Evolution of intron/exon structure of DEAD helicase family genes in Arabidopsis, Caenorhabditis, and Drosophila.

The DEAD box RNA helicase (RH) proteins are homologs involved in diverse cellular functions in all of the organisms from prokaryotes to eukaryotes. Nevertheless, there is a lack of conservation in the splicing pattern in the 53 Arabidopsis thaliana (AtRHs), the 32 Caenorhabditis elegans (CeRHs) and the 29 Drosophila melanogaster (DmRHs) genes. Of the 153 different observed intron positions, 4 are conserved between AtRHs, CeRHs, and DmRHs, and one position is also found in RHs from yeast and human. Of the 27 different AtRH structures with introns, 20 have at least one predicted ancient intron in the regions coding for the catalytic domain. In all of the organisms examined, we found at least one gene with most of its intron predicted to be ancient. In A. thaliana, the large diversity in RH structures suggests that duplications of the ancestral RH were followed by a high number of intron deletions and additions. The very high bias toward phase 0 introns is in favor of intron addition, preferentially in phase 0. Results from this comparative study of the same gene family in a plant and in two animals are discussed in terms of the general mechanisms of gene family evolution.

[1]  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.

[2]  W. Ford Doolittle,et al.  Genes in pieces: were they ever together? , 1978, Nature.

[3]  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.

[4]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[5]  W. Martin,et al.  Structure, evolution and anaerobic regulation of a nuclear gene encoding cytosolic glyceraldehyde-3-phosphate dehydrogenase from maize. , 1989, Journal of molecular biology.

[6]  R. Hardison,et al.  A brief history of hemoglobins: plant, animal, protist, and bacteria. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[7]  A Yoshida,et al.  Exon/intron structure of aldehyde dehydrogenase genes supports the "introns-late" theory. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[8]  E. Koonin,et al.  Intron sliding in conserved gene families. , 2000, Trends in genetics : TIG.

[9]  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.

[10]  S Bagavathi,et al.  Introns and protein revolution — an analysis of the exon/intron organisation of actin genes , 1996, FEBS letters.

[11]  T. Cavalier-smith,et al.  Selfish DNA and the origin of introns , 1985, Nature.

[12]  H. Goodman,et al.  The genome of Arabidopsis thaliana. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[13]  A. Dickson.  On Evolution , 1884, Science.

[14]  S. Aubourg,et al.  The DEAD box RNA helicase family in Arabidopsis thaliana. , 1999, Nucleic acids research.

[15]  Andrew Smith.  Genome sequence of the nematode C-elegans: A platform for investigating biology , 1998 .

[16]  S J de Souza,et al.  Origin of genes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[17]  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.

[18]  R. O’Neill,et al.  De novo insertion of an intron into the mammalian sex determining gene, SRY. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  John M Logsdon,et al.  The recent origins of introns , 1992, Current Biology.

[20]  D. Nouaud,et al.  A P element has induced intron formation in Drosophila. , 1999, Molecular biology and evolution.

[21]  M. Long,et al.  Intron-exon structures of eukaryotic model organisms. , 1999, Nucleic acids research.

[22]  J. Gogarten,et al.  Orthologs, paralogs and genome comparisons. , 1999, Current opinion in genetics & development.

[23]  G. Fichant.  Constraints acting on the exon positions of the splice site sequences and local amino acid composition of the protein. , 1992, Human molecular genetics.

[24]  G. Fink,et al.  Pseudogenes in yeast? , 1987, Cell.

[25]  A. Stoltzfus.  Origin of introns–early or late? , 1994, Nature.

[26]  S. Bak,et al.  Intron-exon organization and phylogeny in a large superfamily, the paralogous cytochrome P450 genes of Arabidopsis thaliana. , 2000, DNA and cell biology.

[27]  Russell F. Doolittle,et al.  Intron Distribution in Ancient Paralogs Supports Random Insertion and Not Random Loss , 1997, Journal of Molecular Evolution.

[28]  R. Lewin.  How mammalian RNA returns to its genome. , 1983, Science.

[29]  The Arabidopsis Genome Initiative.  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[30]  M T Clegg,et al.  The evolution of plant nuclear genes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  N. Raikhel,et al.  The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. , 2000, Plant physiology.

[32]  M. Borodovsky,et al.  GeneMark.hmm: new solutions for gene finding. , 1998, Nucleic acids research.

[33]  W. Doolittle,et al.  A kingdom-level phylogeny of eukaryotes based on combined protein data. , 2000, Science.

[34]  O. Gotoh,et al.  Divergent structures of Caenorhabditis elegans cytochrome P450 genes suggest the frequent loss and gain of introns during the evolution of nematodes. , 1998, Molecular biology and evolution.

[35]  J. Berg.  Genome sequence of the nematode C. elegans: a platform for investigating biology. , 1998, Science.

[36]  H. Robertson.  Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. , 1998, Genome research.

[37]  Eugene V. Koonin,et al.  Helicases: amino acid sequence comparisons and structure-function relationships , 1993 .

[38]  R. Iggo,et al.  Autoregulation of expression of the yeast Dbp2p ‘DEAD‐box’ protein is mediated by sequences in the conserved DBP2 intron. , 1995, The EMBO journal.

[39]  L. Patthy,et al.  Exon shuffling and other ways of module exchange. , 1996, Matrix biology : journal of the International Society for Matrix Biology.

[40]  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.

[41]  M. Zuker,et al.  Testing the exon theory of genes: the evidence from protein structure. , 1994, Science.

[42]  R F Doolittle,et al.  Convergent evolution: the need to be explicit. , 1994, Trends in biochemical sciences.

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

[44]  J. Spieth,et al.  Gene structure and organization in Caenorhabditis elegans. , 1996, Current opinion in genetics & development.

[45]  P Linder,et al.  D‐E‐A‐D protein family of putative RNA helicases , 1992, Molecular microbiology.

[46]  P. Linder.  DEAD-box proteins , 2000, Current Biology.

[47]  R. Schmidt.  The Arabidopsis genome , 2000 .

[48]  H. Puchta,et al.  Species‐specific double‐strand break repair and genome evolution in plants , 2000, The EMBO journal.

[49]  D. Petrov,et al.  Evidence for DNA loss as a determinant of genome size. , 2000, Science.

[50]  Peter G. Korning,et al.  Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. , 1996, Nucleic acids research.

[51]  J D Palmer,et al.  Intron "sliding" and the diversity of intron positions. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[53]  W. Gilbert,et al.  The exon theory of genes. , 1987, Cold Spring Harbor symposia on quantitative biology.

[54]  M. A. Koch,et al.  Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). , 2000, Molecular biology and evolution.

[55]  C. Trotman.  Introns-early: slipping lately? , 1998, Trends in genetics : TIG.