Antagonistic relationships between intron content and codon usage bias of genes in three mosquito species: Functional and evolutionary implications

Evolutionary Applications

Volumn 6, Issue 7, 2013, Pages 1079-1089

  Behura, Susanta K ^a   Singh, Brajendra K ^a   Severson, David W ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Codon bias; Coevolution; Intron; Mosquito; Ortholog

Indexed keywords

EID: 84885799609     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12088     Document Type: Article

References (85)

1. Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32-46.
2. Anderson, M. J., and T. J. Willis 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511-525.
3. Andersson, S. G., and C. G. Kurland 1990. Codon preferences in free-living microorganisms. Microbiological Reviews 54:198-210.
4. Arensburger, P., K. Megy, R. M. Waterhouse, J. Abrudan, P. Amedeo, B. Antelo, L. Bartholomay et al. 2010. Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330:86-88.
5. Behura, S. K. 2006. Molecular marker systems in insects: current trends and future avenues. Molecular Ecology 15:3087-3113.
6. Behura, S. K., and D. W. Severson 2011. Coadaptation of isoacceptor tRNA genes and codon usage bias for translation efficiency in Aedes aegypti and Anopheles gambiae. Insect Molecular Biology 20:177-187.
7. Behura, S. K., and D. W. Severson 2012a. Intrinsic features of Aedes aegypti genes affect transcriptional responsiveness of mosquito genes to dengue virus infection. Infection, Genetics and Evolution 12:1413-1418.
8. Behura, S. K., and D. W. Severson 2012b. Comparative analysis of codon usage bias and codon context patterns between dipteran and hymenopteran sequenced genomes. PLoS ONE 7:e43111.
9. Behura, S. K., and D. W. Severson 2013a. Codon usage bias: causative factors, quantification methods and genome-wide patterns: with emphasis on insect genomes. Biological Reviews 88:49-61.
10. Behura, S. K., and D. W. Severson 2013b. Nucleotide substitutions in dengue virus serotypes from Asian and American countries: insights into intracodon recombination and purifying selection. BMC Microbiology 13:37.
11. Behura, S. K., M. Stanke, C. A. Desjardins, J. H. Werren, and D. W. Severson 2010. Comparative analysis of nuclear tRNA genes of Nasonia vitripennis and other arthropods, and relationships to codon usage bias. Insect Molecular Biology 19:49-58.
12. Behura, S. K., C. Gomez-Machorro, B. W. Harker, B. de Bruyn, D. D. Lovin, R. R. Hemme, A. Mori et al. 2011. Global cross-talk of genes of the mosquito Aedes aegypti in response to dengue virus infection. PLoS Neglected Tropical Diseases 5:e1385.
13. Biro, J. C. 2008. Does codon bias have an evolutionary origin? Theoretical Biology & Medical Modelling 5:16.
14. Botzman, M., and H. Margalit 2011. Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biology 12:R109.
15. Camiolo, S., L. Farina, and A. Porceddu 2012. The relation of codon bias to tissue-specific gene expression in Arabidopsis thaliana. Genetics 192:641-649.
16. Carilini, D. B., Y. Chen, and W. Stephan 2001. The relationship between third-codon position nucleotide content, codon bias, mRNA secondary structure and gene expression in the drosophilid alcohol dehydrogenase genes Adh and Adhr. Genetics 159:623-633.
17. Carmel, L., Y. I. Wolf, I. B. Rogozin, and E. V. Koonin 2007. Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Research 17:1034-1044.
18. Castillo-Davis, C. I., S. L. Mekhedov, D. L. Hartl, E. V. Koonin, and F. A. Kondrashov 2002. Selection for short introns in highly expressed genes. Nature Genetics 31:415-418.
19. Chamary, J. V., and L. D. Hurst 2005. Biased codon usage near intron-exon junctions: selection on splicing enhancers, splice-site recognition or something else? Trends in Genetics 21:256-259.
20. Coleman, J. R., D. Papamichail, S. Skiena, B. Futcher, E. Wimmer, and S. Mueller 2008. Virus attenuation by genome-scale changes in codon pair bias. Science 320:1784-1787.
21. Coulombe-Huntington, J., and J. Majewski 2007a. Intron loss and gain in Drosophila. Molecular Biology and Evolution 24:2842-2850.
22. Coulombe-Huntington, J., and J. Majewski 2007b. Characterization of intron loss events in mammals. Genome Research 17:23-32.
23. Davis, J. C., and D. A. Petrov 2004. Preferential duplication of conserved proteins in eukaryotic genomes. PLoS Biology 2:e55.
24. Drummond, D. A., J. D. Bloom, C. Adami, C. O. Wilke, and F. H. Arnold 2005. Why highly expressed proteins evolve slowly. Proceedings of the National Academy of Sciences of the United States of America 10240:14338-14343.
25. Duret, L., and D. Mouchiroud 1999. 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 96:4482-4487.
26. Fang, J. 2010. Ecology: A world without mosquitoes. Nature 466:432-434.
27. Fletcher, S. P., M. Muto, and S. P. Mayfield 2007. Optimization of recombinant protein expression in the chloroplasts of green algae. Advances in Experimental Medicine and Biology 616:90-98.
28. Fuglsang, A. 2003. Patterns of context-dependent codon biases. Biochemical and Biophysical Research Communications 304:86-90.
29. Gassmann, A. J., D. W. Onstad, and B. R. Pittendrigh 2009. Evolutionary analysis of herbivorous insects in natural and agricultural environments. Pest Management Science 65:1174-1181.
30. Gilbert, W. 1978. Why genes in pieces. Nature 271:501.
31. Grimmelikhuijzen, C. J., G. Cazzamali, M. Williamson, and F. Hauser 2007. The promise of insect genomics. Pest Management Science 63:413-416.
32. Gustafsson, C., S. Govindarajan, and J. Minshull 2004. Codon bias and heterologous protein expression. Trends in Biotechnology 22:346-353.
33. Haddrill, P. R., B. Charlesworth, D. L. Halligan, and P. Andolfatto 2005. Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biology 6:R67.
34. Heckel, D. G. 2003. Genomics in pure and applied entomology. Annual Review of Entomology 48:235-260.
35. Hershberg, R., and D. A. Petrov 2008. Selection on codon bias. Annual review of genetics 42:287-299.
36. Hill, C. A., F. C. Kafatos, S. K. Stansfield, and F. H. Collins 2005. Arthropod-borne diseases: vector control in the genomics era. Nature Reviews Microbiology 3:262-268.
37. Holt, R. A., G. M. Subramanian, A. Halpern, G. G. Sutton, R. Charlab, D. R. Nusskern, P. Wincker et al. 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129-149.
38. de Hoon, M. J. L., S. Imoto, J. Nolan, and S. Miyano 2004. Open source clustering software. Bioinformatics 20:1453-1454.
39. Jeffares, D. C., T. Mourier, and D. Penny 2006. The biology of intron gain and loss. Trends in Genetics 22:16-22.
40. Jeffares, D. C., C. J. Penkett, and J. Bähler 2008. Rapidly regulated genes are intron poor. Trends in Genetics 24:375-378.
41. Koonin, E. V. 2006. The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate? Biology Direct 1:22.
42. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin et al. 2007. ClustalW and ClustalX version 2.0. Bioinformatics 23:2947-2948.
43. Le Hir, H., A. Nott, and M. J. Moore 2003. How introns influence and enhance eukaryotic gene expression. Trends in Biochemical Sciences 28:215-220.
44. Le, Y. J., H. Kim, J. H. Chung, and Y. Lee 2001. Testis-specific expression of an intronless gene encoding a human poly(A) polymerase. Molecules and Cells 11:379-385.
45. Li, W., A. E. Tucker, W. Sung, W. K. Thomas, and M. Lynch 2009. Extensive, recent intron gains in Daphnia populations. Science 326:1260-1262.
46. Lobo, F. P., B. E. Mota, S. D. Pena, V. Azevedo, A. M. Macedo, A. Tauch, C. R. Machado et al. 2009. Virus-host coevolution: common patterns of nucleotide motif usage in Flaviviridae and their hosts. PLoS ONE 4:e6282.
47. Manly, B. F. J. 2006. Randomization, Bootstrap and Monte Carlo Methods in Biology. 3rd edn. Chapman & Hall, London.
48. Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27:209-220.
49. McArthur, G. H. 4th, and S. S. Fong 2010. Toward engineering synthetic microbial metabolism. Journal of Biomedicine & Biotechnology 2010:459760.
50. Meusemann, K., B. M. von Reumont, S. Simon, F. Roeding, S. Strauss, P. Kück, I. Ebersberger et al. 2010. A phylogenomic approach to resolve the arthropod tree of life. Molecular Biology and Evolution 27:2451-2464.
51. Moriyama, E. N., and J. R. Powell 1998. Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Research 26:3188-3193.
52. Mueller, S., D. Papamichail, J. R. Coleman, S. Skiena, and E. Wimmer 2006. Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. Journal of Virology 80:9687-9696.
53. Nene, V., J. R. Wortman, D. Lawson, B. Haas, C. Kodira, Z. J. Tu, B. Loftus et al. 2007. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316:1718-1723.
54. Pagel, M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London. Series B: Biological Sciences 255:37-45.
55. Pagel, M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology 48:612-622.
56. Pagel, M., and A. Meade 2004. A phylogenetic mixture model for detecting pattern-heterogeneity in gene sequence or character-state data. Systematic Biology 53:571-581.
57. Pál, C., B. Papp, and L. D. Hurst 2001. Highly expressed genes in yeast evolve slowly. Genetics 158:927-931.
58. Parmley, J. L., and L. D. Hurst 2007. Exonic splicing regulatory elements skew synonymous codon usage near intron-exon boundaries in mammals. Molecular Biology and Evolution 24:1600-1603.
59. Plotkin, J. B., and G. Kudla 2011. Synonymous but not the same: the causes and consequences of codon bias. Nature Reviews Genetics 12:32-42.
60. Qin, Z., Z. Cai, G. Xia, and M. Wang 2013. Synonymous codon usage bias is correlative to intron number and shows disequilibrium among exons in plants. BMC Genomics 14:56.
61. Rocha, E. P. 2004. Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Research 14:2279-2286.
62. Rodriguez, O., B. K. Singh, D. W. Severson, and S. K. Behura 2012. Translational selection of genes coding for perfectly conserved proteins among three mosquito vectors. Infection, Genetics and Evolution 12:1535-1542.
63. Rodríguez-Trelles, F., R. Tarrío, and F. J. Ayala 2006a. Origins and evolution of spliceosomal introns. Annual Review of Genetics 40:47-76.
64. Rodríguez-Trelles, F., R. Tarrío, and F. J. Ayala 2006b. Models of spliceosomal intron proliferation in the face of widespread ectopic expression. Gene 366:201-208.
65. Rogozin, I. B., L. Carmel, M. Csuros, and E. V. Koonin 2012. Origin and evolution of spliceosomal introns. Biology Direct 7:11.
66. Roy, S. W., and W. Gilbert, 2005a. Rates of intron loss and gain: implications for early eukaryotic evolution. Proceedings of the National Academy of Sciences of the United States of America.102:5773-5778.
67. Roy, S. W., and W. Gilbert 2005b. Resolution of a deep animal divergence by the pattern of intron conservation. Proceedings of the National Academy of Sciences of the United States of America 102:4403-4408.
68. Roy, S. W., and W. Gilbert 2005c. Complex early genes. Proceedings of the National Academy of Sciences of the United States of America 102:1986-1991.
69. Roy, S. W., and W. Gilbert 2005d. The pattern of intron loss. Proceedings of the National Academy of Sciences of the United States of America 102:713-718.
70. Roy, S. W., and W. Gilbert 2006. The evolution of spliceosomal introns: patterns, puzzles and progress. Nature Reviews Genetics 7:211-221.
71. Schneider, D. S., and A. A. James 2006. Bridging the gaps in vector biology. Workshop on the molecular and population biology of mosquitoes and other disease vectors. EMBO Reports 7:259-262.
72. Severson, D. W., and S. K. Behura 2012. Mosquito genomics: progress and challenges. Annual Review of Entomology 57:143-166.
73. Shabalina, S. A., A. Y. Ogurtsov, A. N. Spiridonov, P. S. Novichkov, N. A. Spiridonov, and E. V. Koonin 2010. Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Molecular Biology and Evolution 27:1745-1749.
74. Subramanian, S. 2008. Nearly neutrality and the evolution of codon usage bias in eukaryotic genomes. Genetics 178:2429-2432.
75. Subramanian, S., and S. Kumar 2004. Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168:373-381.
76. Tripet, F. 2009. Ecological immunology of mosquito-malaria interactions: of non-natural versus natural model systems and their inferences. Parasitology 136:1935-1942.
77. Vinogradov, A. E. 1999. Intron-genome size relationship on a large evolutionary scale. Journal of Molecular Evolution 49:376-384.
78. Vinogradov, A. E. 2001. Intron length and codon usage. Journal of Molecular Evolution 52:2-5.
79. Wan, X. F., D. Xu, A. Kleinhofs, and J. Zhou 2004. Quantitative relationship between synonymous codon usage bias and GC composition across unicellular genomes. BMC Evolutionary Biology 4:19.
80. Warnecke, T., and L. D. Hurst 2007. Evidence for a trade-off between translational efficiency and splicing regulation in determining synonymous codon usage in Drosophila melanogaster. Molecular Biology and Evolution 24:2755-2762.
81. Waterhouse, R. M., E. V. Kriventseva, S. Meister, Z. Xi, K. S. Alvarez, L. C. Bartholomay, C. Barillas-Mury et al. 2007. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316:1738-1743.
82. Waterhouse, R. M., S. Wyder, and E. M. Zdobnov 2008. The Aedes aegypti genome: a comparative perspective. Insect Molecular Biology 17:1-8.
83. Yang, Y. F., T. Zhu, and D. K. Niu 2013. Association of intron loss with high mutation rate in Arabidopsis: implications for genome size evolution. Genome Biology and Evolution 5:723-733.
84. Zhang, L., and W. H. Li 2004. Mammalian housekeeping genes evolve more slowly than tissue-specific genes. Molecular Biology and Evolution 21:236-239.
85. Zhu, T., and D. Niu 2013. Frequency of intron loss correlates with processed pseudogene abundance: a novel strategy to test the reverse transcriptase model of intron loss. BMC Biology 11:23.