Letter to the Editor Codon Usage and the Origin of P Elements Jefsrey
R. Powell and Jennifer
Department
of Biology,
M. Gleason
Yale University
Codon usage in Drosophila is highly variable both from gene to gene within a species as well as within a gene between species (Shields et al. 1988; Starmer and Sullivan 1989; Sharp and Lloyd 1993). An extreme shift in codon usage for the same gene among species was (Adh) between documented for Alcohol dehydrogenase Drosophila melanogaster and Drosophila willistoni (Anderson, Carew, and Powell 1993). The major shift occurred for codons that are twofold redundant and can use C or U (T) in the third position. In D. melanogaster Adh, as well as generally in this species, the C-ending codons predominate, whereas in D. willistoni Adh, all such codon families shift to using predominantly U. Two more genes have now been sequenced in D. willistoni and at least based on these three genes, this shift seems to be characteristic of the species (table 1). While the transposable P element was first discovered in D. melanogaster, it has been strongly suggested that it may have originated in D. willistoni and have been acquired by D. melunogaster by horizontal transfer (Daniels et al. 1990; Kidwell 1993; Clark, Maddison, and Kidwell 1994). Here we ask the question as to whether the codon usage pattern of the one protein-coding gene in P elements (the transposase) is more similar to that characteristic of D. melanogaster or D. willistoni. Table 1 summarizes the patterns. The P element has a codon usage pattern more similar to D. willistoni than to D. melanogaster. It is important to point out that the data for the P element shown in this table is for a copy isolated from D. meZunogaster; P element sequences in D. willistoni are greater than 99% identical at the nucleotide level (Clark, Maddison, and Kidwell 1994), so codon usage for copies from this latter species is virtually identical. For the six amino acids with two codons that differ by ending in C or U the sample sizes are sufficient to perform statistical tests (G-tests) to determine if the genes differ significantly in codon usage. (Amino acids with more than two codons often have cells with zeros and it is not clear how to combine cells, so we have not performed similar tests for these cases.) Table 2 shows the results. P element codon usage is Key words: codon usage bias, Drosophila willistoni, P elements, horizontal transfer. Address for correspondence and reprints: Jeffrey R. Powell, Department of Biology, Yale University, New Haven, Connecticut 065208104; e-mail:
[email protected]. Mol. Biol. Evol. 13(1):278-279. 1996 0 1996 by the Society for Molecular Biology and Evolution.
ISSN: 0737-4038
often significantly different from genes in D. melanogaster, especially the gene with the largest sample of codons (per), while it is in no case significantly different from the codon usage of the three D. willistoni genes. The “signature” of D. willistoni codon usage, the shift to U-ending codons at twofold degenerate sites, is evident in the P element. This shift can also occur when C and U are redundant in the first position as for Leu (table 1). Again, both the D. willistoni genes and the P element use Ubeginning Leu codons very frequently, whereas they are rarely used in D. melanogaster. Other amino acids support the similarity between P elements and D. willistoni
Table 1 Codon usage for D. willistoni and D. mehogaster D. AMINO ACID CODON Adh’ Tyr..
Asn
3
5 25
34% 64%
0 0
15 10
19 7
CAC
3
1 7
4 29
34% 66%
8 1
18 14
9 6
. . AAU
2 14
3 4
10 27
42% 58%
7 3
35 19
34 14
5 7
5 5
11 38
52% 48%
7 2
31 16
32 21
8
0 5
2 15
33% 67%
2 3
22 15
23 14
0 2
0 6
6 28
27% 73%
0 3
10 6
6 9
9 14 0
5 4 0
9 22 9
32% 52% 16%
6 4 0
15 7 12
31 7 16
0 3 0 20 0 4 6 8 5 0
1 1 0 5 0 0 6 14 4 1
4 14 3 33 0 3 17 71 41 17
9% 16% 8% 45% 4% 18% 23% 43% 28% 6%
0 0 1 4 0 2 8 12 7 0
8 9 17 13 9 16 46 41 22 6
10 8 5 9 22 20 8 7 13 4
. CAU
. . GAU . . UUU uuc
Cys
. . UGU UGC
Ile
. . . AUU AUC AUA
Leu
Gly
ELE-
pe13
GAC Phe
P
WILLISTONI
1 0
. UAU
AAC Asp
D.
Overall4
UAC His..
MELANOGASTER
. . CUU
..
cut CUA CUG UUA UUG GGU GGC GGA GGG
So&
Adh5 So&
peP MENT~
Nom-Genes are Adh = alcohol dehydrogenase, Sod = superoxide dismutate, per = period. Numbers in the body of the table are the number of times each codon is used in that gene. “Overall” is for more than 250,000 codons available at the time of the review referenced. Sources of data: I Kreitman (1983); * Kwiatowski et al. (1994); 3 Citri et al. (1987); 4 Sharp and Lloyd (1993); 5 Anderson, Carew, and Powell (1993); 6 J. M. Gleason (unpublished); ’ Rio, Laski, and Rubin (1986).
278
Letter to the Editor
Table 2 Results of G-tests
AMINO
ACID
Tyr .............. His.. ............ Asn ............. Asp ............. Phe .............. cys .............. Totals (U vs. C) ...
279
ments on an earlier draft of this paper, for which we are grateful. P ELEMENTVERSUS D. MELANOGASTER
P ELEMENTVERSUS D. WILLISTONI
LITERATURE CITED
Adh
Adh
Sod
ANDERSON, C., E. A. CAREW,
0.05 0.25 0.07
0.11 0.96 0.30 0.35
0.87
0.12
Sod
*
* 0.24
** ***
0.15 0.54
per
*** *** *** ***
*
***
O.-i2
0.10
***
***
per 0.32
0.81 0.52 0.56 0.64 0.63 0.86
Nom.-The analysis tests whether codon usage in the P element is statistically different from usage in genes from D. melanogaster and D. willistoni. Associated probability values are indicated. Underlined entries indicate Fisher’s exact probability for cases with zeros in cells. Blank entries indicate less than five amino acids, a sample size too small to make a legitimate test. Totals sum allU-ending andC-ending frequencies. * P < 0.05; ** P < 0.01; *** P < 0.001.
codon usage. Drosophila melanogaster rarely uses AUA for isoleucine, yet this codon is very common in the P element and per from D. willistoni. The most commonly used codon for glycine in D. melanogaster (GGC) is never the most commonly used in D. willistoni nor in the P element. We can only conclude that codon usage in the P element is more similar to that in D. willistoni than in D. melanogaster. Assuming that transposable elements and the genomes in which they reside are subject to similar selection for codon usage and/or mutation bias, this observation supports the contention that the P element has a longer evolutionary history in D. willistoni than in D. melanogaster and, therefore, is added evidence supporting the hypothesis of horizontal transfer from D. willistoni to D. melanogaster. Based on whether hybrid dysgenesis is induced by males from strains collected from nature at different times, D. melanogaster probably acquired P elements about 45 years ago (Kidwell 1983). Assuming 10-20 generations per year, this implies that 450-900 generations have not been sufficient for the P element to evolve a codon usage pattern more similar to its new “host.”
and J. R. POWELL. 1993. Evolution of the Adh locus in the Drosophila willistoni group: the loss of an intron, and shift in codon usage. Mol. Biol. Evol.
10:605-6
18.
CITRI, Y., H. V. COLOT, A. C. JACQUIER, Q. Yu,
A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene. Nature 326:4247. CLARK, J. B., W. P MADDISON, and M. G. KIDWELL. 1994. Phylogenetic analysis supports horizontal transfer of P transposable elements. Mol. Biol. Evol. 11:40-50. DANIELS, S. B., K. R. PETERSON,L. D. STRAUSBAUGH,M. G. KIDWELL,and A. CHOVNICK. 1990. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124~339-355. KIDWELL, M. G. 1983. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 80: 1655-1659. -. 1993. Lateral transfer in natural populations of eukaryotes. Annu. Rev. Genet. 27:235-256. KREITMAN, M. 1983. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304:412-417. KWIATOWSKI,J., D. SKARECKY, K. BAILEY, and E J. AYALA. 1994. Phylogeny of Drosophila and related genera inferred from the nucleotide sequence of the Cu, Zn, Sod gene. J. Mol. Evol. 38:443-454. RIO, D. C., E A. LAW, and G. M. RUBIN. 1986. Identification and immunochemical analysis of biologicaly active Drosophila P element transposase. Cell 44:21-32. SHARP, P M., and A. T LLOYD. 1993. Codon usage. Pp. 378397 in G. MARONI, ed. An atlas of Drosophila genes: sequences and molecular features. Oxford University Press, New York. SHIELDS,D. C., P M. SHARP, D. G. HIGGINS, and
E WRIGHT.
“Silent” sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol. Biol. Evol. 5:704-7 16. STARMER,W. T. and D. T. SULLIVAN.1989. A shift in the thirdcodon-position nucleotide frequency in alcohol dehydrogenase genes in the genus Drosophila. Mol. Biol. Evol. 6: 546-552. 1988.
Acknowledgments DANIEL L. HARTL,
This work was supported by NSF Grant DEB 9318836 to J.R.I? and a Dissertation Improvement Grant DEB 924749 to J.M.G. Etsuko Moriyama made useful com-
J. C. HALL,
D. BALTIMORE, and M. ROSBASH. 1987.
Accepted
September
reviewing
1, 1995
editor
