Differential Use of Termination Codons in Ciliated Protozoa

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1989 May 1

PMID 2470096

Citations 25

Authors

D S Harper

C L Jahn

Affiliations

Soon will be listed here.

Abstract

Sequence analysis of genes in four species of ciliated protozoa and analysis of tRNAs in Tetrahymena has demonstrated that TAG and TAA encode glutamine or glutamic acid in these organisms and TGA is the only stop codon. Thus, it has generally been assumed that all ciliates use a nonuniversal genetic code in which TGA acts as the sole termination codon. We have sequenced the linear DNA molecules that carry an actin gene and a beta-tubulin gene from the ciliate Euplotes crassus. These genes are shown to use TAA as a termination codon based on homology to known actin and beta-tubulin gene sequences. In addition, we have sequenced a portion of the 3' terminus of the E. crassus H4 histone gene and show that it also uses TAA as a termination codon. These data indicate that the timing of genetic code changes in the ciliates must be reconsidered.

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Sequencing of random Euplotes crassus macronuclear genes supports a high frequency of +1 translational frameshifting.

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References

Hattori M, Sakaki Y . Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986; 152(2):232-8. DOI: 10.1016/0003-2697(86)90403-3. View

Hirono M, Endoh H, Okada N, Numata O, Watanabe Y . Tetrahymena actin. Cloning and sequencing of the Tetrahymena actin gene and identification of its gene product. J Mol Biol. 1987; 194(2):181-92. DOI: 10.1016/0022-2836(87)90367-6. View

Osawa S, Jukes T . Evolution of the genetic code as affected by anticodon content. Trends Genet. 1988; 4(7):191-8. DOI: 10.1016/0168-9525(88)90075-3. View

Kumazaki T, Hori H, Osawa S . Phylogeny of protozoa deduced from 5S rRNA sequences. J Mol Evol. 1983; 19(6):411-9. DOI: 10.1007/BF02102316. View

Greslin A, Loukin S, Oka Y, Prescott D . An analysis of the macronuclear actin genes of Oxytricha. DNA. 1988; 7(8):529-36. DOI: 10.1089/dna.1.1988.7.529. View

Miceli C, La Terza A, Melli M . Isolation and structural characterization of cDNA clones encoding the mating pheromone Er-1 secreted by the ciliate Euplotes raikovi. Proc Natl Acad Sci U S A. 1989; 86(9):3016-20. PMC: 287055. DOI: 10.1073/pnas.86.9.3016. View

Gorovsky M . Genome organization and reorganization in Tetrahymena. Annu Rev Genet. 1980; 14:203-39. DOI: 10.1146/annurev.ge.14.120180.001223. View

Cupples C, Pearlman R . Isolation and characterization of the actin gene from Tetrahymena thermophila. Proc Natl Acad Sci U S A. 1986; 83(14):5160-4. PMC: 323910. DOI: 10.1073/pnas.83.14.5160. View

Helftenbein E . Nucleotide sequence of a macronuclear DNA molecule coding for alpha-tubulin from the ciliate Stylonychia lemnae. Special codon usage: TAA is not a translation termination codon. Nucleic Acids Res. 1985; 13(2):415-33. PMC: 341005. DOI: 10.1093/nar/13.2.415. View

10.

Youngblom J, Schloss J, Silflow C . The two beta-tubulin genes of Chlamydomonas reinhardtii code for identical proteins. Mol Cell Biol. 1984; 4(12):2686-96. PMC: 369278. DOI: 10.1128/mcb.4.12.2686-2696.1984. View

11.

Messing J, Crea R, Seeburg P . A system for shotgun DNA sequencing. Nucleic Acids Res. 1981; 9(2):309-21. PMC: 326694. DOI: 10.1093/nar/9.2.309. View

12.

Sogin M, Swanton M, Gunderson J, Elwood H . Sequence of the small subunit ribosomal RNA gene from the hypotrichous ciliate Euplotes aediculatus. J Protozool. 1986; 33(1):26-9. DOI: 10.1111/j.1550-7408.1986.tb05550.x. View

13.

Yao M, Gorovsky M . Comparison of the sequences of macro- and micronuclear DNA of Tetrahymena pyriformis. Chromosoma. 1974; 48(1):1-18. DOI: 10.1007/BF00284863. View

14.

Messing J . New M13 vectors for cloning. Methods Enzymol. 1983; 101:20-78. DOI: 10.1016/0076-6879(83)01005-8. View

15.

VALLE R, Morch M . Stop making sense: or Regulation at the level of termination in eukaryotic protein synthesis. FEBS Lett. 1988; 235(1-2):1-15. PMC: 7130263. DOI: 10.1016/0014-5793(88)81225-0. View

16.

Ikemura T, Ozeki H . Codon usage and transfer RNA contents: organism-specific codon-choice patterns in reference to the isoacceptor contents. Cold Spring Harb Symp Quant Biol. 1983; 47 Pt 2:1087-97. DOI: 10.1101/sqb.1983.047.01.123. View

17.

PREER Jr J, Preer L, Rudman B, Barnett A . Deviation from the universal code shown by the gene for surface protein 51A in Paramecium. Nature. 1985; 314(6007):188-90. DOI: 10.1038/314188a0. View

18.

Tabor S, Richardson C . DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987; 84(14):4767-71. PMC: 305186. DOI: 10.1073/pnas.84.14.4767. View

19.

Horowitz S, Gorovsky M . An unusual genetic code in nuclear genes of Tetrahymena. Proc Natl Acad Sci U S A. 1985; 82(8):2452-5. PMC: 397576. DOI: 10.1073/pnas.82.8.2452. View

20.

Caron F, Meyer E . Does Paramecium primaurelia use a different genetic code in its macronucleus?. Nature. 1985; 314(6007):185-8. DOI: 10.1038/314185a0. View