Pan-eukaryote ITS 2 homologies revealed by RNA secondary structure

For evolutionary comparisons, phylogenetics and evaluation of potential interbreeding taxa of a species, various loci have served for animals and plants and protistans. One [second internal transcribed spacer (ITS2) of the nuclear ribosomal DNA] is highly suitable for all. Its sequence is species specific. It has already been used extensively and very successfully for plants and some protistans, and a few animals (where historically, the mitochondrial genes have dominated species studies). Despite initial impressions that ITS2 is too variable, it has proven to provide useful biological information at higher taxonomic levels, even across all eukaryotes, thanks to the conserved aspects of its transcript secondary structure. The review of all eukaryote groups reveals that ITS2 is expandable, but always retains in its RNA transcript a common core structure of two helices with hallmark characteristics important for ribosomal RNA processing. This aspect of its RNA transcript secondary structure can rescue difficult alignment problems, making the ITS2a more powerful tool for phylogenetics. Equally important, the recognition of eukaryote-wide homology regions provides extensive and detailed information to test experimental studies of ribosomal rRNA processing.

[1]  Tobias Müller,et al.  The internal transcribed spacer 2 database—a web server for (not only) low level phylogenetic analyses , 2006, Nucleic Acids Res..

[2]  S. Harris,et al.  Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. , 2003, Molecular phylogenetics and evolution.

[3]  A. Coleman,et al.  The advantages of the ITS2 region of the nuclear rDNA cistron for analysis of phylogenetic relationships of insects: a Drosophila example. , 2004, Molecular phylogenetics and evolution.

[4]  A. Coleman,et al.  Paramecium aurelia Revisited , 2005, The Journal of eukaryotic microbiology.

[5]  Unusual compact rDNA gene arrangements within some members of the Ascomycota: evidence for molecular co-evolution between ITS1 and ITS2. , 2005, Genome.

[6]  B. Michot,et al.  Ribosomal internal transcribed spacer 2 (ITS2) exhibits a common core of secondary structure in vertebrates and yeast. , 1999, Nucleic acids research.

[7]  J. Bachellerie,et al.  Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences. , 1999, Nucleic acids research.

[8]  J. Elder,et al.  Concerted Evolution of Repetitive DNA Sequences in Eukaryotes , 1995, The Quarterly Review of Biology.

[9]  R. Gasser,et al.  Sequence differences in the internal transcribed spacers of DNA among four species of hookworm (Ancylostomatoidea: Ancylostoma). , 1999, International journal for parasitology.

[10]  Tobias Müller,et al.  A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the Eukaryota. , 2005, RNA.

[11]  M. Wolf THE SECONDARY STRUCTURE OF THE ITS2 TRANSCRIPT IN CYCLOTELLA AND STEPHANODISCUS (THALASSIOSIRACEAE, BACILLARIOPHYTA) , 2004 .

[12]  J. Wendel,et al.  Ribosomal ITS sequences and plant phylogenetic inference. , 2003, Molecular phylogenetics and evolution.

[13]  R. Planta,et al.  The nucleotide sequence of the intergenic region between the 5.8S and 26S rRNA genes of the yeast ribosomal RNA operon. Possible implications for the interaction between 5.8S and 26S rRNA and the processing of the primary transcript. , 1981, Nucleic acids research.

[14]  Rolf Backofen,et al.  Backofen R: MARNA: multiple alignment and consensus structure prediction of RNAs based on sequence structure comparisons , 2005 .

[15]  R. Planta,et al.  Evolutionarily conserved structural elements are critical for processing of Internal Transcribed Spacer 2 from Saccharomyces cerevisiae precursor ribosomal RNA. , 1995, Journal of molecular biology.

[16]  C H Porter,et al.  Sequence and secondary structure comparisons of ITS rDNA in mosquitoes (Diptera: Culicidae). , 1992, Molecular phylogenetics and evolution.

[17]  S. Barker,et al.  Evolution of the secondary structure of the rRNA internal transcribed spacer 2 (ITS2) in hard ticks (Ixodidae, Arthropoda) , 2002, Heredity.

[18]  A. Coleman,et al.  The Internal Transcribed Spacer 2 Exhibits a Common Secondary Structure in Green Algae and Flowering Plants , 1997, Journal of Molecular Evolution.

[19]  M. Melkonian,et al.  MOLECULAR PHYLOGENY OF STAURASTRUM MEYEN EX RALFS AND RELATED GENERA (ZYGNEMATOPHYCEAE, STREPTOPHYTA) BASED ON CODING AND NONCODING RDNA SEQUENCE COMPARISONS 1 , 2005 .

[20]  Annette W. Coleman,et al.  Exploring the Phylogenetic Utility of ITS Sequences for Animals: A Test Case for Abalone (Haliotis) , 2002, Journal of Molecular Evolution.

[21]  P. Mariottini,et al.  ITS2 rRNA evolution and its congruence with the phylogeny of muricid neogastropods (Caenogastropoda, Muricoidea). , 2002, Molecular phylogenetics and evolution.

[22]  A. M. Dávila,et al.  Internal transcribed spacers (ITS) of Trypanosoma rangeli ribosomal DNA (rDNA): a useful marker for inter-specific differentiation. , 2005, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[23]  Thomas Dandekar,et al.  Homology modeling revealed more than 20,000 rRNA internal transcribed spacer 2 (ITS2) secondary structures. , 2005, RNA.

[24]  Michael Zuker,et al.  Algorithms and Thermodynamics for RNA Secondary Structure Prediction: A Practical Guide , 1999 .

[25]  X. Turon,et al.  Phylogeographical history of the sponge Crambe crambe (Porifera, Poecilosclerida): range expansion and recent invasion of the Macaronesian islands from the Mediterranean Sea , 2004, Molecular ecology.

[26]  A. Coleman,et al.  CLOSTERIUM MONILIFERUM‐EHRENBERGII (CHAROPHYCEAE, CHLOROPHYTA) SPECIES COMPLEX VIEWED FROM THE 1506 GROUP I INTRON AND ITS2 OF NUCLEAR rDNA , 2003 .

[27]  Robert K Jansen,et al.  ITS secondary structure derived from comparative analysis: implications for sequence alignment and phylogeny of the Asteraceae. , 2003, Molecular phylogenetics and evolution.

[28]  R. Gasser,et al.  Secondary structure model for the ITS-2 precursor rRNA of strongyloid nematodes of equids: implications for phylogenetic inference. , 1999, International journal for parasitology.

[29]  A. Coleman,et al.  ITS2 is a double-edged tool for eukaryote evolutionary comparisons. , 2003, Trends in genetics : TIG.

[30]  Q. Cronk,et al.  Evolution and alignment of the hypervariable arm 1 of Aeschynanthus (Gesneriaceae) ITS2 nuclear ribosomal DNA. , 2001, Molecular phylogenetics and evolution.

[31]  C. Cote,et al.  Dynamic conformational model for the role of ITS2 in pre-rRNA processing in yeast. , 2002, RNA.

[32]  T. Gregory,et al.  The correlation between rDNA copy number and genome size in eukaryotes. , 2003, Genome.

[33]  Trematode and Monogenean rRNA ITS2 Secondary Structures Support a Four-Domain Model , 1998, Journal of Molecular Evolution.

[34]  M. Lürling,et al.  A revised secondary structure model for the internal transcribed spacer 2 of the green algae Scenedesmus and Desmodesmus and its implication for the phylogeny of these algae , 2002 .

[35]  C. Severini,et al.  Sequence and secondary structure of the rDNA second internal transcribed spacer in the sibling species Culex pipiens L. and Cx. quinquefasciatus Say (Diptera: Culicidae) , 1996, Insect molecular biology.

[36]  Tobias Müller,et al.  4SALE – A tool for synchronous RNA sequence and secondary structure alignment and editing , 2006, BMC Bioinformatics.

[37]  T. Pröschold,et al.  Portrait of a Species , 2005, Genetics.

[38]  Austen R. D. Ganley,et al.  Highly efficient concerted evolution in the ribosomal DNA repeats: total rDNA repeat variation revealed by whole-genome shotgun sequence data. , 2007, Genome research.

[39]  M. Harrington,et al.  Structural partitioning, paired-sites models and evolution of the ITS transcript in Syzygium and Myrtaceae. , 2007, Molecular phylogenetics and evolution.

[40]  M. Gouy,et al.  Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. , 1998, Nucleic acids research.

[41]  T. Motomura,et al.  Little divergence in ribosomal DNA internal transcribed spacer ‐1 and ‐2 sequences among non‐digitate species of Laminaria (Phaeophyceae) from Hokkaido, Japan , 1999 .

[42]  A. W. Coleman,et al.  The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. , 2000, Protist.

[43]  T. Dandekar,et al.  ITS-2 and 18S rRNA gene phylogeny of Aplysinidae (Verongida, Demospongiae) , 2005, Journal of Molecular Evolution.

[44]  Mark A. Ragan,et al.  Are rRNA sequence comparisons the Rosetta stone of phylogenetics? , 1986, Cell.

[45]  D. Miller,et al.  Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. , 1997, Molecular biology and evolution.

[46]  M. Hershkovitz,et al.  Deep-level diagnostic value of the rDNA-ITS region. , 1996, Molecular biology and evolution.

[47]  L. Malone,et al.  The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. , 1998, Journal of invertebrate pathology.

[48]  B Michot,et al.  Conserved secondary structures in the ITS2 of trematode pre‐rRNA , 1993, FEBS letters.

[49]  M. Gottschling,et al.  Secondary structure models of the nuclear internal transcribed spacer regions and 5.8S rRNA in Calciodinelloideae (Peridiniaceae) and other dinoflagellates. , 2004, Nucleic acids research.

[50]  Tobias Müller,et al.  CBCAnalyzer: inferring phylogenies based on compensatory base changes in RNA secondary structures , 2005, Silico Biol..

[51]  J. Gómez‐Zurita,et al.  Sequence, secondary structure and phylogenetic analyses of the ribosomal internal transcribed spacer 2 (ITS2) in the Timarcha leaf beetles (Coleoptera: Chrysomelidae) , 2000, Insect molecular biology.

[52]  A. Coleman,et al.  Intraspecies Analysis: Comparison of ITS Sequence Data and Gene Intron Sequence Data with Breeding Data for a Worldwide Collection of Gonium pectorale , 1999, Journal of Molecular Evolution.

[53]  T. Stuessy,et al.  Evolution and Speciation of Island Plants. , 1999 .