Factors affecting mito-nuclear codon usage interactions in the OXPHOS system of Drosophila melanogaster

Zheng Sun; Liang Ma; Robert W. Murphy; Xiansheng Zhang; Dawei Huang

doi:10.1016/S1673-8527(08)60228-3

Volume 35 Issue 12

Dec. 2008

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2008 > 35(12): 729-735

PDF( 216 KB)

Factors affecting mito-nuclear codon usage interactions in the OXPHOS system of Drosophila melanogaster

doi: 10.1016/S1673-8527(08)60228-3

a
College of Plant Protection, Shandong Agricultural University, Tai'an 271018, China
b
Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
c
Department of Natural History, Royal Ontario Museum, 100 Queen's Park, Toronto, ON M5S 2C6 Canada
d
College of Life Sciences, Shandong Agricultural University, Tai'an 271018, China

More Information

Corresponding author: E-mail address: huangdw@ioz.ac.cn (Dawei Huang)
Received Date: 2008-05-31
Accepted Date: 2008-10-20
Rev Recd Date: 2008-10-17

Available Online: 2008-12-23

Publish Date: 2008-12-20

Abstract

Abstract

Codon usage bias varies considerably among genomes and even within the genes of the same genome. In eukaryotic organisms, energy production in the form of oxidative phosphorylation (OXPHOS) is the only process under control of both nuclear and mitochondrial genomes. Although factors affecting codon usage in a single genome have been studied, this has not occurred when both interactional genomes are involved. Consequently, we investigated whether or not other factors influence codon usage of coevolved genes. We used Drosophila melanogaster as a model organism. Our χ² test on the number of codons of nuclear and mitochondrial genes involved in the OXPHOS system was significantly different (χ² = 7945.16, P < 0.01). A plot of effective number of codons against GC3s content of nuclear genes showed that few genes lie on the expected curve, indicating that codon usage was random. Correspondence analysis indicated a significant correlation between axis 1 and codon adaptation index ( R = 0.947, P < 0.01) in every nuclear gene sequence. Thus, codon usage bias of nuclear genes appeared to be affected by translational selection. Correlation between axis 1 coordinates and GC content ( R = 0.814, P < 0.01) indicated that the codon usage of nuclear genes was also affected by GC composition. Analysis of mitochondrial genes did not reveal a significant correlation between axis 1 and any parameter. Statistical analyses indicated that codon usages of both nDNA and mtDNA were subjected to context-dependent mutations.
- oxidative phosphorylation,
- nDNA,
- mtDNA,
- codon usage

These authors contributed equally to this work.

FullText(HTML)

References(34)

References

[1]	Barrientos, A., Muller, S., Dey, R. et al. Cytochrome c oxidase assembly in primates is sensitive to small evolutionary variations in amino acid sequence Mol. Biol. Evol., 17 (2000),pp. 1508-1519
[2]	Bayona-Bafaluy, M.P., Muller, S., Moraes, C.T. Fast adaptive coevolution of nuclear and mitochondrial subunits of ATP synthetase in orangutan Mol. Biol. Evol., 22 (2005),pp. 716-724
[3]	Carbone, A., Zinovyev, A., Kepes, F. Codon adaptation index as a measure of dominating codon bias Bioinformatics, 19 (2003),pp. 2005-2015
[4]	D'Elia, D., Catalano, D., Licciulli, F. et al. Mitochondrion, 6 (2006),pp. 252-257
[5]	De Grassi, A., Caggese, C., D'Elia, D. et al. Evolution of nuclearly encoded mitochondrial genes in Metazoa Gene, 354 (2005),pp. 181-188
[6]	Dey, R., Barrientos, A., Moraes, C.T. Functional constraints of nuclear-mitochondrial DNA interactions in xenomitochondrial rodent cell lines J. Biol. Chem., 275 (2000),pp. 31520-31527
[7]	Eyre-Walker, A. Mol. Biol. Evol., 13 (1996),pp. 864-872
[8]	Garesse, R., Vallejo, C.G. Animal mitochondrial biogenesis and function: A regulatory cross-talk between two genomes Gene, 263 (2001),pp. 1-16
[9]	Grossman, L.I., Wildman, D.E., Schmidt, T.R. et al. Accelerated evolution of the electron transport chain in anthropoid primates Trends Genet., 20 (2004),pp. 578-585
[10]	Gupta, S.K., Ghosh, T.C. Gene, 273 (2001),pp. 63-70
[11]	Jia, W., Higgs, P.G. Codon usage in mitochondrial genomes: Distinguishing context-dependent mutation from translational selection Mol. Biol. Evol., 25 (2008),pp. 339-351
[12]	Kliman, R.M., Hey, J. Mol. Biol. Evol., 10 (1993),pp. 1239-1258
[13]	Liu, Q., Feng, Y., Xue, Q. Mitochondrion, 4 (2004),pp. 313-320
[14]	Liu, Q., Dou, S., Ji, Z. et al. Biosystems, 80 (2005),pp. 123-131
[15]	Marais, G., Mouchiroud, D., Duret, L. Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes Proc. Natl. Acad. Sci. USA, 98 (2001),pp. 5688-5692
[16]	Moriyama, E.N., Powell, J.R. Nucleic Acids Res., 26 (1998),pp. 3188-3193
[17]	Naya, H., Romero, H., Carels, N. et al. FEBS Lett., 501 (2001),pp. 127-130
[18]	Novembre, J.A. Accounting for background nucleotide composition when measuring codon usage bias Mol. Biol. Evol., 19 (2002),pp. 1390-1394
[19]	Peixoto, L., Zavala, A., Romero, H. et al. Gene, 320 (2003),pp. 109-116
[20]	Powell, J.R., Moriyama, E.N. Proc. Natl. Acad. Sci. USA, 94 (1997),pp. 7784-7790
[21]	Romero, H., Zavala, A., Musto, H. et al. The influence of translational selection on codon usage in fishes from the family Cyprinidae Gene, 317 (2003),pp. 141-147
[22]	Sardiello, M., Licciulli, F., Catalano, D. et al. Nucleic Acids Res., 31 (2003),pp. 322-324
[23]	Sardiello, M., Tripoli, G., Romito, A. et al. Energy biogenesis: One key for coordinating two genomes Trends Genet., 21 (2005),pp. 12-16
[24]	Sau, K., Gupta, S.K., Sau, S. et al. Factors influencing synonymous codon and amino acid usage biases in Mimivirus Biosystems, 85 (2006),pp. 107-113
[25]	Sharp, P.M., Li, W.-H. The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications Nucleic Acids Res., 15 (1987),pp. 1281-1295
[26]	Sharp, P.M., Tuohy, T.M.F., Mosurski, K.R. Codon usage in yeast: Cluster analysis clearly differentiates highly and lowly expressed genes Nucleic Acids Res., 14 (1986),pp. 5125-5143
[27]	van den Heuvel, L.P., Smeitink, J.A., Rodenburg, R.J.T. Biochemical examination of fibroblasts in the diagnosis and research of oxidative phosphorylation (OXPHOS) defects Mitochondrion, 4 (2004),pp. 395-401
[28]	Wolstenholme, D.R., Clary, D.O. Genetics, 109 (1985),pp. 725-744
[29]	Wright, F. The ‘effective number of codons’ used in a gene Gene, 87 (1990),pp. 23-29
[30]	Wu, G., Culley, D.E., Zhang, W. Microbiology, 151 (2005),pp. 2175-2187
[31]	Xia, X. Maximizing transcription efficiency causes codon usage bias Genetics, 144 (1996),pp. 1309-1320
[32]	Xia, X. Mutation and selection on the anticodon of tRNA genes in vertebrate mitochondrial genomes Gene, 345 (2005),pp. 13-20
[33]	Xia, X. An improved implementation of codon adaptation index Evolutionary Bioinformatics, 3 (2007),pp. 53-58
[34]	Xia, X., Xie, Z. DAMBE: Software package for data analysis in molecular biology and evolution J. Hered., 92 (2001),pp. 371-373