title: Intron-loss evolution of hatching enzyme genes in Teleostei.
abstract: BACKGROUND
  Hatching enzyme, belonging to the astacin metallo-protease family, digests egg envelope at embryo hatching. Orthologous genes of the enzyme are found in all vertebrate genomes. Recently, we found that exon-intron structures of the genes were conserved among tetrapods, while the genes of teleosts frequently lost their introns. Occurrence of such intron losses in teleostean hatching enzyme genes is an uncommon evolutionary event, as most eukaryotic genes are generally known to be interrupted by introns and the intron insertion sites are conserved from species to species. Here, we report on extensive studies of the exon-intron structures of teleostean hatching enzyme genes for insight into how and why introns were lost during evolution.
  
  
  RESULTS
  We investigated the evolutionary pathway of intron-losses in hatching enzyme genes of 27 species of Teleostei. Hatching enzyme genes of basal teleosts are of only one type, which conserves the 9-exon-8-intron structure of an assumed ancestor. On the other hand, otocephalans and euteleosts possess two types of hatching enzyme genes, suggesting a gene duplication event in the common ancestor of otocephalans and euteleosts. The duplicated genes were classified into two clades, clades I and II, based on phylogenetic analysis. In otocephalans and euteleosts, clade I genes developed a phylogeny-specific structure, such as an 8-exon-7-intron, 5-exon-4-intron, 4-exon-3-intron or intron-less structure. In contrast to the clade I genes, the structures of clade II genes were relatively stable in their configuration, and were similar to that of the ancestral genes. Expression analyses revealed that hatching enzyme genes were high-expression genes, when compared to that of housekeeping genes. When expression levels were compared between clade I and II genes, clade I genes tends to be expressed more highly than clade II genes.
  
  
  CONCLUSIONS
  Hatching enzyme genes evolved to lose their introns, and the intron-loss events occurred at the specific points of teleostean phylogeny. We propose that the high-expression hatching enzyme genes frequently lost their introns during the evolution of teleosts, while the low-expression genes maintained the exon-intron structure of the ancestral gene.
authors.affiliation: Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan.
authors.forename: Mari
authors.initials: M
authors.lastname: Kawaguchi
authors.forename: Junya
authors.initials: J
authors.lastname: Hiroi
authors.forename: Masaki
authors.initials: M
authors.lastname: Miya
authors.forename: Mutsumi
authors.initials: M
authors.lastname: Nishida
authors.forename: Ichiro
authors.initials: I
authors.lastname: Iuchi
authors.forename: Shigeki
authors.initials: S
authors.lastname: Yasumasu
mesh_terms: D000818:Animals; D019143:Evolution, Molecular; D005091:Exons / Q000235:genetics; D005399:Fishes / Q000145:classification* / Q000235:genetics*; D007438:Introns / Q000235:genetics*; D008666:Metalloendopeptidases / Q000235:genetics*; D008969:Molecular Sequence Data; D010802:Phylogeny
chemical_list: D008666:Metalloendopeptidases; C024344:envelysin
references.citation: Nucleic Acids Res. 1987 Sep 11;15(17):7155-74
references.pmid: 3658675
references.citation: Dev Growth Differ. 1997 Apr;39(2):191-7
references.pmid: 9108332
references.citation: Genome Res. 2007 Jan;17(1):23-32
references.pmid: 17108319
references.citation: Nucleic Acids Res. 2008 Mar;36(5):1703-12
references.pmid: 18263615
references.citation: J Exp Zool B Mol Dev Evol. 2009 Mar 15;312(2):95-107
references.pmid: 19025965
references.citation: J Biochem. 1989 Feb;105(2):204-11
references.pmid: 2656664
references.citation: J Comput Biol. 2008 Oct;15(8):981-1006
references.pmid: 18808330
references.citation: Bioinformatics. 2006 Nov 1;22(21):2688-90
references.pmid: 16928733
references.citation: Biochem Biophys Res Commun. 1989 Jul 14;162(1):58-63
references.pmid: 2751672
references.citation: Dev Biol. 1975 Apr;43(2):313-21
references.pmid: 1126562
references.citation: J Mol Evol. 2002 Jan;54(1):118-28
references.pmid: 11734905
references.citation: Cell. 1987 Apr 10;49(1):5-6
references.pmid: 3549000
references.citation: Mol Phylogenet Evol. 2003 Jun;27(3):476-88
references.pmid: 12742752
references.citation: Trends Genet. 2008 Aug;24(8):375-8
references.pmid: 18586348
references.citation: Mol Phylogenet Evol. 2004 Jul;32(1):274-86
references.pmid: 15186813
references.citation: Cell. 1981 Mar;23(3):643-6
references.pmid: 7226224
references.citation: Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10267-71
references.pmid: 10468597
references.citation: Dev Genes Evol. 2006 Dec;216(12):769-84
references.pmid: 17016731
references.citation: Dev Biol. 1992 Oct;153(2):250-8
references.pmid: 1397682
references.citation: FEBS J. 2008 Jun;275(11):2884-98
references.pmid: 18430023
references.citation: FEBS J. 2005 Sep;272(17):4315-26
references.pmid: 16128802
references.citation: Dev Genes Evol. 2005 Oct;215(10):489-98
references.pmid: 16003522
references.citation: Int J Dev Biol. 1997 Feb;41(1):19-25
references.pmid: 9074934
references.citation: Nat Rev Genet. 2006 Mar;7(3):211-21
references.pmid: 16485020
references.citation: Mol Biol Evol. 2008 Mar;25(3):526-35
references.pmid: 18089580
references.citation: Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8121-6
references.pmid: 12060758
references.citation: Dev Genes Evol. 2004 Apr;214(4):176-84
references.pmid: 15014992
references.citation: Zoolog Sci. 1996 Jun;13(3):331-40
references.pmid: 8987518
references.citation: Proc Natl Acad Sci U S A. 2005 Apr 19;102(16):5773-8
references.pmid: 15827119
references.citation: Gene. 2005 Apr 11;349:227-35
references.pmid: 15777665
references.citation: Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):7158-62
references.pmid: 12777620
references.citation: Gene. 2007 May 1;392(1-2):77-88
references.pmid: 17222522
references.citation: J Comput Biol. 2006 Mar;13(2):320-35
references.pmid: 16597243
references.citation: FEBS J. 2008 Dec;275(23):5934-46
references.pmid: 19021768
references.citation: J Biol Chem. 2004 Jun 18;279(25):26627-34
references.pmid: 15087446
references.citation: Cell. 1977 Sep;12(1):1-8
references.pmid: 902310
references.citation: Dev Biol. 1995 Oct;171(2):374-85
references.pmid: 7556921
references.citation: J Biochem. 1989 Feb;105(2):212-8
references.pmid: 2656665
references.citation: Mol Phylogenet Evol. 2005 Oct;37(1):165-77
references.pmid: 15890536
references.citation: Nucleic Acids Res. 1997 Dec 15;25(24):4876-82
references.pmid: 9396791
references.citation: Genome Res. 2004 Jul;14(7):1207-20
references.pmid: 15231741
references.citation: Dev Biol. 1992 Feb;149(2):349-56
references.pmid: 1730389
references.citation: Comp Biochem Physiol B Biochem Mol Biol. 2010 Apr;155(4):435-41
references.pmid: 20109577
references.citation: Trends Genet. 2006 Jan;22(1):16-22
references.pmid: 16290250
references.citation: Mol Phylogenet Evol. 2003 Jan;26(1):121-38
references.pmid: 12470944
references.citation: Proc Natl Acad Sci U S A. 1977 Aug;74(8):3171-5
references.pmid: 269380