Skip to main content
SpringerLink
Log in

Variability of Nuclear SSU-rDNA Group Introns Within Septoria Species: Incongruence with Host Sequence Phylogenies

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

We report structural features and distribution patterns of 26 different group I introns located at three distinct nucleotide positions in nuclear small subunit ribosomal DNA (SSU-rDNA) of 10 Septoria and 4 other anamorphic species related to the teleomorphic genus Mycosphaerella. Secondary structure and sequence characteristics assigned the introns to the common IC1 and IE groups. Intron distribution patterns and phylogenetic relationships strongly suggested that some horizontal transfer events have occurred among the closely related fungal species sampled. To test this hypothesis, we used a comparative approach of intron- and rDNA-based phylogenies through MP- and ML-based topology tests. Our results showed two statistically well-supported major incongruences between the intron and the equivalent internal transcribed spacer (ITS) tree comparisons made. Such absence of a co-evolutive history between group I introns and host sequences is discussed relatively to the intron structures, the mechanisms of intron movement, and the biology of the Mycosphaerella pathogenic fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Bell-Pedersen D, Quirck SM, Aubrey M, Belfort M (1989). A site-specific endonuclease and co-conversion of flanking exons associated with the mobile td intron of phage T4. Gene 82:119–126

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharya D, Friedl T, Damberger S (1996) Nuclear-encoded rDNA group I introns: origin and phylogenetic relationships of insertion site lineages in the green algae. Mol Biol Evol 13:978–989

    PubMed  CAS  Google Scholar 

  • Bhattacharya D, Friedl T, Helms G (2002) Vertical evolution and intragenic spread of lichen-fungal group I Introns. J Mol Evol 55:74–84

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharya D, Reeb V, Simon DM, Lutzoni F (2005) Phylogenetic analyses suggest reverse splicing spread of group I introns in fungal ribosomal DNA. BMC Evol Biol 5:68

    Article  PubMed  CAS  Google Scholar 

  • Burke JM, Belfort M, Cech TR, Davies RW, Schweyen RJ, Shub DA, Szostak JW, Tabak HF (1987) Structural convention for group I introns. Nucleic Acids Res 15:7217–7221

    Article  PubMed  CAS  Google Scholar 

  • Cannone JJ, Subramanian S, Schane MM, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Muller KM, Pande N, Schang Z, Yu N, Gutell RR (2002) The comparative RNA Web (CRW): on line database of comparative sequence and structure information for ribosomal intron and other RNAs. BioMed Central Bioinform 3:1–31

    Google Scholar 

  • Cech TR (1988) Conserved sequences and structures of group I introns: building an active site for RNA catalysis-a review. Gene 73:259–271

    Article  PubMed  CAS  Google Scholar 

  • Costa M, Michel F (1995) Frequent use of the same tertiary motif by self-folding RNAs. EMBO J 14:1276–1285

    PubMed  CAS  Google Scholar 

  • Crous PW, Aptroot A, Kang JC, Braun U, Wingfieid MJ (2000) The genus Mycosghaerella and its anamorphs. Stud Mycol 45:107–121

    Google Scholar 

  • Crous PW, Kang JC, Braun U (2001) A phylogenetic redefinition of anamorph genera in Mycosphaerella based on ITS rDNA sequence and morphology. Mycologia 93:1081–1101

    Article  CAS  Google Scholar 

  • Crous PW, Groenewald JZ, Pongpanich K, Himaman W, Arzanlou M, Wingfieid MJ (2004) Cryptic speciation and host specificity among Mycosphaerella spp. occurring on Australian Acacia species grown as exotics in the tropics. Stud Mycol 50:457–469

    Google Scholar 

  • Dujon B (1989) Group I introns as mobile genetic elements: facts and mechanistic speculations-a review. Gene 82:91–114

    Article  PubMed  CAS  Google Scholar 

  • Feau N, Hamelin RC, Bernier L (2006) Attributes and congruence of three molecular data sets: inferring phytogenies among Septoria-related species form woody perennial plants. Mol Phylogent Evol 40:808–829

    Article  PubMed  CAS  Google Scholar 

  • Gargas A, Taylor JW (1992) Polymerase chain reactiori (PCR) primers for amplifying and sequencing nuclear 18 S rDNA lichenized fungi. Mycologia 84:589–592

    Article  CAS  Google Scholar 

  • Gibb EA, Hausner G (2003) A group I intron-like sequence in the nuclear small ribosomal subunit gene of the ophiostomatoid fungus Gondwanamyces proteae. Mycol Res 107:1442–1450

    Article  PubMed  CAS  Google Scholar 

  • Goddard MR, Burt A (1999) Recurrent invasion and extinction of a selfish gene. Proc Natl Acad Sci USA 96:13880–13885

    Article  PubMed  CAS  Google Scholar 

  • Goldman N, Anderson JP, Rodrigo AG (2000) Likelihood based-test of topologies in phylogenetics. Syst Biol 49:652–670

    Article  PubMed  CAS  Google Scholar 

  • Guo F, Gooding AR, Cech T (2004) Structure of the Tetrahymena ribozyme: base triple sandwich and metal ion active site. Mol Cell 16:351–362

    PubMed  CAS  Google Scholar 

  • Gutell RR (1993) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res 21:3051–3054

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  PubMed  CAS  Google Scholar 

  • Haugen P, Reeb V, Lutzoni F, Bhattacharya D (2004) The evolution of homing endonuclease genes and group I introns nuclear rDNA. Mol Biol Evol 21:129–140

    Article  PubMed  CAS  Google Scholar 

  • Haugen P, Simon DM, Bhattacharya D (2005) The natural history of group I introns. Trends Genet 21:111–119

    Article  PubMed  CAS  Google Scholar 

  • Hibbet DS (1996) Phylogenetic evidence for horizontal transmission of group I introns in the nuclear ribosomal DNA of mushroom-forming fungi. Mol Biol Evol 13:903–909

    Google Scholar 

  • Holst-Jensen A, Vaage M, Schumacher T, Johansen S (1999) Structural characteristics and possible horizontal transfer of group I introns between closely related plant pathogenic fungi. Mol Biol Evol 16:114–126

    PubMed  CAS  Google Scholar 

  • Hufford L, McMahon MM, Sherwood AM, Reeves G, Chase MW (2003) The major clades of Loasaceae: phylogenetic analysis using the plastid matK and trnL-trnF regions. Am J Bot 90:1215–1228

    CAS  Google Scholar 

  • Johansen S, Haugen P (1999) A complex group I intron in Nectria galligena rDNA. Microbiology 145:516–517

    Article  PubMed  CAS  Google Scholar 

  • Johansen S, Haugen P (2001) A new nomenclature of group I introns in ribosomal DNA. RNA 7:935–936

    Article  PubMed  CAS  Google Scholar 

  • Johansen S, Embley TM, Willassen NP (1993) A family of nuclear homing endonucleases. Nucleic Acids Res 21:4405

    Article  PubMed  CAS  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Lehnert V, Jaeger L, Michel F, Westhof E (1996) New loop-tertiary interactions in self-splicing introns q subgroup 1C and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. Chem Biol 3:993–1009

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Zhang Y (2005) Predicting the secondary structures and tertiary interactions of 211 group I introns in IE subgroup. Nucleic Acids Res 33:2118–2128

    Article  PubMed  CAS  Google Scholar 

  • Machouart-Dubach M, Lacroix C, Vaury C, Feuilhade de Chauvin M, Bellanne C, Derouin F, Lorenzo F (2001) Nucleotide structure of the Scytalidium hyalinum and Scytalidium dimidiatum 18S subunit ribosomal RNA gene: evidence for the insertion of a group IE intron in the rDNA gene of S. dimidiatum. FEMS Microbiol Lett 208:187–196

    Article  Google Scholar 

  • Michel F, Westhof E (1990) Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 216:585–610

    Article  PubMed  CAS  Google Scholar 

  • Nikoh N, Fukatsu T (2001) Evolutionary dynamics of multiple group I introns jn nuclear ribosomal RNA genes of endoparasitic fungi of the genus Cordyceps. Mol Biol Evol 18:1631–1642

    PubMed  CAS  Google Scholar 

  • Nishida H, Tajiri Y, Sugiyama J (1998) Multiple origin of fungal group I intron located in the same position of nuclear SSU-rDNA gene. J Mol Evol 46:442–448

    Article  PubMed  CAS  Google Scholar 

  • Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217

    Article  PubMed  CAS  Google Scholar 

  • Perotto S, Nepote-Fus P, Saletta L, Bandi C, Young JPW (2000) A 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

    PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Roman J, Woodson SA (1998) Integration of the Tetrahymena group I intron into bacterial rRNA by reverse splicing in vivo. Proc Natl Acad Sci USA 95:2134–2139

    Article  PubMed  CAS  Google Scholar 

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    CAS  Google Scholar 

  • Simon D, Moline J, Helms G, Friedl T, Bhattacharya D (2005) Divergent histories of rDNA group I introns in the lichen family Physaciaceae. J Mol Evol 60:434–446

    Article  PubMed  CAS  Google Scholar 

  • Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295

    PubMed  CAS  Google Scholar 

  • Suf SO, Jones KG, Blackwell M (1999) A group I intron in the nuclear small subunit rRNA gene of Cryptendoxyla hypophtoia, an ascomycetous fungus: evidence for a new major class of group I introns. J Mol Evol 48:493–500

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with a particular reference to the evolution of humans and apes. Evolution 37:221–244

    Article  CAS  Google Scholar 

  • Verkley GJM, Priest MJ (2000) Septoria and similar coelomycetous anamorphs of Mycosphaerella. Stud Mycol 43:123–128

    Google Scholar 

  • Verkley GJM, Starink-Willemse M, van Iperen A, Abeln EGA (2004) Phylogenetic analyses of Septoria species based on the ITS and LSU-D2 regions of nuclear ribosomal DNA. Mycologia 96:558–571

    CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungai, ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninskv JJ, White TJ, (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Wingfield MJ, Slippers B, Roux J, Wingfield BD (2001) Worldwide movement of exotic forest fungi, especially in the tropics and the Southern Hemisphere. BioScience 51:134–140

    Article  Google Scholar 

  • Woodson SA, Cech TR (1989) Reverse self-splicing of the Tetrahymena group I intron: implication for the directionality of splicing and for intron transposition. Cell 57:335–345

    Article  PubMed  CAS  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are greatly indebted to Dr. Pascal Frey (Institut National de la Recherche Agronomique, Nancy, France) for constructive and helpful discussions. L. Bernier and R.C. Hamelin acknowledge support from a Fonds québécois de la recherche sur la nature et les technologies (FQRNT) team grant.

Author information

Authors and Affiliations

  1. Centre d’étude de la forêt, Université Laval, Québec, G1K 7P4, Canada

    Nicolas Feau & Louis Bernier

  2. Service canadien des forêts, Ressources naturelles Canada, Centre de foresterie des Laurentides, 1055 du PEPS, P.O. Box 3800, Québec, G1V 4C7, Canada

    Nicolas Feau & Richard C. Hamelin

Authors
  1. Nicolas Feau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard C. Hamelin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Louis Bernier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Louis Bernier.

Additional information

Reviewing Editor: Debashish Bhattacharya

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feau, N., Hamelin, R.C. & Bernier, L. Variability of Nuclear SSU-rDNA Group Introns Within Septoria Species: Incongruence with Host Sequence Phylogenies. J Mol Evol 64, 489–499 (2007). https://doi.org/10.1007/s00239-005-0309-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-005-0309-7

Keywords

Search

Navigation