Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Aug 29, 1995; 92(18): 8507–8511.
PMCID: PMC41186

Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory.

Abstract

The gene encoding the glycolytic enzyme triose-phosphate isomerase (TPI; EC 5.3.1.1) has been central to the long-standing controversy on the origin and evolutionary significance of spliceosomal introns by virtue of its pivotal support for the introns-early view, or exon theory of genes. Putative correlations between intron positions and TPI protein structure have led to the conjecture that the gene was assembled by exon shuffling, and five TPI intron positions are old by the criterion of being conserved between animals and plants. We have sequenced TPI genes from three diverse eukaryotes--the basidiomycete Coprinus cinereus, the nematode Caenorhabditis elegans, and the insect Heliothis virescens--and have found introns at seven novel positions that disrupt previously recognized gene/protein structure correlations. The set of 21 TPI introns now known is consistent with a random model of intron insertion. Twelve of the 21 TPI introns appear to be of recent origin since each is present in but a single examined species. These results, together with their implication that as more TPI genes are sequenced more intron positions will be found, render TPI untenable as a paradigm for the introns-early theory and, instead, support the introns-late view that spliceosomal introns have been inserted into preexisting genes during eukaryotic evolution.

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 (1.2M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. [PubMed]
  • Darnell JE., Jr Implications of RNA-RNA splicing in evolution of eukaryotic cells. Science. 1978 Dec 22;202(4374):1257–1260. [PubMed]
  • Darnell JE, Doolittle WF. Speculations on the early course of evolution. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1271–1275. [PMC free article] [PubMed]
  • Gilbert W, Marchionni M, McKnight G. On the antiquity of introns. Cell. 1986 Jul 18;46(2):151–153. [PubMed]
  • Gilbert W. The exon theory of genes. Cold Spring Harb Symp Quant Biol. 1987;52:901–905. [PubMed]
  • Gilbert W, Glynias M. On the ancient nature of introns. Gene. 1993 Dec 15;135(1-2):137–144. [PubMed]
  • Cavalier-Smith T. Selfish DNA and the origin of introns. Nature. 1985 May 23;315(6017):283–284. [PubMed]
  • Palmer JD, Logsdon JM., Jr The recent origins of introns. Curr Opin Genet Dev. 1991 Dec;1(4):470–477. [PubMed]
  • Cavalier-Smith T. Intron phylogeny: a new hypothesis. Trends Genet. 1991 May;7(5):145–148. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Go M, Nosaka M. Protein architecture and the origin of introns. Cold Spring Harb Symp Quant Biol. 1987;52:915–924. [PubMed]
  • Tittiger C, Whyard S, Walker VK. A novel intron site in the triosephosphate isomerase gene from the mosquito Culex tarsalis. Nature. 1993 Feb 4;361(6411):470–472. [PubMed]
  • Doolittle WF, Stoltzfus A. Molecular evolution. Genes-in-pieces revisited. Nature. 1993 Feb 4;361(6411):403–403. [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]
  • 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]
  • Logsdon JM, Jr, Palmer JD. Origin of introns--early or late? Nature. 1994 Jun 16;369(6481):526–528. [PubMed]
  • Patthy L. Intron-dependent evolution: preferred types of exons and introns. FEBS Lett. 1987 Apr 6;214(1):1–7. [PubMed]
  • Rogers JH. How were introns inserted into nuclear genes? Trends Genet. 1989 Jul;5(7):213–216. [PubMed]
  • Rogers JH. The role of introns in evolution. FEBS Lett. 1990 Aug 1;268(2):339–343. [PubMed]
  • Stoltzfus A, Ford Doolittle W. Molecular evolution: slippery introns and globin gene evolution. Curr Biol. 1993 Apr 1;3(4):215–217. [PubMed]
  • Kwiatowski J, Krawczyk M, Kornacki M, Bailey K, Ayala FJ. Evidence against the exon theory of genes derived from the triose-phosphate isomerase gene. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8503–8506. [PMC free article] [PubMed]
  • Dibb NJ, Newman AJ. Evidence that introns arose at proto-splice sites. EMBO J. 1989 Jul;8(7):2015–2021. [PMC free article] [PubMed]
  • Mueller MW, Allmaier M, Eskes R, Schweyen RJ. Transposition of group II intron aI1 in yeast and invasion of mitochondrial genes at new locations. Nature. 1993 Nov 11;366(6451):174–176. [PubMed]
  • Giroux MJ, Clancy M, Baier J, Ingham L, McCarty D, Hannah LC. De novo synthesis of an intron by the maize transposable element Dissociation. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12150–12154. [PMC free article] [PubMed]
  • Stoltzfus A. Origin of introns--early or late. Nature. 1994 Jun 16;369(6481):526–528. [PubMed]
  • Kwiatowski J, Skarecky D, Ayala FJ. 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. [PubMed]
  • Bruns TD, Vilgalys R, Barns SM, Gonzalez D, Hibbett DS, Lane DJ, Simon L, Stickel S, Szaro TM, Weisburg WG, et al. Evolutionary relationships within the fungi: analyses of nuclear small subunit rRNA sequences. Mol Phylogenet Evol. 1992 Sep;1(3):231–241. [PubMed]
  • Leipe DD, Gunderson JH, Nerad TA, Sogin ML. Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol. 1993 May;59(1):41–48. [PubMed]
  • Baldauf SL, Palmer JD. Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11558–11562. [PMC free article] [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

  • MedGen
    MedGen
    Related information in MedGen
  • Nucleotide
    Nucleotide
    Published Nucleotide sequences
  • OMIM
    OMIM
    OMIM record citing PubMed
  • Protein
    Protein
    Published protein sequences
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links
  • Taxonomy
    Taxonomy
    Related taxonomy entry
  • Taxonomy Tree
    Taxonomy Tree

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...