Skip to main content
SpringerLink
Log in

The Chloroplast trnT–trnF Region in the Seed Plant Lineage Gnetales

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

Abstract

The trnT–trnF region is located in the large single-copy region of the chloroplast genome. It consists of the trnL intron, a group I intron, and the trnT–trnL and trnL–trnF intergenic spacers. We analyzed the evolution of the region in the three genera of the gymnosperm lineage Gnetales (Gnetum, Welwitschia, and Ephedra), with especially dense sampling in Gnetum for which we sequenced 41 accessions, representing most of the 25–35 species. The trnL intron has a conserved secondary structure and contains elements that are homologous across land plants, while the spacers are so variable in length and composition that homology cannot be found even among the three genera. Palindromic sequences that form hairpin structures were detected in the trnL–trnF spacer, but neither spacer contained promoter elements for the tRNA genes. The absence of promoters, presence of hairpin structures in the trnL–trnF spacer, and high sequence variation in both spacers together suggest that trnT and trnF are independently transcribed. Our model for the expression and processing of the genes tRNAThr(UGU), tRNALeu(UAA), and tRNAPhe (GAA) therefore attributes the seemingly neutral evolution of the two spacers to their escape from functional constraints.

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

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Bakker FT, Culham A, Gomez-Martinez R, Carvalho J, Compton J, Dawtrey R, Gibby M (2000) Patterns of nucleotide substitution in angiosperm cpDNA trnL (UAA)-trnF (GAA) regions. Mol Biol Evol 17:1146–1155

    PubMed  Google Scholar 

  • Belfort M, Derbyshire V, Parker MM, Cousineau B, Lambowitz AM (2002) Mobile introns: pathways and proteins. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. ASM Press, Washington, DC, pp 761–783

    Google Scholar 

  • Besendahl A, Qiu Y-L, Lee J, Palmer JD, Bhattacharya D (2000) The cyanobacterial origin and vertical transmission of the plastid tRNALeu group-I intron. Curr Genet 37:12–23

    Article  PubMed  Google Scholar 

  • Bogorad L (1991) Replication and transcription of plastid DNA. In: Bogorad L, Vasil IK (eds) The molecular biology of plastids: Cell culture and somatic cell genetics of plants, Vol. 7A. Academic Press, San Diego, pp 93–124

    Google Scholar 

  • Bonnard G, Michel F, Weil JH, Steinmetz AA (1984) Nucleotide sequence of the split tRNALeu gene from Vicia faba chloroplasts: evidence for structural homologies of the chloroplast tRNALeu intron with the intron from the autosplicable Tetrahymena ribosomal RNA precursor. Mol Gen Genet 194:330–336

    Article  Google Scholar 

  • Borsch T, Hilu KW, Quandt D, Wilde V, Neihuis C, Barthlott W (2003) Noncoding plastid trnT–trnF sequences reveal a well resolved phylogeny of basal angiosperms. J Evol Biol 16:558–576

    Article  PubMed  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  Google Scholar 

  • Cech TR, Damberger SH, Gutell RR (1994) Representation of the secondary and tertiary structure of group I introns. Nature Struct Biol 1:273–280

    Article  PubMed  Google Scholar 

  • Cheng YS, Lin C-H, Chen L-J (1997) Transcription and processing of the gene for spinach chloroplast threonine tRNA in a homologous in vitro system. Biochem Biophys Res Comm 233:380–385

    Article  PubMed  Google Scholar 

  • Christopher DA, Hallick RB (1990) Complex RNA maturation pathway for a chloroplast ribosomal protein operon with an internal tRNA cistron. Plant Cell 2:659–671

    Article  PubMed  Google Scholar 

  • Delp G, Igloi GL, Kössel H (1991) Identification of in vivo processing intermediates and of splice junctions of tRNAs from maize chloroplasts by amplification with the polymerase chain reaction. Nucleic Acids Res 19:713–716

    PubMed  Google Scholar 

  • Frank DN, Pace NR (1998) Ribonuclease P: unity and diversity in a tRNA processing ribozyme. Annu Rev Biochem 67:153–180

    Article  PubMed  Google Scholar 

  • Galli G, Hofstetter H, Birnstiel ML (1981) Two conserved sequence blocks within eukaryotic tRNA genes are major promoter elements. Nature 294:626–631

    Article  PubMed  Google Scholar 

  • Gegenheimer P (1996) Structure, mechanism, and evolution of chloroplast transfer RNA processing systems. Mol Biol Rep 22:147–150

    Article  Google Scholar 

  • Graham SW, Reeves PA, Burns ACE, Olmstead RG (2000) Microstructural changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference. Int J Plant Sci 161 (Suppl 6):S83–S96

    Article  Google Scholar 

  • Gruissem W, Zurawski G (1985) Identification and mutational analysis of the promoter for a spinach chloroplast transfer RNA gene. EMBO J 4:1637–1644

    PubMed  Google Scholar 

  • Gruissem W, Greenberg BM, Zurawski G, Prescott DM, Hallick RB (1983) Biosynthesis of chloroplast transfer RNA in a spinach chloroplast transcription system. Cell 35:815–828

    Article  PubMed  Google Scholar 

  • Gruissem W, Elsner-Menzel C, Latshaw S, Narita JO, Schaffer MA, Zurawski G (1986) A subpopulation of spinach chloroplast tRNA genes does not require upstream promoter elements for transcription. Nucleic Acids Res 14:7541–7556

    PubMed  Google Scholar 

  • Hanley-Bowdoin L, Chua N-H (1987) Chloroplast promoters. Trends Biochem 12:67–70

    Article  Google Scholar 

  • Hilu KW, Borsch T, Müller K, Soltis DE, Soltis PS, Savolainen V, Chase MW, Powell MP, Alice LA, Evans R, Sauquet H, Neinhuis C, Slotta TAB, Rohwer JG, Slotta TAB, Rohwer JG, Campbell CS, Chatrou LW (2003) Angiosperm phylogeny based on matK sequence information. Am J Bot 90:1758–1776

    Google Scholar 

  • Holschuh K, Bottomley W, Whitfeld PR (1984) Structure of the spinach chloroplast genes for the D2 and 44 Kd reaction-center proteins of photosystem II and for tRNASer (UGA). Nucleic Acids Res 12:8819–8834

    PubMed  Google Scholar 

  • Huang J, Giannasi DE, Price RA (2005) Phylogenetic relationships in Ephedra (Ephedraceae) inferred from chloroplast and nuclear DNA sequences. Mol Phylogenet Evol 35:48–59

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist FR (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  Google Scholar 

  • Ickert-Bond SM, Wojciechowski MF (2004) Phylogenetic relationships in Ephedra (Gnetales): evidence from nuclear and chloroplast DNA sequence data. Syst Bot 29:834–849

    Article  Google Scholar 

  • Inokuchi H, Yamao F (1995) Structure and expression of prokaryotic tRNA genes. In: Söll D, RajBahndary U (eds) tRNA: Structure, biogenesis, and function. ASM Press, Washington, DC, pp 17–30

    Google Scholar 

  • Jahn D (1992) Expression of the Chlamydomonas reinhardtii chloroplast tRNAGlu gene in a homologous in vitro transcription system is independent of upstream promoter elements. Arch Biochem Biophys 298:505–513

    Article  PubMed  Google Scholar 

  • Källersjö M, Farris JS, Chase MW, Bremer B, Fay MF, Humphries CJ, Petersen G, Seberg O, Bremer K (1998) Simultaneous parsimony jackknife analysis of 2538 rbcL DNA sequences reveals support for major clades of green plants, land plants, seed plants, and flowering plants. Pl Syst Evol 213:259–287

    Article  Google Scholar 

  • Kanno A, Hirai A (1993) A transcription map of the chloroplast genome from rice (Oryza sativa). Curr Genet 23:166–174

    Article  PubMed  Google Scholar 

  • Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 87:482–498

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  Google Scholar 

  • Koch MA, Dobes C, Matschinger M, Bleeker W, Vogel J, Kiefer M, Mitchell-Olds T (2005) Evolution of the trnF(GAA) gene in Arabidopsis relatives and the Brassicaceae family: monophyletic origin and subsequent diversification of a plastidic pseudogene. Mol Biol Evol 22:1032–1043

    Article  PubMed  Google Scholar 

  • Kuhsel MG, Strickland R, Palmer JD (1990) An acient group I intron shared by Eubacteria and chloroplasts. Science 250:1570–1573

    PubMed  Google Scholar 

  • Kunzmann A, Brennicke A, Marchfelder A (1998) 5′ end maturation and RNA editing have to precede tRNA 3′ processing in plant mitochondria. Proc Natl Acad Sci USA 95:108–113

    Article  PubMed  Google Scholar 

  • Lambowitz AM, Caprara MG, Zimmerly S, Perlman PS (1999) Group I and group II ribozymes as RNPs: clues to the past and guides to the future. In: Gesteland RF, Cech TR, Atkins JF (eds) The RNA world, 2nd ed. The world of modern RNA suggests a prebiotic RNA. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 451–485

    Google Scholar 

  • Leach DRF (1994) Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair. Bioessays 16:893–900

    Article  PubMed  Google Scholar 

  • Leal-Klevezas DS, Martínez-Soriano JP, Nazar RN (2000) Cotranscription of 5S rRNA-tRNAArg(ACG) from Brassica napus chloroplast and processing of their intergenic spacer. Gene 253:303–311

    Article  PubMed  Google Scholar 

  • Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221

    PubMed  Google Scholar 

  • Marion-Poll A, Hibbert CS, Radebaugh CA, Hallick RB (1988) Processing of mono-, di-and tricistronic transfer RNA precursors in a spinach or pea chloroplast soluble extract. Plant Mol Biol 11:45–56

    Article  Google Scholar 

  • Martin NC (1995) Organellar tRNAs: Biosynthesis and function. In: Söll D, RajBahndary U (eds) tRNA: Structure, biogenesis, and function. ASM Press, Washington, DC, pp 127–140

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Morden CW, Wolfe KH, dePamphilis CW, Palmer JD. 1991. Plastid translation and transcription genes in a non–photosynthetic plant: intact, missing and pseudo genes. EMBO J 10:3281–3288

    PubMed  Google Scholar 

  • Nakamura T, Ohta M, Sugiura M, Sugita M (1999) Chloroplast ribonucleoproteins are associated with both mRNAs and intron containing precursor tRNAs. FEBS Lett 460:437–441

    Article  PubMed  Google Scholar 

  • Nasar F, Jankowski C, Nag DK (2000) Long palindromic sequences induce double-strand beaks during meiosis in yeast. Mol Cell Biol 20:3449–3458

    Article  PubMed  Google Scholar 

  • Ohme M, Kamogashira T, Sinozaki K, Sugiura M (1985) Structure and cotranscription of tobacco chloroplast genes for tRNAGlu(UUC), tRNATyr(GUA), and tRNAAsp(GUC). Nucleic Acids Res 13:1045–1056

    PubMed  Google Scholar 

  • Quandt D, Müller K, Stech M, Hilu KW, Frey W, Frahm J-P, Borsch T (2004) Molecular evolution of the chloroplast trnL-F region in land plants. Monogr Syst Bot Mo Bot Gard 98:13–37

    Google Scholar 

  • Schiffer S, Helm M, Théobald-Dietrich A, Giegé R, Marchfelder A (2001) The plant tRNA 3′ processing enzyme has a broad substrate spectrum. Biochemistry 40:8264–8272

    Article  PubMed  Google Scholar 

  • Schiffer S, Rösch S, Marchfelder A (2002) Assigning a function to a conserved group of proteins: the tRNA 3′-processing enzyme. EMBO J 21:2769–2777

    Article  PubMed  Google Scholar 

  • Schwarz Z, Jolly SO, Steinmetz AA, Bogorad L (1981) Overlapping divergent genes in the maize chloroplast chromosome and in vitro transcription of the gene for tRNAHis. Proc Natl Acad Sci USA 78:3423–3427

    Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166

    Google Scholar 

  • Simon D, Fewer D, T Friedl, Bhattacharya D (2003) Phylogeny and self-splicing ability of the plastid tRNA-Leu group I intron. J Mol Evol 57:710–20

    Article  PubMed  Google Scholar 

  • Steinmetz AA, Krebbers ET, Schwarz Z, Gubbins EJ, Bogorad L (1983) Nucleotide sequences of five maize chloroplast transfer RNA genes and their flanking regions. J Biol Chem 258:5503–5511

    PubMed  Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Mol Biol 17:1105–1109

    Article  Google Scholar 

  • Tonkyn JC, Gruissem W (1993) Differential expression of the partially duplicated chloroplast S10 ribosomal protein operon. Mol Gen Genet 241:141–152

    Article  PubMed  Google Scholar 

  • van Ham RCHJ, ‘t Hart H, Mes THM, Sandbrink JM (1994) Molecular evolution of noncoding regions of the chloroplast genome in the Crassulaceae and related species. Curr Genet 25:558–566

    Article  PubMed  Google Scholar 

  • Vogel J, Hess WR (2001) Complete 5′ and 3′ end maturation of group II intron-containing tRNA precursors. RNA 7:285–292

    Article  PubMed  Google Scholar 

  • Vogel J, Börner T, Hess WR (1999) Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants. Nucleic Acids Res 27:3866–3874

    Article  PubMed  Google Scholar 

  • Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91:9794–9798

    PubMed  Google Scholar 

  • Wang MJ, Davis NW, Gegenheimer P (1988) Novel mechanisms for maturation of chloroplast transfer RNA precursors. EMBO J 7:1567–1574

    Google Scholar 

  • Wolfe KH, Morden CW, Ems SC, Palmer JD (1992) Rapid evolution of the plastid translation apparatus in a nonphotosynthetic plant: loss or accelerated sequence evolution of tRNA and ribosomal protein genes. J Mol Evol 35:304–317

    Article  PubMed  Google Scholar 

  • Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA 100:10824–10829

    Article  PubMed  Google Scholar 

  • Won H, Renner SS (2005a) The internal transcribed spacer of nuclear ribosomal DNA in the gymnosperm Gnetum. Mol Phylogenet Evol 36 (in press)

  • Won H, Renner SS (2005b) Bayesian relaxed clock estimates suggest that the gymnosperm Gnetum (Gnetales) dispersed over water between South America, Africa and Asia (submitted for publication)

  • Wu C-Y, Lin C-H, Chen L-J (1997) Identification of the transcription site for the spinach chloroplast tRNA genes. FEBS Lett 418:157–161

    Article  PubMed  Google Scholar 

  • Xu MQ, Kathe SD, Goodrich-Blair H, Nierzwicki-Bauer SA, Shub DA (1990) Science 250:1566–1570

    PubMed  Google Scholar 

  • Zaug AJ, McEvoy MM, Cech TR (1993) Self-splicing of the group I intron from Anabaena pre-tRNA: requirement for base-pairing of the exons in the anticodon stem. Biochemistry 32:7946–7953

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This paper represents a portion of a dissertation submitted by the first author in partial fulfillment of the requirements for a Ph.D. from University of Missouri—St. Louis. Financial support from the American Society of Plant Taxonomy, the International Association of Plant Taxonomy, and the International Center for Tropical Ecology at the University of Missouri—St. Louis is gratefully acknowledged.

Author information

Author notes

  1. Hyosig Won

    Present address: Seoul National University, Colleges of Natural Sciences, School of Bilogical Sciences, Seoul, Korea, 151-742

Authors and Affiliations

  1. Department of Biology, University of Missouri—St. Louis, 8001 Natural Bridge Road, St. Louis, MO, 63121, USA

    Hyosig Won

  2. Missouri Botanical Garden, P.O. Box 299, St. Louis, MO, 63166, USA

    Susanne S. Renner

Authors
  1. Hyosig Won
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susanne S. Renner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susanne S. Renner.

Additional information

[Reviewing Editor: Debashish Bhattacharya]

Appendix

Appendix

Table A1 Species sampled, vouchers, GenBank accession numbers, and summary for length (bp) and G+C (%) content for chloroplast trnT–trnL IGS, trnL intron, and trnL–trnF IGS sequences
Full size table
Table A2 List of informative gaps in the Gnetum chloroplast tRNALeu intron and adjacent IGS regions: Base positions 142–181, 246–260, 297–301, 576–606, 706–745, 810–853, 976–993, and 1012–1070, which include these gaps, were excluded from the analyses
Full size table
Table A3 Sequence divergences (K-2-P) for the cp trnL intron and adjacent IGS regions
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Won, H., Renner, S.S. The Chloroplast trnT–trnF Region in the Seed Plant Lineage Gnetales. J Mol Evol 61, 425–436 (2005). https://doi.org/10.1007/s00239-004-0240-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-0240-3

Keywords

Search

Navigation