Abstract
The exon theory of genes proposes that the introns of protein-encoding nuclear genes are remnants of the DNA spacers between ancient minigenes. The discovery of an intron at a predicted position in the triose-phosphate isomerase (EC 5.3.1.1) gene of Culex mosquitoes has been hailed as an evidential pillar of the theory. We have found that that intron is also present in Aedes mosquitoes, which are closely related to Culex, but not in the phylogenetically more distant Anopheles, nor in the fly Calliphora vicina, nor in the moth Spodoptera littoralis. The presence of this intron in Culex and Aedes is parsimoniously explained as the result of an insertion in a recent common ancestor of these two species rather than as the remnant of an ancient intron. The absence of the intron in 19 species of very diverse organisms requires at least 10 independent evolutionary losses in order to be consistent with the exon theory.
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Selected References
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- Alber T., Kawasaki G. Nucleotide sequence of the triose phosphate isomerase gene of Saccharomyces cerevisiae. J Mol Appl Genet. 1982;1(5):419–434. [PubMed] [Google Scholar]
- Darnell J. E., Jr Implications of RNA-RNA splicing in evolution of eukaryotic cells. Science. 1978 Dec 22;202(4374):1257–1260. doi: 10.1126/science.364651. [DOI] [PubMed] [Google Scholar]
- Doolittle R. F. Counting and discounting the universe of exons. Science. 1991 Aug 9;253(5020):677–680. doi: 10.1126/science.1871603. [DOI] [PubMed] [Google Scholar]
- Dorit R. L., Schoenbach L., Gilbert W. How big is the universe of exons? Science. 1990 Dec 7;250(4986):1377–1382. doi: 10.1126/science.2255907. [DOI] [PubMed] [Google Scholar]
- Gilbert W., Glynias M. On the ancient nature of introns. Gene. 1993 Dec 15;135(1-2):137–144. doi: 10.1016/0378-1119(93)90058-b. [DOI] [PubMed] [Google Scholar]
- Gilbert W., Marchionni M., McKnight G. On the antiquity of introns. Cell. 1986 Jul 18;46(2):151–153. doi: 10.1016/0092-8674(86)90730-0. [DOI] [PubMed] [Google Scholar]
- Gilbert W. The exon theory of genes. Cold Spring Harb Symp Quant Biol. 1987;52:901–905. doi: 10.1101/sqb.1987.052.01.098. [DOI] [PubMed] [Google Scholar]
- Hawkins J. D. A survey on intron and exon lengths. Nucleic Acids Res. 1988 Nov 11;16(21):9893–9908. doi: 10.1093/nar/16.21.9893. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
- Hurst L. D. Molecular evolution. The uncertain origin of introns. Nature. 1994 Sep 29;371(6496):381–382. doi: 10.1038/371381a0. [DOI] [PubMed] [Google Scholar]
- Kao W. Y., Trewitt P. M., Bergtrom G. Intron-containing globin genes in the insect Chironomus thummi. J Mol Evol. 1994 Mar;38(3):241–249. doi: 10.1007/BF00176086. [DOI] [PubMed] [Google Scholar]
- Kohl L., Callens M., Wierenga R. K., Opperdoes F. R., Michels P. A. Triose-phosphate isomerase of Leishmania mexicana mexicana. Cloning and characterization of the gene, overexpression in Escherichia coli and analysis of the protein. Eur J Biochem. 1994 Mar 1;220(2):331–338. doi: 10.1111/j.1432-1033.1994.tb18629.x. [DOI] [PubMed] [Google Scholar]
- Kwiatowski J., Skarecky D., Ayala F. J. Structure and sequence of the Cu,Zn Sod gene in the Mediterranean fruit fly, Ceratitis capitata: intron insertion/deletion and evolution of the gene. Mol Phylogenet Evol. 1992 Mar;1(1):72–82. doi: 10.1016/1055-7903(92)90037-h. [DOI] [PubMed] [Google Scholar]
- Logsdon J. M., Jr, Tyshenko M. G., Dixon C., D-Jafari J., Walker V. K., Palmer J. D. Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8507–8511. doi: 10.1073/pnas.92.18.8507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marchionni M., Gilbert W. The triosephosphate isomerase gene from maize: introns antedate the plant-animal divergence. Cell. 1986 Jul 4;46(1):133–141. doi: 10.1016/0092-8674(86)90867-6. [DOI] [PubMed] [Google Scholar]
- McKnight G. L., O'Hara P. J., Parker M. L. Nucleotide sequence of the triosephosphate isomerase gene from Aspergillus nidulans: implications for a differential loss of introns. Cell. 1986 Jul 4;46(1):143–147. doi: 10.1016/0092-8674(86)90868-8. [DOI] [PubMed] [Google Scholar]
- Mowatt M. R., Weinbach E. C., Howard T. C., Nash T. E. Complementation of an Escherichia coli glycolysis mutant by Giardia lamblia triosephosphate isomerase. Exp Parasitol. 1994 Feb;78(1):85–92. doi: 10.1006/expr.1994.1008. [DOI] [PubMed] [Google Scholar]
- Old S. E., Mohrenweiser H. W. Nucleotide sequence of the triosephosphate isomerase gene from Macaca mulatta. Nucleic Acids Res. 1988 Sep 26;16(18):9055–9055. doi: 10.1093/nar/16.18.9055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palmer J. D., Logsdon J. M., Jr The recent origins of introns. Curr Opin Genet Dev. 1991 Dec;1(4):470–477. doi: 10.1016/s0959-437x(05)80194-7. [DOI] [PubMed] [Google Scholar]
- Patthy L. Exons--original building blocks of proteins? Bioessays. 1991 Apr;13(4):187–192. doi: 10.1002/bies.950130408. [DOI] [PubMed] [Google Scholar]
- Ranie J., Kumar V. P., Balaram H. Cloning of the triosephosphate isomerase gene of Plasmodium falciparum and expression in Escherichia coli. Mol Biochem Parasitol. 1993 Oct;61(2):159–169. doi: 10.1016/0166-6851(93)90062-3. [DOI] [PubMed] [Google Scholar]
- Russell P. R. Transcription of the triose-phosphate-isomerase gene of Schizosaccharomyces pombe initiates from a start point different from that in Saccharomyces cerevisiae. Gene. 1985;40(1):125–130. doi: 10.1016/0378-1119(85)90031-9. [DOI] [PubMed] [Google Scholar]
- Shaw-Lee R. L., Lissemore J. L., Sullivan D. T. Structure and expression of the triose phosphate isomerase (Tpi) gene of Drosophila melanogaster. Mol Gen Genet. 1991 Nov;230(1-2):225–229. doi: 10.1007/BF00290672. [DOI] [PubMed] [Google Scholar]
- Smothers J. F., von Dohlen C. D., Smith L. H., Jr, Spall R. D. Molecular evidence that the myxozoan protists are metazoans. Science. 1994 Sep 16;265(5179):1719–1721. doi: 10.1126/science.8085160. [DOI] [PubMed] [Google Scholar]
- Sogin M. L. Early evolution and the origin of eukaryotes. Curr Opin Genet Dev. 1991 Dec;1(4):457–463. doi: 10.1016/s0959-437x(05)80192-3. [DOI] [PubMed] [Google Scholar]
- Stoltzfus A., Spencer D. F., Zuker M., Logsdon J. M., Jr, Doolittle W. F. Testing the exon theory of genes: the evidence from protein structure. Science. 1994 Jul 8;265(5169):202–207. doi: 10.1126/science.8023140. [DOI] [PubMed] [Google Scholar]
- Straus D., Gilbert W. Genetic engineering in the Precambrian: structure of the chicken triosephosphate isomerase gene. Mol Cell Biol. 1985 Dec;5(12):3497–3506. doi: 10.1128/mcb.5.12.3497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swinkels B. W., Gibson W. C., Osinga K. A., Kramer R., Veeneman G. H., van Boom J. H., Borst P. Characterization of the gene for the microbody (glycosomal) triosephosphate isomerase of Trypanosoma brucei. EMBO J. 1986 Jun;5(6):1291–1298. doi: 10.1002/j.1460-2075.1986.tb04358.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tittiger C., Whyard S., Walker V. K. A novel intron site in the triosephosphate isomerase gene from the mosquito Culex tarsalis. Nature. 1993 Feb 4;361(6411):470–472. doi: 10.1038/361470a0. [DOI] [PubMed] [Google Scholar]
- Xu Y., Harris-Haller L. W., McCollum J. C., Hardin S. H., Hall T. C. Nuclear gene encoding cytosolic triosephosphate isomerase from rice (Oryza sativa L.). Plant Physiol. 1993 Jun;102(2):697–697. doi: 10.1104/pp.102.2.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- dos Reis M. G., Davis R. E., Singh H., Skelly P. J., Shoemaker C. B. Characterization of the Schistosoma mansoni gene encoding the glycolytic enzyme, triosephosphate isomerase. Mol Biochem Parasitol. 1993 Jun;59(2):235–242. doi: 10.1016/0166-6851(93)90221-i. [DOI] [PubMed] [Google Scholar]