[1] Xu Yuming, Qi Ting, Gu Wanjun, Lu Zuhong, et al. Evolutionary selection on synonymous codons in RNAG-quadruplex structural region [J]. Journal of Southeast University (English Edition), 2021, 37 (2): 177-183. [doi:10.3969/j.issn.1003-7985.2021.02.007]
Copy
Evolutionary selection on synonymous codons in RNAG-quadruplex structural region(
)
RNA G-四联体结构区的同义密码子进化选择
)Journal of Southeast University (English Edition)[ISSN:1003-7985/CN:32-1325/N]
- Volumn:
- 37
- Issue:
- 2021 2
- Page:
- 177-183
- Research Field:
- Biological Science and Medical Engineering
- Publishing date:
- 2021-06-20
Info
- Title:
- Evolutionary selection on synonymous codons in RNAG-quadruplex structural region
- RNA G-四联体结构区的同义密码子进化选择
- Author(s):
- Xu Yuming, Qi Ting, Gu Wanjun, Lu Zuhong
- School of Biological Science and Medical Engineering, Southeast University, Nanjing 210096, China
State Key Laboratory of Bioelectronics, Southeast University, Nanjing 210096, China
- PACS:
- Q311
- DOI:
- 10.3969/j.issn.1003-7985.2021.02.007
- Abstract:
- To investigate how synonymous codons have been adapted to the formation of ribonucleic acid(RNA)G-quadruplex(rG4)structure, a computational searching algorithm G4Hunter was applied to detect rG4 structures in protein-coding sequences of mRNAs in five eukaryotic species. The native sequences forming rG4s were then compared with randomized sequences to evaluate selection on synonymous codons. Factors that may influence the formation of rG4 were also investigated, and the selection pressures of rG4 in different gene regions were compared to explore its potential roles in gene regulation. The results show universal selective pressure acts on synonymous codons in rG4 regions to facilitate rG4 formation in five eukaryotic organisms. While G-rich codon combinations are preferred in the rG4 structural region, C-rich codon combinations are selectively unfavorable for rG4 formation. Gene’s codon usage bias, nucleotide composition, and evolutionary rate can account for the selective variations on synonymous codons among rG4 structures within a species. Moreover, rG4 structures in the translational initiation region showed significantly higher selective pressures than those in the translational elongation region.
- 为探索同义密码子对RNA G-四联体(rG4)形成的适应效应, 利用G4Hunter算法搜寻5类真核生物mRNA蛋白编码区的rG4结构.通过对比天然序列和随机序列, 评估rG4结构对同义密码子的选择偏好, 分析影响rG4形成的因素, 检验基因特定区域rG4结构的选择压力, 以揭示rG4在基因调控中的潜在作用.结果表明, 在5类真核生物中, rG4结构区内的同义密码子普遍受到促使rG4形成的选择压力.在rG4结构区内的蛋白编码序列倾向于使用富含鸟嘌呤的密码子组合, 不倾向于选择富含胞嘧啶的密码子组合.密码子使用偏好、碱基成分以及进化速率等因素和rG4对同义密码子的选择压力具有相关性.基因翻译起始区的序列受到更强的促使rG4结构形成的选择压力.
References:
[1] Shabalina S A, Spiridonov N A, Kashina A. Sounds of silence: Synonymous nucleotides as a key to biological regulation and complexity[J].Nucleic Acids Research, 2013, 41(4): 2073-2094. DOI:10.1093/nar/gks1205.
[2] Plotkin J B, Kudla G. Synonymous but not the same: The causes and consequences of codon bias[J].Nature Reviews Genetics, 2011, 12(1): 32-42. DOI:10.1038/nrg2899.
[3] Hunt R C, Simhadri V L, Iandoli M, et al. Exposing synonymous mutations[J].Trends in Genetics, 2014, 30(7): 308-321. DOI:10.1016/j.tig.2014.04.006.
[4] Chamary J V, Hurst L D. Biased codon usage near intron-exon junctions: Selection on splicing enhancers, splice-site recognition or something else? [J].Trends in Genetics, 2005, 21(5): 256-259. DOI:10.1016/j.tig.2005.03.001.
[5] Stoletzki N. Conflicting selection pressures on synonymous codon use in yeast suggest selection on mRNA secondary structures[J].BMC Evolutionary Biology, 2008, 8(1): 1-9. DOI:10.1186/1471-2148-8-224.
[6] Warnecke T, Batada N N, Hurst L D. The impact of the nucleosome code on protein-coding sequence evolution in yeast[J].PLoS Genetics, 2008, 4(11): e1000250. DOI:10.1371/journal.pgen.1000250.
[7] Parmley J L, Chamary J V, Hurst L D. Evidence for purifying selection against synonymous mutations in mammalian exonic splicing enhancers[J].Molecular Biology and Evolution, 2006, 23(2): 301-309. DOI:10.1093/molbev/msj035.
[8] Warnecke T, Hurst L D. Evidence for a trade-off between translational efficiency and splicing regulation in determining synonymous codon usage in drosophila melanogaster[J].Molecular Biology and Evolution, 2007, 24(12): 2755-2762. DOI:10.1093/molbev/msm210.
[9] Gu W J, Wang X F, Zhai C Y, et al. Selection on synonymous sites for increased accessibility around miRNA binding sites in plants[J].Molecular Biology and Evolution, 2012, 29(10): 3037-3044. DOI:10.1093/molbev/mss109.
[10] Kudla G, Murray A W, Tollervey D, et al. Coding-sequence determinants of gene expression in escherichia coli[J].Science, 2009, 324(5924): 255-258. DOI:10.1126/science.1170160.
[11] Gu W J, Zhou T, Wilke C O. A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes[J].PLoS Computational Biology, 2010, 6(2): e1000664. DOI:10.1371/journal.pcbi.1000664.
[12] Tuller T, Waldman Y Y, Kupiec M, et al. Translation efficiency is determined by both codon bias and folding energy[J].PNAS, 2010, 107(8): 3645-3650. DOI:10.1073/pnas.0909910107.
[13] Gingold H, Pilpel Y. Determinants of translation efficiency and accuracy[J].Molecular Systems Biology, 2011, 7: 481. DOI:10.1038/msb.2011.14.
[14] Thanaraj T A, Argos P. Ribosome-mediated translational pause and protein domain organization[J].Protein Science, 1996, 5(8): 1594-1612. DOI:10.1002/pro.5560050814.
[15] Komar A A, Lesnik T, Reiss C. Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation[J]. FEBS Letters, 1999, 462(3): 387-391. DOI:10.1016/s0014-5793(99)01566-5.
[16] Kharel P, Balaratnam S, Beals N, et al. The role of RNA G-quadruplexes in human diseases and therapeutic strategies[J].Wiley Interdisciplinary Reviews RNA, 2020, 11(1): e1568. DOI:10.1002/wrna.1568.
[17] Kwok C K, Marsico G, Sahakyan A B, et al. rG4-seq reveals widespread formation of G-quadruplex structures in the human transcriptome[J].Nature Methods, 2016, 13(10): 841-844. DOI:10.1038/nmeth.3965.
[18] Huang H L, Zhang J, Harvey S E, et al. RNA G-quadruplex secondary structure promotes alternative splicing via the RNA-binding protein hnRNPF[J].Genes & Development, 2017, 31(22): 2296-2309. DOI:10.1101/gad.305862.117.
[19] Beaudoin J D, Perreault J P. Exploring mRNA 3’-UTR G-quadruplexes: Evidence of roles in both alternative polyadenylation and mRNA shortening[J].Nucleic Acids Research, 2013, 41(11): 5898-5911. DOI:10.1093/nar/gkt265.
[20] Subramanian M, Rage F, Tabet R, et al. G-quadruplex RNA structure as a signal for neurite mRNA targeting[J].EMBO Reports, 2011, 12(7): 697-704. DOI:10.1038/embor.2011.76.
[21] Kanai Y, Dohmae N, Hirokawa N. Kinesin transports RNA: Isolation and characterization of an RNA-transporting granule[J].Neuron, 2004, 43(4): 513-525. DOI:10.1016/j.neuron.2004.07.022.
[22] Stefanovic S, Bassell G J, Mihailescu M R. G quadruplex RNA structures in PSD-95 mRNA: Potential regulators of miR-125a seed binding site accessibility[J].RNA, 2015, 21(1): 48-60. DOI:10.1261/rna.046722.114.
[23] Beaudoin J D, Perreault J P. 5’-UTR G-quadruplex structures acting as translational repressors[J].Nucleic Acids Research, 2010, 38(20): 7022-7036. DOI:10.1093/nar/gkq557.
[24] Bugaut A, Balasubramanian S. 5′-UTR RNA G-quadruplexes: Translation regulation and targeting[J].Nucleic Acids Research, 2012, 40(11): 4727-4741. DOI:10.1093/nar/gks068.
[25] Kamura T, Katsuda Y, Kitamura Y, et al. G-quadruplexes in mRNA: A key structure for biological function[J].Biochemical and Biophysical Research Communications, 2020, 526(1): 261-266. DOI:10.1016/j.bbrc.2020.02.168.
[26] Kumari S, Bugaut A, Huppert J L, et al. An RNA G-quadruplex in the 5′ UTR of the NRAS proto-oncogene modulates translation[J].Nature Chemical Biology, 2007, 3(4): 218-221. DOI:10.1038/nchembio864.
[27] Murat P, Marsico G, Herdy B, et al. RNA G-quadruplexes at upstream open reading frames cause DHX36-and DHX9-dependent translation of human mRNAs[J].Genome Biology, 2018, 19(1): 229. DOI:10.1186/s13059-018-1602-2.
[28] Simone R, Fratta P, Neidle S, et al. G-quadruplexes: Emerging roles in neurodegenerative diseases and the non-coding transcriptome[J].FEBS Letters, 2015, 589(14): 1653-1668. DOI:10.1016/j.febslet.2015.05.003.
[29] Fay M M, Lyons S M, Ivanov P. RNA G-quadruplexes in biology: Principles and molecular mechanisms[J].Journal of Molecular Biology, 2017, 429(14): 2127-2147. DOI:10.1016/j.jmb.2017.05.017.
[30] Mirihana Arachchilage G, Hetti Arachchilage M, Venkataraman A, et al. Stable G-quadruplex enabling sequences are selected against by the context-dependent codon bias[J].Gene, 2019, 696: 149-161. DOI:10.1016/j.gene.2019.02.006.
[31] Kinsella R J, K�E4;h�E4;ri A, Haider S, et al. Ensembl BioMarts: A hub for data retrieval across taxonomic space[J].Database, 2011, 2011(10.1093): database. DOI:10.1093/database/bar030.
[32] Chen Y H, Wang X W. miRDB: An online database for prediction of functional microRNA targets[J].Nucleic Acids Research, 2020, 48(D1): D127-D131. DOI:10.1093/nar/gkz757.
[33] Liu W J, Wang X W. Prediction of functional microRNA targets by integrative modeling of microRNA binding and target expression data[J].Genome Biology, 2019, 20(1): 18. DOI:10.1186/s13059-019-1629-z.
[34] Wright F. The ‘effective number of codons’ used in a gene[J].Gene, 1990, 87(1): 23-29. DOI:10.1016/0378-1119(90)90491-9.
[36] Nielsen R. Molecular signatures of natural selection[J].Annual Review of Genetics, 2005, 39: 197-218. DOI:10.1146/annurev.genet.39.073003.112420.
[37] Bedrat A, Lacroix L, Mergny J L. Re-evaluation of G-quadruplex propensity with G4Hunter[J].Nucleic Acids Research, 2016, 44(4): 1746-1759. DOI:10.1093/nar/gkw006.
[38] Lacroix L. G4HunterApps[J].Bioinformatics, 2019, 35(13): 2311-2312. DOI:10.1093/bioinformatics/bty951.
[39] Puig Lombardi E, Londo�F1;o-Vallejo A. A guide to computational methods for G-quadruplex prediction[J].Nucleic Acids Research, 2020, 48(1): 1-15. DOI:10.1093/nar/gkz1097.
[40] Guo J U, Bartel D P. RNA G-quadruplexes are globally unfolded in eukaryotic cells and depleted in bacteria[J].Science, 2016, 353(6306):5371. DOI:10.1126/science.aaf5371.
Memo
- Memo:
-
Biographies: Xu Yuming(1988—), male, Ph.D. candidate; Lu Zuhong(corresponding author), male, doctor, professor, zhlu@seu.edu.cn.
Foundation items: The National Key Research and Development Program of China(No. 2018YFC1314900, 2018YFC1314902), the National Natural Science Foundation of China(No. 61571109), the Fundamental Research Funds for the Central Universities(No. 2242017K3DN04).
Citation: Xu Yuming, Qi Ting, Gu Wanjun, et al.Evolutionary selection on synonymous codons in RNA G-quadruplex structural region[J].Journal of Southeast University(English Edition), 2021, 37(2):177-183.DOI:10.3969/j.issn.1003-7985.2021.02.007.