Molecular Biology and Evolution 17:467-468 (2000)
© 2000 Society for Molecular Biology and Evolution
Letter to the Editor |
Codon Usage and the Origin of P Elements
*Laboratoire Populations, Génétique et Evolution, Centre National de la Recherche Scientifique, Gif/Yvette, France;
and
Laboratoire Biométrie et Biologie Évolutive, Centre National de la Recherche Scientifique, Université de Lyon I, Villeurbanne, France
The authors of a recent comparison of the P transposable element and three genes of Drosophila melanogaster and Drosophila willistoni suggested that the codon usage of the D. melanogaster P element is similar to that of D. willistoni genes (Powell and Gleason 1996
). They concluded that this could be further evidence of the recent horizontal transfer of the P element from D. willistoni to D. melanogaster indicated by several previous findings (Clark and Kidwell 1997
). More specifically, it was shown that D. willistoni genes tend to be T-ending-codon genes, whereas those of D. melanogaster tend to be C-ending-codon genes. The transposase genes of the P elements from both species was found to be AT-ending-codon genes, and one explanation for this may be that the P element of D. melanogaster originated from D. willistoni. This hypothesis assumes that the codon usage in transposable elements (TEs) and that in the host genome are similar. However, analysis of a large number of genes and TEs in D. melanogaster suggests that the T-ending-codon feature of the P element could be a general characteristic of all TEs in Drosophila species and independent of the host genome (Shields and Sharp 1989
).
We extracted from the GenBank DNA sequence database the sequences of six genes common to D. melanogaster and D. willistoni: Alcohol dehydrogenase (Adh, M11290 and L08648), Amylase-related gene (amyrel, U69607 and AF039560), superoxide dismutase (SOD, Y00367 and L13281), xanthine dehydrogenase (Xdh, Y00307 and AF058985), glycerol 3 phosphate dehydrogenase (Gpdh, X80204 and L37038), and period (per, M30114 and U51055). The sequences of the last three genes have been only partially determined for D. willistoni. We therefore used only the homologous regions in both species to avoid bias due to differences in gene length (Moryiama and Powell 1998; Duret and Mouchiroud 1999
). P elements, which have been reported in distantly related Drosophila species, were also added. These elements were described in Drosophila bifasciata (Hagemann, Miller, and Pinkser 1992
), Drosophila subobscura (Paricio et al. 1991
), and Scaptomyza pallida (Simonelig and Anxolabéhère 1991
). All sequences of RNA (class I) and DNA (class II) elements described in the species previously mentioned were also used to compare P element features with those of other elements.
The relative codon frequencies were estimated for all sense codons (59 codons) for each gene and transposable element according to the formula
where nij is the number of codon j observed for the amino acid i, and si is the number of synonymous codons for the the amino acid i. The 59 columns of the matrix are the variables of a factorial correspondence analysis (FCA). Because relative and absolute codon frequencies can be sensitive to several biases (Perrière and Thioulouze, personal communication), FCA was also performed using absolute codon frequencies and relative synonymous codon usage (RSCU), frequently used for such analyses (see, e.g., Shields and Sharp 1989
). In all cases, the FCA gave similar topologies on the first two axes. Figure 1
shows a factor map crossing the first two axes when the relative frequencies given above are used.
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The first two axes accounted for 44% of the total variance (34% on the first axis and 10% on the second). The percentage of the variance explained by the remaining axes was very low, close to 1% for the third and fourth axes, respectively, and <1% for the other ones. Drosophila melanogaster and D. willistoni genes are clearly separated. The projection of the codons shows that GC-ending codons (gray ellipses) are more frequent in the D. melanogaster genes than in those of D. willistoni, which display several T-ending codons. The TEs (black spots) of different Drosophila species clearly display a higher frequency of AT-ending codons. Codon usage patterns of P elements from different species are similar and clearly differ from those of the host genes. Moreover, the codon usage variability among genes from different species is lower than that between genes and TEs within the same species. A MANOVA (Statistica, version 3.0b, StatSoft) using the coordinates of each point on the first two axes as variables shows that the difference observed between genes of D. melanogaster and D. willistoni is significant, with a P value of 7.34 x 10-4, while the difference between transposable elements and genes of D. melanogaster is significant, with a P value of <10-7.
The characteristics of the P element in D. willistoni described by Powell and Gleason (1996) could be a general feature of TEs in Drosophila, and not attributable to the host. This was suggested by a previous analysis of D. melanogaster (Shields and Sharp 1989
) and is confirmed by similarities in P elements from different hosts. Moreover, these elements and other DNA and RNA elements described for several Drosophila species group together in our analysis (black spots in fig. 1
).
These findings strongly suggest that codon usage cannot be employed to demonstrate horizontal transfers of TEs between Drosophila species. TEs and host genes may not be subject to the same constraints, but the possibility that the evolutions of these two entities are linked cannot be ruled out. For instance, the most frequent codon for the host gene could be the least frequent for TEs and vice versa. The only way to check this will be to analyze species using different codon usage strategies.
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Footnotes |
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Manolo Gouy, Reviewing Editor
1 Keywords: P element
transposable elements
Drosophila,
codon usage
horizontal transfer 
2 Address for correspondence and reprints: Pierre Capy, Laboratoire Populations, Génétique et Evolution, Centre National de la Recherche Scientifique, UPR 9034, Bât. 13, 91198 Gif/Yvette Cedex, France. E-mail: capy{at}pge.cnrs-gif.fr
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literature cited |
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 TOP literature cited |
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Clark, J. B., and M. G. Kidwell. 1997. A phylogenetic perspective on P transposable element evolution in Drosophila. Proc. Natl. Acad. Sci. USA 94:11428–11433.
Duret, L., and D. Mouchiroud. 1999. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis.. Proc. Natl. Acad. Sci. USA 96:4482–4487.
Hagemann, S., W. J. Miller, and W. Pinsker. 1992. Identification of a complete P element in the genome of Drosophila bifasciata. Nucleic Acids Res. 20:409–413.
Moriyama, E. N., and J. R. Powell. 1998. Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Res. 26:3188–3193.
Paricio, N., A. M. Perez-Alonso, M. J. Martinez-Sebastian, and R. Frutos. 1991. P sequences of Drosophila subobscura lack exon 3 and may encode a 66 kd repressor-like protein. Nucleic Acids Res. 19:6713–6718.
Powell, J. R., and J. M. Gleason. 1996. Codon usage and the origin of P elements. Mol. Biol. Evol. 13:278–279.[Web of Science][Medline]
Shields, D. C., and P. M. Sharp. 1989. Evidence that mutation patterns vary among Drosophila transposable elements. J. Mol. Biol. 207:843–846.[Web of Science][Medline]
Simonelig, M., and D. Anxolabéhère. 1991. A P element of Scaptomyza pallida is active in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 88:6102–6106.
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