Temperature-Dependent Structural Variability of RNAs: spliced Leader RNAs and their Evolutionary History

The structures attained by RNA molecules depend not only on their sequence but also on environmental parameters such as their temperature. So far, this effect has been largely neglected in bioinformatics studies. Here, we show that structural comparisons can be facilitated and more coherent structural models can be obtained when differences in environmental parameters are taken into account. We re-evaluate the secondary structures of the spliced leader (SL) RNAs from the seven eukaryotic phyla in which SL RNA trans-splicing has been described. Adjusting structure prediction to the natural growth temperatures and considering energetically similar secondary structures, we observe striking similarities among Euglenida, Kinetoplastida, Dinophyceae, Cnidaria, Rotifera, Nematoda, Platyhelminthes, and Tunicata that cannot be explained easily by the independent innovation of SL RNAs in each of these phyla. Supplementary Table is available at http://www.worldscinet.com/jbcb/.

[1]  David Hirsh,et al.  A trans-spliced leader sequence on actin mRNA in C. elegans , 1987, Cell.

[2]  D. Turner,et al.  A set of nearest neighbor parameters for predicting the enthalpy change of RNA secondary structure formation , 2006, Nucleic acids research.

[3]  S. França,et al.  Topology of splicing and snRNP biogenesis in dinoflagellate nuclei , 2006, Biology of the cell.

[4]  A. Simpson,et al.  Eukaryotic evolution: Early origin of canonical introns , 2002, Nature.

[5]  C. Ebel,et al.  Characterization of trans-splicing in Euglenoids , 2000, Current Genetics.

[6]  M. Zuker On finding all suboptimal foldings of an RNA molecule. , 1989, Science.

[7]  I. Stansfield,et al.  Spliced leader trans-splicing in the nematode Trichinella spiralis uses highly polymorphic, noncanonical spliced leaders. , 2008, RNA.

[8]  R. Chan,et al.  Short leader sequences may be transferred from small RNAs to pre‐mature mRNAs by trans‐splicing in Euglena. , 1991, The EMBO journal.

[9]  Senjie Lin,et al.  Dinoflagellate spliced leader RNA genes display a variety of sequences and genomic arrangements. , 2009, Molecular biology and evolution.

[10]  K. P. Watkins,et al.  Identification of a novel Y branch structure as an intermediate in trypanosome mRNA processing: Evidence for Trans splicing , 1986, Cell.

[11]  Philip E. Bourne,et al.  Sm/Lsm Genes Provide a Glimpse into the Early Evolution of the Spliceosome , 2009, PLoS Comput. Biol..

[12]  Sean R. Eddy,et al.  Rfam: annotating non-coding RNAs in complete genomes , 2004, Nucleic Acids Res..

[13]  T. Nilsen,et al.  Most mRNAs in the nematode Ascaris lumbricoides are trans-spliced: a role for spliced leader addition in translational efficiency. , 1995, RNA.

[14]  C. Ebel,et al.  Trans-splicing and cis-splicing in the colourless Euglenoid, Entosiphon sulcatum , 1999, Current Genetics.

[15]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[16]  D. Campbell Bodo caudatus medRNA and 5S rRNA genes: tandem arrangement and phylogenetic analyses. , 1992, Biochemical and biophysical research communications.

[17]  P. Schuster,et al.  RNA multi-structure landscapes , 1993, European Biophysics Journal.

[18]  R. Sommer,et al.  Operon structure and trans-splicing in the nematode Pristionchus pacificus. , 2003, Molecular biology and evolution.

[19]  Hans-Werner Mewes,et al.  Molecular evolution of eukaryotic genomes: hemiascomycetous yeast spliceosomal introns. , 2003, Nucleic acids research.

[20]  G. Hannon,et al.  Intramolecular base pairing between the nematode spliced leader and its 5′ splice site is not essential for trans‐splicing in vitro. , 1991, EMBO Journal.

[21]  A. Frasch,et al.  Comparison of the genes coding for the common 5' terminal sequence of messenger RNAs in three trypanosome species. , 1984, Nucleic acids research.

[22]  Hua Luo,et al.  Transcription Initiation at the TATA-less Spliced Leader RNA Gene Promoter Requires at Least Two DNA-binding Proteins and a Tripartite Architecture That Includes an Initiator Element* , 1999, The Journal of Biological Chemistry.

[23]  M. Blaxter,et al.  Nematode spliced leaders--ubiquity, evolution and utility. , 1996, International journal for parasitology.

[24]  Minghui Jiang,et al.  uShuffle: A useful tool for shuffling biological sequences while preserving the k-let counts , 2008, BMC Bioinformatics.

[25]  N. A. Stover,et al.  Trans-spliced leader addition to mRNAs in a cnidarian , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Sather,et al.  Identification of a small rna containing the trypanosome spliced leader: A donor of shared 5′ sequences of trypanosomatid mRNAs? , 1984, Cell.

[27]  Jamie J. Cannone,et al.  Evaluation of the suitability of free-energy minimization using nearest-neighbor energy parameters for RNA secondary structure prediction , 2004, BMC Bioinformatics.

[28]  A. Tunnacliffe,et al.  Spliced leader RNA-mediated trans-splicing in phylum Rotifera. , 2005, Molecular biology and evolution.

[29]  T. Blumenthal,et al.  trans Splicing of PolycistronicCaenorhabditis elegans Pre-mRNAs: Analysis of the SL2 RNA , 2000, Molecular and Cellular Biology.

[30]  Jiunn-Liang Chen,et al.  Secondary Structure of Vertebrate Telomerase RNA , 2000, Cell.

[31]  P. Schuster,et al.  Complete suboptimal folding of RNA and the stability of secondary structures. , 1999, Biopolymers.

[32]  R. Davis,et al.  RNA trans-splicing in Fasciola hepatica. Identification of a spliced leader (SL) RNA and SL sequences on mRNAs. , 1994, The Journal of biological chemistry.

[33]  R. Dassanayake,et al.  Trans-spliced leader RNA, 5S-rRNA genes and novel variant orphan spliced-leader of the lymphatic filarial nematode Wuchereria bancrofti, and a sensitive polymerase chain reaction based detection assay. , 2001, Gene.

[34]  R. Reinhardt,et al.  Spliced-Leader RNA trans Splicing in a Chordate, Oikopleura dioica, with a Compact Genome , 2004, Molecular and Cellular Biology.

[35]  K. Hastings,et al.  mRNA 5'-leader trans-splicing in the chordates. , 2001, Genes & development.

[36]  M. L. Muhich,et al.  The monogenetic kinetoplastid protozoan, Crithidia fasciculata, contains a transcriptionally active, multicopy mini-exon sequence. , 1987, Nucleic acids research.

[37]  J. Wohlschlegel,et al.  Spliceosomal snRNAs in the unicellular eukaryote Trichomonas vaginalis are structurally conserved but lack a 5'-cap structure. , 2008, RNA.

[38]  T. Nilsen Evolutionary origin of SL-addition trans-splicing: still an enigma. , 2001, Trends in genetics : TIG.

[39]  S. Miller,et al.  Cloning and characterization of a Leishmania gene encoding a RNA spliced leader sequence. , 1986, Nucleic acids research.

[40]  D. Penny,et al.  Computational Identification of Four Spliceosomal snRNAs from the Deep-Branching Eukaryote Giardia intestinalis , 2008, PloS one.

[41]  A. Rajkovic,et al.  A spliced leader is present on a subset of mRNAs from the human parasite Schistosoma mansoni. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[42]  D. Knox,et al.  Haemonchus contortus SL2 trans-spliced RNA leader sequence. , 2001, Molecular and biochemical parasitology.

[43]  K. Hastings SL trans-splicing: easy come or easy go? , 2005, Trends in genetics : TIG.

[44]  K. Brehm,et al.  mRNA Trans-splicing in the Human Parasitic CestodeEchinococcus multilocularis * , 2000, The Journal of Biological Chemistry.

[45]  R. Zayas,et al.  Spliced-leader trans-splicing in freshwater planarians. , 2005, Molecular biology and evolution.

[46]  Axel Mosig,et al.  Structure and Function of the Smallest Vertebrate Telomerase RNA from Teleost Fish* , 2008, Journal of Biological Chemistry.

[47]  F. V. Van Dolah,et al.  Spliced Leader RNA‐Mediated trans‐Splicing in a Dinoflagellate, Karenia brevis , 2007, The Journal of eukaryotic microbiology.

[48]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

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

[50]  T. Gaasterland,et al.  Spliced leader RNA trans-splicing in dinoflagellates , 2007, Proceedings of the National Academy of Sciences.

[51]  P. Stadler,et al.  Invertebrate 7SK snRNAs , 2008, Journal of Molecular Evolution.

[52]  Walter Fontana,et al.  Fast folding and comparison of RNA secondary structures , 1994 .

[53]  P. Stadler,et al.  Arthropod 7SK RNA. , 2008, Molecular biology and evolution.

[54]  P. Stadler,et al.  Secondary structure prediction for aligned RNA sequences. , 2002, Journal of molecular biology.

[55]  J. Sabina,et al.  Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. , 1999, Journal of molecular biology.

[56]  Ivo L. Hofacker,et al.  Vienna RNA secondary structure server , 2003, Nucleic Acids Res..

[57]  R. Bundschuh,et al.  A statistical analysis of RNA folding algorithms through thermodynamic parameter perturbation , 2004, Nucleic acids research.