• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Dec 19, 1995; 92(26): 12495–12499.
PMCID: PMC40384

Intron phase correlations and the evolution of the intron/exon structure of genes.

Abstract

Two issues in the evolution of the intron/exon structure of genes are the role of exon shuffling and the origin of introns. Using a large data base of eukaryotic intron-containing genes, we have found that there are correlations between intron phases leading to an excess of symmetric exons and symmetric exon sets. We interpret these excesses as manifestations of exon shuffling and make a conservative estimate that at least 19% of the exons in the data base were involved in exon shuffling, suggesting an important role for exon shuffling in evolution. Furthermore, these excesses of symmetric exons appear also in those regions of eukaryotic genes that are homologous to prokaryotic genes: the ancient conserved regions. This last fact cannot be explained in terms of the insertional theory of introns but rather supports the concept that some of the introns were ancient, the exon theory of genes.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Cavalier-Smith T. Intron phylogeny: a new hypothesis. Trends Genet. 1991 May;7(5):145–148. [PubMed]
  • Rogers J. Exon shuffling and intron insertion in serine protease genes. Nature. 1985 Jun 6;315(6019):458–459. [PubMed]
  • Rogers JH. How were introns inserted into nuclear genes? Trends Genet. 1989 Jul;5(7):213–216. [PubMed]
  • Gilbert W. The exon theory of genes. Cold Spring Harb Symp Quant Biol. 1987;52:901–905. [PubMed]
  • Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. [PubMed]
  • Gilbert W, Glynias M. On the ancient nature of introns. Gene. 1993 Dec 15;135(1-2):137–144. [PubMed]
  • Gilbert W, Marchionni M, McKnight G. On the antiquity of introns. Cell. 1986 Jul 18;46(2):151–153. [PubMed]
  • Go M. Correlation of DNA exonic regions with protein structural units in haemoglobin. Nature. 1981 May 7;291(5810):90–92. [PubMed]
  • Marchionni M, Gilbert W. The triosephosphate isomerase gene from maize: introns antedate the plant-animal divergence. Cell. 1986 Jul 4;46(1):133–141. [PubMed]
  • Nawrath C, Schell J, Koncz C. Homologous domains of the largest subunit of eucaryotic RNA polymerase II are conserved in plants. Mol Gen Genet. 1990 Aug;223(1):65–75. [PubMed]
  • Pardo JM, Serrano R. Structure of a plasma membrane H+-ATPase gene from the plant Arabidopsis thaliana. J Biol Chem. 1989 May 25;264(15):8557–8562. [PubMed]
  • Shah DM, Hightower RC, Meagher RB. Genes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not. J Mol Appl Genet. 1983;2(1):111–126. [PubMed]
  • Imajuku Y, Hirayama T, Endoh H, Oka A. Exon-intron organization of the Arabidopsis thaliana protein kinase genes CDC2a and CDC2b. FEBS Lett. 1992 Jun 8;304(1):73–77. [PubMed]
  • Iwabe N, Kuma K, Kishino H, Hasegawa M, Miyata T. Compartmentalized isozyme genes and the origin of introns. J Mol Evol. 1990 Sep;31(3):205–210. [PubMed]
  • Kersanach R, Brinkmann H, Liaud MF, Zhang DX, Martin W, Cerff R. Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature. 1994 Jan 27;367(6461):387–389. [PubMed]
  • Obaru K, Tsuzuki T, Setoyama C, Shimada K. Structural organization of the mouse aspartate aminotransferase isoenzyme genes. Introns antedate the divergence of cytosolic and mitochondrial isoenzyme genes. J Mol Biol. 1988 Mar 5;200(1):13–22. [PubMed]
  • Setoyama C, Joh T, Tsuzuki T, Shimada K. Structural organization of the mouse cytosolic malate dehydrogenase gene: comparison with that of the mouse mitochondrial malate dehydrogenase gene. J Mol Biol. 1988 Aug 5;202(3):355–364. [PubMed]
  • Logsdon JM, Jr, Palmer JD. Origin of introns--early or late? Nature. 1994 Jun 16;369(6481):526–528. [PubMed]
  • Stoltzfus A. Origin of introns--early or late. Nature. 1994 Jun 16;369(6481):526–528. [PubMed]
  • Stoltzfus A, Spencer DF, Zuker M, Logsdon JM, Jr, Doolittle WF. Testing the exon theory of genes: the evidence from protein structure. Science. 1994 Jul 8;265(5169):202–207. [PubMed]
  • Sharp PA. Speculations on RNA splicing. Cell. 1981 Mar;23(3):643–646. [PubMed]
  • Burks C, Cinkosky MJ, Gilna P, Hayden JE, Abe Y, Atencio EJ, Barnhouse S, Benton D, Buenafe CA, Cumella KE, et al. GenBank: current status and future directions. Methods Enzymol. 1990;183:3–22. [PubMed]
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. [PMC free article] [PubMed]
  • Green P, Lipman D, Hillier L, Waterston R, States D, Claverie JM. Ancient conserved regions in new gene sequences and the protein databases. Science. 1993 Mar 19;259(5102):1711–1716. [PubMed]
  • Fedorov A, Suboch G, Bujakov M, Fedorova L. Analysis of nonuniformity in intron phase distribution. Nucleic Acids Res. 1992 May 25;20(10):2553–2557. [PMC free article] [PubMed]
  • Patthy L. Intron-dependent evolution: preferred types of exons and introns. FEBS Lett. 1987 Apr 6;214(1):1–7. [PubMed]
  • Hodges D, Bernstein SI. Genetic and biochemical analysis of alternative RNA splicing. Adv Genet. 1994;31:207–281. [PubMed]
  • McKeown M. Alternative mRNA splicing. Annu Rev Cell Biol. 1992;8:133–155. [PubMed]
  • Palmer JD, Logsdon JM., Jr The recent origins of introns. Curr Opin Genet Dev. 1991 Dec;1(4):470–477. [PubMed]
  • Patthy L. Exons--original building blocks of proteins? Bioessays. 1991 Apr;13(4):187–192. [PubMed]
  • Stoltzfus A, Spencer DF, Zuker M, Logsdon JM, Jr, Doolittle WF. Testing the exon theory of genes: the evidence from protein structure. Science. 1994 Jul 8;265(5169):202–207. [PubMed]
  • Domon C, Steinmetz A. Exon shuffling in anther-specific genes from sunflower. Mol Gen Genet. 1994 Aug 2;244(3):312–317. [PubMed]
  • Wilson R, Ainscough R, Anderson K, Baynes C, Berks M, Bonfield J, Burton J, Connell M, Copsey T, Cooper J, et al. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994 Mar 3;368(6466):32–38. [PubMed]
  • Stephens RM, Schneider TD. Features of spliceosome evolution and function inferred from an analysis of the information at human splice sites. J Mol Biol. 1992 Dec 20;228(4):1124–1136. [PubMed]
  • Horowitz DS, Krainer AR. Mechanisms for selecting 5' splice sites in mammalian pre-mRNA splicing. Trends Genet. 1994 Mar;10(3):100–106. [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • PubMed
    PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...