Abstract
The wide but sporadic distribution of group I introns in protists, plants, and fungi, as well as in eubacteria, likely resulted from extensive lateral transfer followed by differential loss. The extent of horizontal transfer of group I introns can potentially be determined by examining closely related species or genera. We used a phylogenetic approach with a large data set (including 62 novel large subunit [LSU] rRNA group I introns) to study intron movement within the monophyletic lichen family Physciaceae. Our results show five cases of horizontal transfer into homologous sites between species but do not support transposition into ectopic sites. This is in contrast to previous work with Physciaceae small subunit (SSU) rDNA group I introns where strong support was found for multiple ectopic transpositions. This difference in the apparent number of ectopic intron movements between SSU and LSU rDNA genes may in part be explained by a larger number of positions in the SSU rRNA, which can support the insertion and/or retention of group I introns. In contrast, we suggest that the LSU rRNA may have fewer acceptable positions and therefore intron spread is limited in this gene.
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References
N Ban P Nissen J Hansen PB Moore TA Steitz (2000) ArticleTitleThe complete atomic structure of the large ribosomal subunit at 2.4 Å resolution Science 289 905–919 Occurrence Handle10.1126/science.289.5481.905 Occurrence Handle1:STN:280:DC%2BD3cvgslCgsA%3D%3D Occurrence Handle10937989
A Besendahl Y-L Qiu J Lee JD Palmer D Bhattacharya (2000) ArticleTitleThe cyanobacterial origin and vertical transmission of the plastid tRNALeu group-I intron Curr Genet 37 12–23 Occurrence Handle10.1007/s002940050002 Occurrence Handle1:CAS:528:DC%2BD3cXitFartQ%3D%3D Occurrence Handle10672439
M Belfort PS Perlman (1995) ArticleTitleMechanisms of intron mobility J Biol Chem 270 30237–30240 Occurrence Handle10.1074/jbc.270.51.30237 Occurrence Handle1:CAS:528:DyaK28XhtFGqug%3D%3D Occurrence Handle8530436
D Bhattacharya (1998) ArticleTitleThe origin and evolution of protist group I introns Protist 149 113–122
D Bhattacharya B Surek M Rusing S Damberger M Melkonian (1994) ArticleTitleGroup I introns are inherited through common ancestry in the nuclear-encoded rRNA of Zygnematales (Charophyceae) Proc Natl Acad Sci USA 91 9916–9920 Occurrence Handle1:CAS:528:DyaK2MXht1Cmsbk%3D Occurrence Handle7937917
D Bhattacharya T Friedl S Damberger (1996) ArticleTitleNuclear-encoded rDNA group I introns: origin and phylogenetic relationships of insertion site lineages in the green algae Mol Biol Evol 13 978–989 Occurrence Handle1:CAS:528:DyaK28XltlSmsLc%3D Occurrence Handle8752006
D Bhattacharya F Lutzoni V Reeb D Simon F Fernandez (2000) ArticleTitleWidespread occurrence of spliceosomal introns in the rDNA genes of ascomycetes Mol Biol Evol 17 1971–1984 Occurrence Handle1:CAS:528:DC%2BD3cXptVWrtro%3D Occurrence Handle11110913
D Bhattacharya JJ Cannone RR Gutell (2001) ArticleTitleGroup I intron lateral transfer between red and brown algal ribosomal RNA Curr Genet 40 82–90 Occurrence Handle10.1007/s002940100227 Occurrence Handle1:CAS:528:DC%2BD3MXlvVaqsbY%3D Occurrence Handle11570520
D Bhattacharya T Friedl G Helms (2002) ArticleTitleVertical evolution and intragenic spread of lichen-fungal group I introns J Mol Evol 55 74–84 Occurrence Handle10.1007/s00239-001-2305-x Occurrence Handle1:CAS:528:DC%2BD38XlvVCqsbc%3D Occurrence Handle12165844
D Bhattacharya D Simon J Huang JJ Cannone RR Gutell (2003) ArticleTitleThe exon context and distribution of Euascomycetes rRNA spliceosomal introns BMC Evol Biol 3 7 Occurrence Handle10.1186/1471-2148-3-7 Occurrence Handle12716459
JJ Cannone S Subramanian MN Schnare JR Collett LM D’Souza Y Du B Feng N Lin LV Madabusi KM Muller N Pande Z Shang N Yu RR Gutell (2002) ArticleTitleThe Comparative RNA Web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs BMC Bioinformatics 3 15 Occurrence Handle10.1186/1471-2105-3-15
JR Cassidy D Moore BC Lu PJ Pukkila (1984) ArticleTitleUnusual organization and lack of recombination in the ribosomal-RNA genes of Coprinus cinereus Curr Genet 8 607–613 Occurrence Handle10.1007/BF00395706 Occurrence Handle1:CAS:528:DyaL2MXhvVyjsA%3D%3D
TR Cech (1985) ArticleTitleSelf-splicing RNA: implications for evolution Int Rev Cytol 93 3–22 Occurrence Handle1:CAS:528:DyaL2MXks1Krs7Y%3D Occurrence Handle3891660
Y Cho JD Palmer (1999) ArticleTitleMultiple acquisitions via horizontal transfer of a group I intron in the mitochondrial cox1 gene during evolution of the Araceae family Mol Biol Evol 16 1155–1165 Occurrence Handle1:CAS:528:DyaK1MXmtVWntb4%3D Occurrence Handle10486971
Y Cho Y-L Qiu P Kuhlman JD Palmer (1998) ArticleTitleExplosive invasion of plant mitochondria by group I intron Proc Natl Acad Sci USA 95 14244–14249 Occurrence Handle10.1073/pnas.95.24.14244 Occurrence Handle1:CAS:528:DyaK1cXns1Gmu7s%3D Occurrence Handle9826685
PT DePriest MD Been (1992) ArticleTitleNumerous group I introns with variable distributions in the ribosomal DNA of a lichen fungus J Mol Biol 228 315–321 Occurrence Handle10.1016/0022-2836(92)90819-6 Occurrence Handle1:CAS:528:DyaK3sXjtlyhtw%3D%3D Occurrence Handle1453441
B Dujon (1989) ArticleTitleGroup I introns as mobile genetic elements: facts and mechanistic speculations—A review Gene 82 91–114 Occurrence Handle10.1016/0378-1119(89)90034-6 Occurrence Handle1:CAS:528:DyaL1MXmtV2kurg%3D Occurrence Handle2555264
PS Dyer GJ Murtagh PD Crittenden (2001) ArticleTitleUse of RAPD-PCR DNA fingerprinting and vegetative incompatibility tests to investigate genetic variation within lichen-forming fungi Symbiosis 31 213–229 Occurrence Handle1:CAS:528:DC%2BD3MXls1Wrurg%3D
J Felsenstein (1985) ArticleTitleConfidence intervals on phytogenies: an approach using the bootstrap Evolution 39 783–791
T Friedl (1987) ArticleTitleThallus development and phycobionts of the parasitic lichen Diploschistes muscorum Lichenologist 19 183–191
T Friedl A Besendahl P Pfeiffer D Bhattacharya (2000) ArticleTitleThe distribution of group I introns in lichen algae suggests that lichenization facilitates intron lateral transfer Mol Phylogenet Evol 14 342–352 Occurrence Handle10.1006/mpev.1999.0711 Occurrence Handle1:CAS:528:DC%2BD3cXhsFyltrY%3D Occurrence Handle10712840
A Gargas PT DePriest JW Taylor (1995) ArticleTitlePositions of multiple insertions in SSU rDNA of lichen-forming fungi Mol Biol Evol 12 208–218 Occurrence Handle1:CAS:528:DyaK2MXjvVajt7w%3D Occurrence Handle7700150
MR Goddard A Burt (1999) ArticleTitleRecurrent invasion and extinction of a selfish gene Proc Natl Acad Sci USA 96 13880–13885 Occurrence Handle10.1073/pnas.96.24.13880 Occurrence Handle1:CAS:528:DyaK1MXns1OqtLY%3D Occurrence Handle10570167
BL Golden AR Gooding ER Podell TR Cech (1998) ArticleTitleA preorganized active site in the crystal structure of the Tetrahymena ribozyme Science 282 259–264 Occurrence Handle10.1126/science.282.5387.259 Occurrence Handle1:CAS:528:DyaK1cXmsF2jtLs%3D Occurrence Handle9841391
TA Hall (1999) ArticleTitleBioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp Ser 41 95–98 Occurrence Handle1:CAS:528:DC%2BD3cXhtVyjs7Y%3D
P Haugen D Bhattacharya (2004) ArticleTitleThe spread of LAGLIDADG homing endonuclease genes in rDNA Nucleic Acids Res 32 2049–2057 Occurrence Handle10.1093/nar/gkh520 Occurrence Handle1:CAS:528:DC%2BD2cXjt1ejsL0%3D Occurrence Handle15069127
P Haugen HJ Runge D Bhattacharya (2004a) ArticleTitleLong-term evolution of the S788 fungal nuclear small subunit rRNA group I introns RNA 10 1084–1096 Occurrence Handle10.1261/rna.5202704 Occurrence Handle1:CAS:528:DC%2BD2cXltlKmu78%3D
P Haugen V Reeb F Lutzoni D Bhattacharya (2004b) ArticleTitleThe evolution of homing endonuclease genes and group I introns in nuclear rDNA Mol Biol Evol 21 129–140 Occurrence Handle10.1093/molbev/msh005 Occurrence Handle1:CAS:528:DC%2BD2cXhvVKqs7g%3D
P Haugen D Simon D Bhattacharya (2005) ArticleTitleThe natural history of group I introns Trends Genet 21 111–119 Occurrence Handle10.1016/j.tig.2004.12.007 Occurrence Handle1:CAS:528:DC%2BD2MXmslKgtA%3D%3D Occurrence Handle15661357
G Helms T Friedl G Rambold H Mayhofer (2001) ArticleTitleIdentification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing Lichenologist 33 73–86 Occurrence Handle10.1006/lich.2000.0298
DS Hibbett (1996) ArticleTitlePhylogenetic evidence for horizontal transmission of group I introns in the nuclear ribosomal DNA of mushroom-forming fungi Mol Biol Evol 13 903–917 Occurrence Handle1:CAS:528:DyaK28XltlSmsL8%3D Occurrence Handle8751999
A Hoist-Jensen M Vaage T Schumacher S Johansen (1999) ArticleTitleStructural characteristics and possible horizontal transfer of group I introns between closely related pathogenic fungi Mol Biol Evol 16 114–126 Occurrence Handle1:CAS:528:DyaK1MXjvVGksA%3D%3D Occurrence Handle10331256
JP Huelsenbeck F Ronquist (2001) ArticleTitleMrBayes: Bayesian inference of phylogeny Bioinformatics 17 754–755 Occurrence Handle10.1093/bioinformatics/17.8.754 Occurrence Handle1:STN:280:DC%2BD3MvotV2isw%3D%3D Occurrence Handle11524383
S Jackson J Cannone J Lee R Gutell S Woodson (2002) ArticleTitleDistribution of rRNA introns in the three-dimensional structure of the ribosome J Mol Biol 323 35–52 Occurrence Handle10.1016/S0022-2836(02)00895-1 Occurrence Handle1:CAS:528:DC%2BD38XnsVant74%3D Occurrence Handle12368097
J Kjems RA Garrett (1991) ArticleTitleRibosomal RNA introns in archaea and evidence for RNA conformational changes associated with splicing Proc Natl Acad Sci USA 88 439–443 Occurrence Handle1:CAS:528:DyaK3MXhtFGqsbs%3D Occurrence Handle1899138
DJ Klein TM Schmeing PB Moore TA Steitz (2001) ArticleTitleThe kink-turn: a new RNA secondary structure motif EMBO J 20 4214–4221 Occurrence Handle10.1093/emboj/20.15.4214 Occurrence Handle1:CAS:528:DC%2BD3MXmtlChtL0%3D Occurrence Handle11483524
K Kruger PJ Grabowski AJ Zaug J Sands DE Gottschling TR Cech (1982) ArticleTitleSelf-splicing RNA: Autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena Cell 31 147–157 Occurrence Handle10.1016/0092-8674(82)90414-7 Occurrence Handle1:CAS:528:DyaL3sXht1eguw%3D%3D Occurrence Handle6297745
AM Lambowitz M Belfort (1993) ArticleTitleIntrons as mobile genetic elements Annu Rev Biochem 62 587–622 Occurrence Handle10.1146/annurev.bi.62.070193.003103 Occurrence Handle1:CAS:528:DyaK3sXlvFKltL0%3D Occurrence Handle8352597
EB Lickey KW Hughes RH Peterson (2003) ArticleTitleVariablility and phylogenetic incongruence of an SSU nrDNA group I intron in Artomyces, Auriscalpium, and Lentinellus (Auriscalpiaceae: Homobasdiomycetes) Mol Biol Evol 20 1909–1916 Occurrence Handle10.1093/molbev/msg210 Occurrence Handle1:CAS:528:DC%2BD3sXpt1Kgtrk%3D Occurrence Handle12885954
EW Lundblad C Einvik S Rønning K Haugli S Johansen (2004) ArticleTitleTwelve group I introns in the same pre-rRNA transcript of the myxomycete Fuligo septica: RNA processing and evolution Mol Biol Evol 21 1283–1293 Occurrence Handle10.1093/molbev/msh126 Occurrence Handle1:CAS:528:DC%2BD2cXltlKls7o%3D Occurrence Handle15034133
DR Maddison WP Maddison (2002) MacClade 4.05 Sinauer Associates Sunderland, MA
F Michel E Westoff (1990) ArticleTitleModelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis J Mol Biol 216 585–610 Occurrence Handle10.1016/0022-2836(90)90386-Z Occurrence Handle1:CAS:528:DyaK3MXps1agtw%3D%3D Occurrence Handle2258934
GJ Murtagh PS Dyer PD Crittenden (2000) ArticleTitleSex and the single lichen Nature 404 564 Occurrence Handle10.1038/35007142 Occurrence Handle1:CAS:528:DC%2BD3cXis1Gmtro%3D Occurrence Handle10766229
N Nikoh T Fukatsu (2001) ArticleTitleEvolutionary dynamics of multiple group I introns in nuclear ribosomal RNA genes of endoparasitic fungi of the genus Cordyceps Mol Biol Evol 18 1631–1642 Occurrence Handle1:CAS:528:DC%2BD3MXmt12iurg%3D Occurrence Handle11504844
K Nishida S Suzuki Y Kimura N Nomura M Fujie T Yamada (1998) ArticleTitleGroup I introns found in Chlorella viruses: biological implications Virology 242 319–326 Occurrence Handle10.1006/viro.1998.9030 Occurrence Handle1:CAS:528:DyaK1cXhvFWnt7w%3D Occurrence Handle9514979
S Perotto P Nepote-Fus L Saletta C Bandi JP Young (2000) ArticleTitleA diverse population of introns in the nuclear ribosomal genes of ericoid mycorrhizal fungi includes elements with sequence similarity to endonuclease-coding genes Mol Biol Evol 17 44–59 Occurrence Handle1:CAS:528:DC%2BD3cXotF2qtQ%3D%3D Occurrence Handle10666705
D Posada KA Crandall (1998) ArticleTitleMODELTEST: testing the model of DNA substitution Bioinformatics 14 817–818 Occurrence Handle10.1093/bioinformatics/14.9.817 Occurrence Handle1:CAS:528:DyaK1MXktlCltw%3D%3D Occurrence Handle9918953
D Posada KA Crandall (200la) ArticleTitleSelecting the best-fit model of nucleotide substitution Syst Biol 50 580–601 Occurrence Handle10.1080/106351501750435121
D Posada KA Crandall (2001b) ArticleTitleSimple (wrong) models for complex trees: a case from Retroviridae Mol Biol Evol 18 271–275 Occurrence Handle1:CAS:528:DC%2BD3MXotVOltQ%3D%3D
V Ramakrishnan PB Moore (2001) ArticleTitleAtomic structures at last: the ribosome in 2000 Curr Opin Struct Biol 11 144–154 Occurrence Handle10.1016/S0959-440X(00)00184-6 Occurrence Handle1:CAS:528:DC%2BD3MXjsVyju7o%3D Occurrence Handle11297922
F Rodriguez JL Oliver A Marin JR Medina (1990) ArticleTitleThe general stochastic model of nucleotide substitution J Theor Biol 142 485–501 Occurrence Handle2338834
J Roman SA Woodson (1995) ArticleTitleReverse splicing of the Tetrahymena IVS: evidence for multiple reaction sites in the 23S rRNA RNA 1 478–490 Occurrence Handle1:CAS:528:DyaK2MXnsl2ltrw%3D Occurrence Handle7489509
J Roman SA Woodson (1998) ArticleTitleIntegration of the Tetrahymena group I intron into bacterial rRNA by reverse splicing in vivo Proc Natl Acad Sci USA 95 2134–2139 Occurrence Handle10.1073/pnas.95.5.2134 Occurrence Handle1:CAS:528:DyaK1cXhsleju7s%3D Occurrence Handle9482851
PJ Russell S Wagner KD Rodland RL Feinbaum JP Russell MS Bretharte SJ Free RL Metzenberg (1984) ArticleTitleOrganization of the ribosomal ribonucleic acid genes in various wild-type strains and wild-collected strains of Neurospora Mol Gen Genet 196 275–282 Occurrence Handle10.1007/BF00328060 Occurrence Handle1:CAS:528:DyaL2cXmt1ert7Y%3D Occurrence Handle6092870
JM Schroeder-Diedrich PA Fuerst TJ Byers (1998) ArticleTitleGroup-I introns with unusual sequences occur at three sites in nuclear 18S rRNA genes of Acanthamoeba lenticulata Curr Genet 34 71– 87 Occurrence Handle10.1007/s002940050368 Occurrence Handle1:CAS:528:DyaK1cXks12hsLk%3D Occurrence Handle9683678
H Shimodaira M Hasegawa (2001) ArticleTitleCONSEL: for assessing the confidence of phylogenetic tree selection Bioinformatics 17 1246–1247 Occurrence Handle1:STN:280:DC%2BD38%2FgtFOlsw%3D%3D Occurrence Handle11751242
D Simon D Fewer T Friedl D Bhattacharya (2003) ArticleTitlePhylogeny and self-splicing ability of the plastid tRNA-Leu group I intron J Mol Evol 57 710–720 Occurrence Handle10.1007/s00239-003-2533-3 Occurrence Handle1:CAS:528:DC%2BD2cXjsVemtQ%3D%3D Occurrence Handle14745540
SO Suh KG Jones M Blackwell (1999) ArticleTitleA group I intron in the nuclear small subunit rRNA gene of Cryptendoxyla hypophloia, an ascomycetous fungus: evidence for a new major class of group I introns J Mol Evol 1999 48 493–500 Occurrence Handle1:CAS:528:DyaK1MXisFGisrY%3D
DL Swofford (2003) PAUP*: Phylogenetic analysis using parsimony (*and other methods) 4.0b8. Sinauer Associates Sunderland, MA
AJ Thompson DL Herrin (1994) ArticleTitleA chloroplast group I intron undergoes the first step of reverse splicing into host cytoplasmic 5.8S rRNA: implications for intron-mediated RNA recombination, intron transposition and 5.8S rRNA structure J Mol Biol 236 455–468 Occurrence Handle10.1006/jmbi.1994.1157 Occurrence Handle1:CAS:528:DyaK2cXis1artb0%3D Occurrence Handle8107133
M Turmel RR Gutell JP Mercier C Otis C Lemieux (1993) ArticleTitleAnalysis of the chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa. Three internal transcribed spacers and 12 group I intron insertion sites J Mol Biol 232 446–467 Occurrence Handle10.1006/jmbi.1993.1402 Occurrence Handle1:CAS:528:DyaK2cXpslCksw%3D%3D Occurrence Handle8393936
M Turmel V Cote C Otis JP Mercier MW Gray KM Lonergan C Lemieux (1995) ArticleTitleEvolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion) Mol Biol Evol 12 533–545 Occurrence Handle1:CAS:528:DyaK2MXmsVOqsrY%3D Occurrence Handle7659010
JC Vaughn MT Mason GL Sper-Whitis P Kuhlman JD Palmer (1995) ArticleTitleFungal origin by horizontal transfer of a plant mitochondrial group I intron in the chimeric CoxI gene of Pepperomia J Mol Evol 41 563–572 Occurrence Handle10.1007/BF00175814 Occurrence Handle1:CAS:528:DyaK2MXpsVKgtLw%3D Occurrence Handle7490770
KS Wilson HF Noller (1998) ArticleTitleMolecular movement inside the translational engine Cell 92 337–349 Occurrence Handle10.1016/S0092-8674(00)80927-7 Occurrence Handle1:CAS:528:DyaK1cXhtFGisLg%3D Occurrence Handle9476894
BT Wimberly DE Brodersen WM demons RJ Morgan-Warren AP Carter C Vonrhein T Hartsch V Ramakrishnan (2000) ArticleTitleStructure of the 30S ribosomal subunit Nature 407 327– 339 Occurrence Handle10.1038/35030006 Occurrence Handle1:CAS:528:DC%2BD3cXntFyktb4%3D Occurrence Handle11014182
SA Woodson TR Cech (1989) ArticleTitleReverse self-splicing of the Tetrahymena group I intron: implication for the directionality of splicing and for intron transposition Cell 57 335–345 Occurrence Handle10.1016/0092-8674(89)90971-9 Occurrence Handle1:CAS:528:DyaL1MXit1Knurk%3D Occurrence Handle2702692
SA Woodson TR Cech (1991) ArticleTitleAlternative secondary structures in the 5′ exon affect both forward and reverse self-splicing of the Tetrahymena intervening sequence RNA Biochemistry 30 2042–2050 Occurrence Handle10.1021/bi00222a006 Occurrence Handle1:CAS:528:DyaK3MXpslaltQ%3D%3D Occurrence Handle1998665
Z Yang (1997) ArticleTitlePAML: A program package for phylogenetic analysis by maximum likelihood CABIOS 13 555–556 Occurrence Handle1:CAS:528:DyaK2sXntlGnu7s%3D Occurrence Handle9367129
M Zuker (2003) ArticleTitleMfold web server for nucleic acid folding and hybridization prediction Nucleic Acids Res 31 3406–3415 Occurrence Handle10.1093/nar/gkg595 Occurrence Handle1:CAS:528:DC%2BD3sXltVWisr8%3D Occurrence Handle12824337
Acknowledgments
This work was supported by a grant awarded to D.B. from the National Science Foundation (MCB 01-10252) and a grant from the Deutsche Forschungsgemeinschaft to T.F. (Fr 905/7-1,2). D.S. was partially supported by a Stanley Fellowship and an Avis E. Cone research fellowship from the University of Iowa and J.M. was supported by a NSF-REU grant (MCB-03-26864) awarded to D.B. We also thank Peik Haugen (Iowa) for helpful discussions.
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Simon, D., Moline, J., Helms, G. et al. Divergent Histories of rDNA Group I Introns in the Lichen Family Physciaceae. J Mol Evol 60, 434–446 (2005). https://doi.org/10.1007/s00239-004-0152-2
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DOI: https://doi.org/10.1007/s00239-004-0152-2