Molecular Evolution of the trnT_UGU-trnF_GAA Region in Bryophytes

Abstract

Structure, variability, and molecular evolution of the trnT-F region in the Bryophyta (mosses and liverworts) is analyzed based on about 200 sequences of the trnT-L spacer and trnL 5′ exon, 1000 sequences of the trnL intron, and 800 sequences of the trnL 3′ exon and trnL-F spacer, including comparisons of lengths, GC contents, sequence similarities, and functional elements. Mutations occurring in the trnL 5′ and 3′ exons, including compensatory base pair changes, and a transition in the trnL anticodon in Takakia lepidozioides, are discussed. All three non-coding regions display a mosaic structure of highly variable elements (V1 - V3 in the trnT-L spacer, V4/V5 corresponding to stem-loop regions P6/P8 in the trnL intron, and V6/V7 in the trnL-F spacer) and more conserved elements. In the trnL intron this structure is a consequence of the defined secondary structure necessary for correct splicing, whereas in both spacers conserved regions are restricted to promoter elements. At least the highly variable regions in the trnT-L spacer and stem-loop region P8 of the trnL intron seem to evolve independently in the major bryophyte lineages and are therefore not suitable for high taxonomic level phylogenetic reconstructions. In mosses, a trend of length reduction towards the more derived lineages is observed in all three non-coding regions. GC contents are mostly linked to sequence variability, with the conserved regions being more GC rich and the more variable AT rich. The lowest GC values (< 10 %) are found in the trnT-L spacer of mosses. In addition to two putative sigma⁷⁰-type promoters in the trnT-L spacer, a third putative promoter is present in the trnL-F spacer, although trnL and trnF are assumed to be co-transcribed. Consensus sequences are provided for the -35 and -10 sequences of the major bryophyte lineages. The third promoter is part of a hairpin secondary structure, whose loop region is highly homoplastic in mosses due to an inversion occurring independently in non-related taxa, even at the intraspecific level.

Key words

Molecular evolution - non-coding chloroplast DNA - trnT-F - trnL - group I intron - inversions - hairpins - secondary structure

References

• 1 Bakker F. T., Culham A., Gomez-Martinez R., Carvalho J., Compton J., Dawtrea R., Gibby M.. Patterns of nucleotide substitutions in angiosperm cpDNA trnL (UAA)-trnF (GAA) regions.  Molecular Biology and Evolution. (2000);  17 1146-1155
• 2 Blowers A., Klein D. U., Ellmore G. S., Bogorad L.. Functional in vivo analysis of the 3′ flanking sequences of the Chlamydomonas chloroplast rbcL and psaB genes.  Molecular and General Genetics. (1993);  238 339-349
• 3 Borsch T., Hilu W., Quandt D., Wilde V., Neinhuis C., Barthlott W.. Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms.  Journal of Evolutionary Biology. (2003);  16 558-576
• 4 Buck W. R., Goffinet B.. Morphology and classification of mosses. Shaw, A. J. and Goffinet, B., eds. Bryophyte Biology. Cambridge; Cambridge University Press (2000): 71-123
• 5 Buck W. R., Goffinet B., Shaw A. J.. Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnLF and rps4 sequences.  Molecular Phylogenetics and Evolution. (2000);  16 180-198
• 6 Burke J. M.. Molecular genetics of group I introns: RNA structures and protein factors required for splicing - a review.  Gene. (1988);  73 273-294
• 7 Cech T. R.. Conserved sequences and structures of group I introns: building an active site for RNA catalysis - a review.  Gene. (1988);  73 259-271
• 8 Cech T. R., Damberger S. H., Gutell R. R.. Representation of the secondary and tertiary structure of group I introns.  Structural Biology. (1994);  1 273-280
• 9 Cox C. J., Hedderson T. A.. Phylogenetic relationships among the ciliate arthrodontous mosses: evidence from chloroplast and nuclear DNA sequences.  Plant Systematics and Evolution. (1999);  215 119-139
• 10 Davies R. W., Waring R. B., Ray J. A., Brown T. A., Scazzocchio C.. Making ends meet: a model for RNA splicing in gingal mitochondria.  Nature. (1982);  300 719-724
• 11 De Luna E., Buck W. R., Akiyama H., Arikawa T., Tsubota H., Gonzalez D., Newton A. E., Shaw A. J.. Ordinal phylogeny within the Hypnobryalean pleurocarpous mosses inferred from cladistic analyses of three chloroplast DNA sequence data sets: trnL-F, rps4, and rbcL.  Bryologist. (2000);  103 242-256
• 12 Goffinet B.. Origin and phylogenetic relationships of bryophytes. Shaw, A. J. and Goffinet, B., eds. Bryophyte Biology. Cambridge; Cambridge University Press (2000): 124-149
• 13 Graham S. W., Reeves P. A., Burns A. C. E., Olmstead R. G.. Microstructural changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference.  International Journal of Plant Sciences. (2000);  161 (Suppl.) S83-S96
• 14 Hepperle D.. Alignment Editor Align. Heidelberg; distributed by the author (2002)
• 15 Hong L., Stevenson J. K., Roth W. B., Hallick R. B.. Euglena gracilis chloroplast psbB, psbT, psbH and psbN gene cluster: regulation of psbB-psbT pre-mRNA processing.  Molecular and General Genetics. (1995);  247 180-188
• 16 Hyvönen J., Hedderson T. A., Smith Merrill G. L., Gibbings J. G., Koskinen S.. On the phylogeny of the Polytrichales.  Bryologist. (1999);  101 489-504
• 17 Kanno A., Hirai A.. A transcription map of the chloroplast genome from rice (Oryza sativa). .  Current Genetics. (1993);  23 166-174
• 18 Kelchner S. A.. The Evolution of non-coding chloroplast DNA and its application in plant systematics.  Annals of the Missouri Botanical Garden. (2000);  87 482-498
• 19 Kugita M., Kaneko A., Yamamoto Y., Takeya Y., Matsumoto T., Yoshinaga K.. The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants.  Nucleic Acids Research. (2003);  31 176-721
• 20 Kuhsel M. G., Strickland R., Palmer J. D.. An ancient group I intron shared by eubacteria and chloroplasts.  Science. (1990);  250 1570-1573
• 21 Kumar S., Tamura K., Jakobsen I. B., Nei M.. MEGA2: molecular evolutionary genetics analysis software. Tempe, Arizona, USA; Arizona State University (2001)
• 22 Levinson G., Gutman A.. Slipped-stran mispairing: a major mechanism for DNA sequence evolution.  Molecular Biology and Evolution. (1987);  4 203-221
• 23 Lück R., Gräf S., Steger G.. ConStruct: a tool for thermodynamic controlled prediction of conserved secondary structure.  Nucleic Acids Research. (1999);  21 4208-4217
• 24 Lück R., Steger G., Riesner D.. Thermodynamic prediction of conserved secondary structure: Application to RRE-element of HIV, tRNA-like element of CMV, and mRNA of prion protein.  Journal of Molecular Biology. (1996);  258 813-826
• 25 Mathews D. H., Zuker M., Turner D. H.. RNAstructure 3.6. University of Rochester: distributed by the author. (2001)
• 26 Michel F., Jacquier A., Dujon B.. Comparison of fungal mitochondrial introns reveals extensive homologies in RNA secondary structure.  Biochemie. (1982);  64 867-881
• 27 Newton A. E., Cox C. J., Duckett J. G., Wheeler J. A., Goffinet B., Mishler B. D.. Evolution of the major moss lineages: phylogenetic analyses based on multiple gene sequences and morphology.  Bryologist. (2000);  103 187-211
• 28 Quandt D., Huttunen S., Streimann H., Frahm J.-P., Frey W.. Molecular phylogenetics of the Meteoriaceae s.str.: focusing on the genera Meteorium and Papillaria. .  Molecular Phylogenetics and Evolution. (2004 a);  32 435-461
• 29 Quandt D., Müller K., Stech M., Hilu K. W., Frey W., Frahm J.-P., Borsch T.. Molecular evolution of the chloroplast trnL-F region in land plants.  Monographs in Systematic Botany from the Missouri Botanical Garden. (2004 b);  in press
• 31 Quandt D., Stech M.. Molecular systematics of bryophytes in context of land plant phylogeny. Sharma, A. K. and Sharma, A., eds. Plant Genome. New Delhi; Oxford and IBH Publishing (2003): 267-295
• 32 Quandt D., Tangney R. S., Frahm J.-P., Frey W.. A molecular contribution for understanding the Lembophyllaceae (Bryopsida) based on noncoding chloroplast regions (cpDNA) and ITS2 (nrDNA) sequence data. Studies in austral temperate rain forest bryophytes 8.  Journal of the Hattori Botanical Laboratory. (2000);  89 71-92
• 33 Shaw A. J.. Phylogeny of the Sphagnopsida based on chloroplast and nuclear DNA sequences.  Bryologist. (2000);  103 277-306
• 34 Stech M., Frahm J.-P.. The systematic position of Ochyraea tatrensis (Hypnobartlettiaceae, Bryopsida) based on molecular data.  Bryologist. (2001);  104 199-203
• 35 Stech M., Frahm J.-P., Hilger H., Frey W.. Molecular relationship of Treubia Goebel (Treubiaceae, Treubiopsida) and high taxonomic level classification of the Hepaticophytina. Studies in austral temperate rain forest bryophytes 6.  Nova Hedwigia. (2000);  71 195-208
• 36 Stech M., Frey W.. CpDNA relationship and classification of the liverworts (Hepaticophytina, Bryophyta).  Nova Hedwigia. (2001);  72 45-58
• 37 Stech M., Konstantinova N. A., Frey W.. Molecular divergence between Treubia Goebel and Apotreubia S. Hatt. & Mizut., the two genera of the archaic liverwort class Treubiopsida (Hepaticophytina). Studies in austral temperate rain forest bryophytes 19.  Nova Hedwigia. (2002);  75 91-100
• 38 Stech M., Quandt D., Frey W.. Molecular evolution of the chloroplast DNA trnL-trnF region in the hornworts (Anthocerotophyta) and its phylogenetic implications.  Journal of Plant Research. (2003 a);  116 389-398
• 39 Stech M., Quandt D., Lindlar A., Frahm J.-P.. The systematic position of Pulchrinodus inflatus (Eucamptodon inflatus) based on molecular data. Studies in austral temperate rain forest bryophytes 21.  Australian Systematic Botany. (2003 b);  16 561-568
• 40 Stern D. B., Gruissem W.. Control of plastid gene expression: 3′inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription.  Cell. (1987);  51 1145-1157
• 41 Taberlet P., Gielly L., Pautou G., Bouvet J.. Universal primers for amplification of three non-coding regions of the chloroplast DNA.  Plant Molecular Biology. (1991);  17 1105-1109
• 42 Tamura K., Nei M.. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.  Molecular Biology and Evolution. (1993);  10 512-526
• 43 Turmel M., Otis C., Lemieux C.. The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants.  Proceedings of the National Academy of Sciences USA. (2002);  99 11275-11280
• 44 Vanderpoorten A., Hedenäs L., Cox C. J., Shaw A. J.. Phylogeny and morphological evolution of the Amblystegiaceae (Bryopsida).  Molecular Phylogenetics and Evolution. (2002);  23 1-21
• 45 Wakasugi T., Nagai T., Kapoor M., Sugita M., Ito M., Ito S., Tsudzuki J., Nakashima K., Tsudzuki J., Suzuki Y., Hamada A., Ohta T., Inamura A., Yoshinaga K., Sugiura M.. Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division.  Proceedings of the National Academy of Sciences USA. (1997);  94 5967-5972
• 46 Zuker M., Mathews D. H., Turner D. H.. Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. Barciszewski, J. and Clark, B. F. C., eds. RNA Biochemistry and Biotechnology. NATO ASI Series; Kluwer Academic Publishers (1999): 11-43

Section Editor: F. Salamini