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Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes.

Ragg H, Kumar A, Köster K, Bentele C, Wang Y, Frese MA, Prib N, Krüger O - BMC Evol. Biol. (2009)

Bottom Line: DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously.The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biotechnology, Faculty of Technology and Center for Biotechnology, University of Bielefeld, D-33501 Bielefeld, Germany. hr@zellkult.techfak.uni-bielefeld.de

ABSTRACT

Background: Intron gains reportedly are very rare during evolution of vertebrates, and the mechanisms underlying their creation are largely unknown. Previous investigations have shown that, during metazoan radiation, the exon-intron patterns of serpin superfamily genes were subject to massive changes, in contrast to many other genes.

Results: Here we investigated intron dynamics in the serpin superfamily in lineages pre- and postdating the split of vertebrates. Multiple intron gains were detected in a group of ray-finned fishes, once the canonical groups of vertebrate serpins had been established. In two genes, co-occurrence of non-standard introns was observed, implying that intron gains in vertebrates may even happen concomitantly or in a rapidly consecutive manner. DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.

Conclusion: Multiple intron acquisitions were identified in serpin genes of a lineage of ray-finned fishes, but not in any other vertebrates, suggesting that insertion rates for introns may be episodically increased. The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously. The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site. The association of intron gains in the serpin superfamily with a group of fishes that underwent genome compaction may indicate that DNA breakage/repair processes might foster intron birth.

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Alignment of angiotensinogen sequences and intron location analysis. Angiotensinogen sequences were aligned together with mature human α1-antitrypsin (A1) serving as reference protein. The following color code is used to characterize introns: red, standard introns; green, non-canonical introns exclusively present in Oryzias latipes, Gasterosteus aculeatus and Takifugu rubripes (Fugu), but not in lampreys (Petromyzon marinus, Lampetra fluviatilis), tetrapods (human, chicken) and Danio rerio. Positions and phases (a-c) of introns are depicted above the alignment and refer to human α1-antitrypsin. The angiotensin signature sequence is reproduced in white on pink background. Residues conserved in all sequences are printed in white on grey background.
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Figure 2: Alignment of angiotensinogen sequences and intron location analysis. Angiotensinogen sequences were aligned together with mature human α1-antitrypsin (A1) serving as reference protein. The following color code is used to characterize introns: red, standard introns; green, non-canonical introns exclusively present in Oryzias latipes, Gasterosteus aculeatus and Takifugu rubripes (Fugu), but not in lampreys (Petromyzon marinus, Lampetra fluviatilis), tetrapods (human, chicken) and Danio rerio. Positions and phases (a-c) of introns are depicted above the alignment and refer to human α1-antitrypsin. The angiotensin signature sequence is reproduced in white on pink background. Residues conserved in all sequences are printed in white on grey background.

Mentions: Inspection of lamprey serpin sequences disclosed the presence of angiotensinogen and heparin cofactor II (HCII), two prominent members of group V2. All known angiotensinogen proteins depict a conserved decapeptide sequence close to the N-terminus that, after controlled enzymatic cleavage, gives rise to formation of peptides (angiotensin I-IV) involved in blood pressure regulation and other important physiological processes [24]. Clearly, such a sequence is also present in angiotensinogen orthologues from L. fluviatilis and P. marinus (Figure 2). The NVIYFKG signature (positions 268–274 in L. fluviatilis), among other features, definitely reveals this protein as member of the serpin superfamily.


Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes.

Ragg H, Kumar A, Köster K, Bentele C, Wang Y, Frese MA, Prib N, Krüger O - BMC Evol. Biol. (2009)

Alignment of angiotensinogen sequences and intron location analysis. Angiotensinogen sequences were aligned together with mature human α1-antitrypsin (A1) serving as reference protein. The following color code is used to characterize introns: red, standard introns; green, non-canonical introns exclusively present in Oryzias latipes, Gasterosteus aculeatus and Takifugu rubripes (Fugu), but not in lampreys (Petromyzon marinus, Lampetra fluviatilis), tetrapods (human, chicken) and Danio rerio. Positions and phases (a-c) of introns are depicted above the alignment and refer to human α1-antitrypsin. The angiotensin signature sequence is reproduced in white on pink background. Residues conserved in all sequences are printed in white on grey background.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2746811&req=5

Figure 2: Alignment of angiotensinogen sequences and intron location analysis. Angiotensinogen sequences were aligned together with mature human α1-antitrypsin (A1) serving as reference protein. The following color code is used to characterize introns: red, standard introns; green, non-canonical introns exclusively present in Oryzias latipes, Gasterosteus aculeatus and Takifugu rubripes (Fugu), but not in lampreys (Petromyzon marinus, Lampetra fluviatilis), tetrapods (human, chicken) and Danio rerio. Positions and phases (a-c) of introns are depicted above the alignment and refer to human α1-antitrypsin. The angiotensin signature sequence is reproduced in white on pink background. Residues conserved in all sequences are printed in white on grey background.
Mentions: Inspection of lamprey serpin sequences disclosed the presence of angiotensinogen and heparin cofactor II (HCII), two prominent members of group V2. All known angiotensinogen proteins depict a conserved decapeptide sequence close to the N-terminus that, after controlled enzymatic cleavage, gives rise to formation of peptides (angiotensin I-IV) involved in blood pressure regulation and other important physiological processes [24]. Clearly, such a sequence is also present in angiotensinogen orthologues from L. fluviatilis and P. marinus (Figure 2). The NVIYFKG signature (positions 268–274 in L. fluviatilis), among other features, definitely reveals this protein as member of the serpin superfamily.

Bottom Line: DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously.The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biotechnology, Faculty of Technology and Center for Biotechnology, University of Bielefeld, D-33501 Bielefeld, Germany. hr@zellkult.techfak.uni-bielefeld.de

ABSTRACT

Background: Intron gains reportedly are very rare during evolution of vertebrates, and the mechanisms underlying their creation are largely unknown. Previous investigations have shown that, during metazoan radiation, the exon-intron patterns of serpin superfamily genes were subject to massive changes, in contrast to many other genes.

Results: Here we investigated intron dynamics in the serpin superfamily in lineages pre- and postdating the split of vertebrates. Multiple intron gains were detected in a group of ray-finned fishes, once the canonical groups of vertebrate serpins had been established. In two genes, co-occurrence of non-standard introns was observed, implying that intron gains in vertebrates may even happen concomitantly or in a rapidly consecutive manner. DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.

Conclusion: Multiple intron acquisitions were identified in serpin genes of a lineage of ray-finned fishes, but not in any other vertebrates, suggesting that insertion rates for introns may be episodically increased. The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously. The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site. The association of intron gains in the serpin superfamily with a group of fishes that underwent genome compaction may indicate that DNA breakage/repair processes might foster intron birth.

Show MeSH