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. 1986 Apr;83(7):2133–2137. doi: 10.1073/pnas.83.7.2133

Origin of eukaryotic introns: a hypothesis, based on codon distribution statistics in genes, and its implications.

P Senapathy
PMCID: PMC323245  PMID: 3457379

Abstract

A hypothesis for the origin of introns in eukaryotic genes is developed. By computer simulation it was found that the reading-frame lengths in a random nucleotide sequence are distributed in a negative exponential manner and that there exists an upper limit of about 200 codons in the length of the reading frames (RFs). These characteristics suggest that, if primordial DNA contained a random nucleotide sequence, the most primitive cells would have been under selective pressure to eliminate interfering stop codons in order to increase the length of RFs. Further, they indicate that the only possible way that a coding sequence that is considerably longer than 600 nucleotides could be derived from the short coding sequences occurring in a random sequence would be to splice the short coding sequences and to eliminate the stretches of sequences containing clusters of inframe stop codons. Thus, introns are suggested to be those stretches of sequences containing interfering stop codons that were originally earmarked in the first primitive cells to be eliminated in order to enable the coding for long polypeptides. Because the statistical characteristics of codon distributions in today's eukaryotic DNA sequences resemble closely those of a random sequence and because the upper limit in the length of RFs (200 codons) in a random sequence corresponds precisely to the observed maximum length of exons in today's eukaryotic genes (600 nucleotides), it is suggested that introns originated in the most primitive unicellular eukaryotes when they evolved from primordial sequences. The data from the prokaryotic gene sequences indicate that prokaryotic genes may have been derived originally from primitive unicellular eukaryotic genes by losing introns from them.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bernstein L. B., Mount S. M., Weiner A. M. Pseudogenes for human small nuclear RNA U3 appear to arise by integration of self-primed reverse transcripts of the RNA into new chromosomal sites. Cell. 1983 Feb;32(2):461–472. doi: 10.1016/0092-8674(83)90466-x. [DOI] [PubMed] [Google Scholar]
  2. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  3. Crick F. Split genes and RNA splicing. Science. 1979 Apr 20;204(4390):264–271. doi: 10.1126/science.373120. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  6. Gillies S. D., Morrison S. L., Oi V. T., Tonegawa S. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983 Jul;33(3):717–728. doi: 10.1016/0092-8674(83)90014-4. [DOI] [PubMed] [Google Scholar]
  7. Goff S. P., Gilboa E., Witte O. N., Baltimore D. Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell. 1980 Dec;22(3):777–785. doi: 10.1016/0092-8674(80)90554-1. [DOI] [PubMed] [Google Scholar]
  8. Leder A., Swan D., Ruddle F., D'Eustachio P., Leder P. Dispersion of alpha-like globin genes of the mouse to three different chromosomes. Nature. 1981 Sep 17;293(5829):196–200. doi: 10.1038/293196a0. [DOI] [PubMed] [Google Scholar]
  9. Mercola M., Wang X. F., Olsen J., Calame K. Transcriptional enhancer elements in the mouse immunoglobulin heavy chain locus. Science. 1983 Aug 12;221(4611):663–665. doi: 10.1126/science.6306772. [DOI] [PubMed] [Google Scholar]
  10. Naora H., Deacon N. J. Relationship between the total size of exons and introns in protein-coding genes of higher eukaryotes. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6196–6200. doi: 10.1073/pnas.79.20.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Schopf J. W., Oehler D. Z. How old are the eukaryotes? Science. 1976 Jul 2;193(4247):47–49. doi: 10.1126/science.193.4247.47. [DOI] [PubMed] [Google Scholar]
  12. Schwartz R. M., Dayhoff M. O. Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science. 1978 Jan 27;199(4327):395–403. doi: 10.1126/science.202030. [DOI] [PubMed] [Google Scholar]
  13. Tiemeier D. C., Tilghman S. M., Polsky F. I., Seidman J. G., Leder A., Edgell M. H., Leder P. A comparison of two cloned mouse beta-globin genes and their surrounding and intervening sequences. Cell. 1978 Jun;14(2):237–245. doi: 10.1016/0092-8674(78)90110-1. [DOI] [PubMed] [Google Scholar]

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