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

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.

Authors

  • Logsdon, J M Jr, Logsdon JM Jr, Department of Biology, Indiana University, Bloomington 47405, USA.

  • Tyshenko, M G, Tyshenko MG,

  • Dixon, C, Dixon C,

  • D-Jafari, J, D-Jafari J,

  • Walker, V K, Walker VK,

  • Palmer, J D, Palmer JD,

YEAR OF PUBLICATION: 1995
SOURCE: Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8507-11. doi: 10.1073/pnas.92.18.8507.
JOURNAL TITLE ABBREVIATION: Proc Natl Acad Sci U S A
JOURNAL TITLE: Proceedings of the National Academy of Sciences of the United States of America
ISSN: 0027-8424 (Print) 1091-6490 (Electronic) 0027-8424 (Linking)
VOLUME: 92
ISSUE: 18
PAGES: 8507-11
PLACE OF PUBLICATION: United States
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.
LANGUAGE: eng
DATE OF PUBLICATION: 1995 Aug 29
DATE COMPLETED: 19951012
DATE REVISED: 20190501
MESH DATE: 2001/03/28 10:01
EDAT: 1995/08/29 00:00
STATUS: MEDLINE
PUBLICATION STATUS: ppublish
SECONDARY SOURCE ID: GENBANK/U23079||GENBANK/U23080||GENBANK/U23081
OWNER: NLM

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Michael G. Tyshenko

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Dr. Michael G. Tyshenko is a Senior Health Risk Analyst at Risk Sciences International (RSI), where he has contributed since 2018 to some of the organization’s most complex and cross-cutting public health risk projects. As RSI’s lead on chemical peer...
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