Origins of recently gained introns in Caenorhabditis.

The genomes of the nematodes Caenorhabditis elegans and Caenorhabditis briggsae both contain approximately 100,000 introns, of which >6,000 are unique to one or the other species. To study the origins of new introns, we used a conservative method involving phylogenetic comparisons to animal orthologs and nematode paralogs to identify cases where an intron content difference between C. elegans and C. briggsae was caused by intron insertion rather than deletion. We identified 81 recently gained introns in C. elegans and 41 in C. briggsae. Novel introns have a stronger exon splice site consensus sequence than the general population of introns and show the same preference for phase 0 sites in codons over phases 1 and 2. More of the novel introns are inserted in genes that are expressed in the C. elegans germ line than expected by chance. Thirteen of the 122 gained introns are in genes whose protein products function in premRNA processing, including three gains in the gene for spliceosomal protein SF3B1 and two in the nonsense-mediated decay gene smg-2. Twenty-eight novel introns have significant DNA sequence identity to other introns, including three that are similar to other introns in the same gene. All of these similarities involve minisatellites or palindromes in the intron sequences. Our results suggest that at least some of the intron gains were caused by reverse splicing of a preexisting intron.

[1]  S. Brenner,et al.  Late changes in spliceosomal introns define clades in vertebrate evolution. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Thomas Blumenthal,et al.  Caenorhabditis elegans operons: form and function , 2003, Nature Reviews Genetics.

[3]  J. Rogers,et al.  How were introns inserted into nuclear genes? , 1989, Trends in genetics : TIG.

[4]  F Crick,et al.  Split genes and RNA splicing. , 1979, Science.

[5]  M. Giroux,et al.  De novo synthesis of an intron by the maize transposable element Dissociation. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J D Palmer,et al.  Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[7]  W. Gilbert,et al.  Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  S. Brenner,et al.  Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Brown,et al.  Genomic analysis of gene expression in C. elegans. , 2000, Science.

[10]  J. Logsdon,et al.  The recent origins of spliceosomal introns revisited. , 1998, Current opinion in genetics & development.

[11]  Arlin Stoltzfus,et al.  Molecular evolution: Recent cases of spliceosomal intron gain? , 1998, Current Biology.

[12]  T. Nagamine,et al.  p-SINE1-like intron of the CatA catalase homologs and phylogenetic relationships among AA-genome Oryza and related species , 1999, Theoretical and Applied Genetics.

[13]  Alexei Fedorov,et al.  Mystery of intron gain. , 2003, Genome research.

[14]  W. J. Kent,et al.  Conservation, regulation, synteny, and introns in a large-scale C. briggsae-C. elegans genomic alignment. , 2000, Genome research.

[15]  I. Ebersberger,et al.  A variable intron distribution in globin genes of Chironomus: evidence for recent intron gain. , 1997, Gene.

[16]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[17]  Y. Ohshima,et al.  Spliceosomal introns in conserved sequences of U1 and U5 small nuclear RNA genes in yeast Rhodotorula hasegawae. , 1996, Journal of biochemistry.

[18]  Roger E. Moore,et al.  Composition and functional characterization of the yeast spliceosomal penta-snRNP. , 2002, Molecular cell.

[19]  Arlin Stoltzfus,et al.  The evolutionary gain of spliceosomal introns: sequence and phase preferences. , 2004, Molecular biology and evolution.

[20]  M. V. Katti,et al.  Differential distribution of simple sequence repeats in eukaryotic genome sequences. , 2001, Molecular biology and evolution.

[21]  J D Beggs,et al.  Identification and functional analysis of hPRP17, the human homologue of the PRP17/CDC40 yeast gene involved in splicing and cell cycle control. , 1998, RNA.

[22]  D. Guiliano,et al.  Conservation of long-range synteny and microsynteny between the genomes of two distantly related nematodes , 2002, Genome Biology.

[23]  M. Lynch.  Intron evolution as a population-genetic process , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Igor B. Rogozin,et al.  Evidence of Splice Signal Migration from Exon to Intron during Intron Evolution , 2003, Current Biology.

[25]  B. Slatko,et al.  First sequenced genome of a parasitic nematode. , 2004, Trends in parasitology.

[26]  D. Charlesworth,et al.  The evolution of the alcohol dehydrogenase gene family by loss of introns in plants of the genus Leavenworthia (Brassicaceae). , 1998, Molecular biology and evolution.

[27]  M. Syvanen,et al.  Horizontal Gene Transfer , 2015, Evolution, Medicine, and Public Health.

[28]  R. Durbin,et al.  A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. , 1995, Gene.

[29]  D. Higgins,et al.  T-Coffee: A novel method for fast and accurate multiple sequence alignment. , 2000, Journal of molecular biology.

[30]  A. Newman,et al.  Evidence that introns arose at proto‐splice sites. , 1989, The EMBO journal.

[31]  C. R. McClung,et al.  Intron loss and gain during evolution of the catalase gene family in angiosperms. , 1998, Genetics.

[32]  H. Robertson.  Updating the str and srj (stl) families of chemoreceptors in Caenorhabditis nematodes reveals frequent gene movement within and between chromosomes. , 2001, Chemical senses.

[33]  R. Parker,et al.  Yeast Exosome Mutants Accumulate 3′-Extended Polyadenylated Forms of U4 Small Nuclear RNA and Small Nucleolar RNAs , 2000, Molecular and Cellular Biology.

[34]  Michael Lynch,et al.  The evolution of spliceosomal introns. , 2002, Current opinion in genetics & development.

[35]  W. Pearson.  Effective protein sequence comparison. , 1996, Methods in enzymology.

[36]  Phillip A. Sharp,et al.  On the origin of RNA splicing and introns , 1985, Cell.

[37]  Jean Thierry-Mieg,et al.  A global analysis of Caenorhabditis elegans operons , 2002, Nature.

[38]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..

[39]  K. Anders,et al.  SMG-2 Is a Phosphorylated Protein Required for mRNA Surveillance in Caenorhabditis elegans and Related to Upf1p of Yeast , 1999, Molecular and Cellular Biology.

[40]  E. Koonin,et al.  Remarkable Interkingdom Conservation of Intron Positions and Massive, Lineage-Specific Intron Loss and Gain in Eukaryotic Evolution , 2003, Current Biology.

[41]  W. Gilbert.  Why genes in pieces? , 1978, Nature.

[42]  A. Podtelejnikov,et al.  The yeast exosome and human PM-Scl are related complexes of 3' --> 5' exonucleases. , 1999, Genes & development.

[43]  W. Keller,et al.  Human pre-mRNA cleavage factor Im is related to spliceosomal SR proteins and can be reconstituted in vitro from recombinant subunits. , 1998, Molecular cell.

[44]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[45]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[46]  C. Guthrie,et al.  Splicing a spliceosomal RNA , 1989, Nature.

[47]  R. Durbin,et al.  The Genome Sequence of Caenorhabditis briggsae: A Platform for Comparative Genomics , 2003, PLoS biology.

[48]  F J Ayala,et al.  New Drosophila introns originate by duplication. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Ping Zhang,et al.  Timing and targeting of P-element local transposition in the male germline cells of Drosophila melanogaster. , 2002, Genetics.

[50]  S J de Souza,et al.  Relationship between "proto-splice sites" and intron phases: evidence from dicodon analysis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.