• 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 6, 1994; 91(25): 12150–12154.
PMCID: PMC45394

De novo synthesis of an intron by the maize transposable element Dissociation.

Abstract

The mechanisms by which introns are gained or lost in the evolution of eukaryotic genes remain poorly understood. The discovery that transposable elements sometimes alter RNA splicing to allow partial or imperfect removal of the element from the primary transcripts suggests that transposons are a potential and continuing source of new introns. To date, splicing events that precisely restore the wild-type RNA sequence at the site of insertion have not been detected. Here we describe alternative RNA splicing patterns that result in precise removal of a Dissociation (Ds) insertion and one copy of its eight-nucleotide host site duplication from an exon sequence of the maize shrunken2-mutabe1 (sh2-m1) mutant. In one case, perfect splicing of Ds was associated with aberrant splicing of an intron located 32 bp upstream of the insertion site. The second transcript type was indistinguishable from wild-type mRNA, indicating that Ds was spliced like a normal intron in about 2% of the sh2-m1 transcripts. Our results suggest that the transposition of Ds into sh2 in 1968, in effect, marked the creation of a new intron in a modern eukaryotic gene. The possibility of precise intron formation by a transposable element demonstrated here may be a general phenomenon of intron formation, since consensus intron splice sites can be explained by insertions that duplicate host sequences upon integration. A model is presented.

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 (1.1M), 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.
  • Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. [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]
  • 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]
  • Cavalier-Smith T. Selfish DNA and the origin of introns. Nature. 1985 May 23;315(6017):283–284. [PubMed]
  • Bhave MR, Lawrence S, Barton C, Hannah LC. Identification and molecular characterization of shrunken-2 cDNA clones of maize. Plant Cell. 1990 Jun;2(6):581–588. [PMC free article] [PubMed]
  • Hannah LC, Nelson OE. Characterization of adenosine diphosphate glucose pyrophosphorylases from developing maize seeds. Plant Physiol. 1975 Feb;55(2):297–302. [PMC free article] [PubMed]
  • Varagona MJ, Purugganan M, Wessler SR. Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell. 1992 Jul;4(7):811–820. [PMC free article] [PubMed]
  • Wessler SR, Baran G, Varagona M. The maize transposable element Ds is spliced from RNA. Science. 1987 Aug 21;237(4817):916–918. [PubMed]
  • Kim HY, Schiefelbein JW, Raboy V, Furtek DB, Nelson OE., Jr RNA splicing permits expression of a maize gene with a defective Suppressor-mutator transposable element insertion in an exon. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5863–5867. [PMC free article] [PubMed]
  • Simon R, Starlinger P. Transposable element Ds2 of Zea mays influences polyadenylation and splice site selection. Mol Gen Genet. 1987 Aug;209(1):198–199. [PubMed]
  • Paszkowski J, Peterhans A, Bilang R, Filipowicz W. Expression in transgenic tobacco of the bacterial neomycin phosphotransferase gene modified by intron insertions of various sizes. Plant Mol Biol. 1992 Aug;19(5):825–836. [PubMed]
  • Schwarz-Sommer Z, Gierl A, Cuypers H, Peterson PA, Saedler H. Plant transposable elements generate the DNA sequence diversity needed in evolution. EMBO J. 1985 Mar;4(3):591–597. [PMC free article] [PubMed]
  • Church GM, Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. [PMC free article] [PubMed]
  • Shaw JR, Hannah LC. Genomic Nucleotide Sequence of a Wild-Type Shrunken-2 Allele of Zea mays. Plant Physiol. 1992 Mar;98(3):1214–1216. [PMC free article] [PubMed]
  • Varagona M, Wessler SR. Implications for the cis-requirements for Ds transposition based on the sequence of the wxB4 Ds element. Mol Gen Genet. 1990 Feb;220(3):414–418. [PubMed]
  • Hannah LC, Tuschall DM, Mans RJ. Multiple forms of maize endosperm adp-glucose pyrophosphorylase and their control by shrunken-2 and brittle-2. Genetics. 1980 Aug;95(4):961–970. [PMC free article] [PubMed]
  • Wessler SR. The splicing of maize transposable elements from pre-mRNA--a minireview. Gene. 1989 Oct 15;82(1):127–133. [PubMed]
  • Callis J, Fromm M, Walbot V. Introns increase gene expression in cultured maize cells. Genes Dev. 1987 Dec;1(10):1183–1200. [PubMed]
  • Vasil V, Clancy M, Ferl RJ, Vasil IK, Hannah LC. Increased gene expression by the first intron of maize shrunken-1 locus in grass species. Plant Physiol. 1989 Dec;91(4):1575–1579. [PMC free article] [PubMed]
  • McClintock B. The significance of responses of the genome to challenge. Science. 1984 Nov 16;226(4676):792–801. [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
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...