229.
[48] Perrière G, Thioulouse J. Use and misuse of correspondence analysis in codon usage studies. Nucleic Acids Research, 2002, 30(20): 4548-4555.
[49] Liu H, He R, Zhang H, et al. Analysis of synonymous codon usage in Zea mays. Molecular Biology Reports, 2010, 37(2): 677-684.
[50] Yang G F, Su K L, Zhao Y R, et al. Analysis of codon usage in the chloroplast genome of Medicago truncatula. Acta Prataculturae Sinica, 2015, 24(12): 171-179.
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. 草业学报, 2015, 24(12): 171-179.
[51] Sharp P M, Cowe E. Synonymous codon usage in Saccharomyces cerevisiae. Yeast, 1991, 7(7): 657-678.