Download PDF
Plant Biol (Stuttg) 2003; 5(4): 400-410
DOI: 10.1055/s-2003-42715
Original Paper

Georg Thieme Verlag Stuttgart · New York

Characterisation of the Chloroplast DNA psbT-H Region and the Influence of Dyad Symmetrical Elements on Phylogenetic Reconstructions

D. Quandt 1 , K. Müller 1 , S. Huttunen 2
  • 1Botanisches Institut und Botanischer Garten, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
  • 2Botanical Museum, University of Helsinki, Helsinki, Finland
Further Information

Publication History

Publication Date:
02 October 2003 (online)

   Permissions and Reprints

Abstract

The tandemly arranged genes psbT, psbN, and psbH code for proteins of photosystem II and are located in the large single copy region (LSC) of the chloroplast genome, downstream of psbB. So far, most of the studies dealing with this region have been interested in the organization and transcription of the psbB operon, while less is known about the transcription of psbN or the phylogenetic utility of this region. In the current study we discuss a sigma70-type bacterial promoter motif upstream of psbN and present its consensus sequence for bryophytes. An analysis of the 3′ flanking inverted repeat sequences revealed a dyad symmetrical element, which is able to form a stable stem-loop structure. This hairpin structure is characterised for land plants, with an emphasis on bryophytes. Furthermore, we observed an inversion of up to 9 bases in the loop region of the hairpin structure, which occasionally occurred in different unrelated bryophyte families, orders and classes. Small inversions are frequently obscured in the alignment since, during automatic alignment, many gap-weighting schemes may not introduce gaps, nor does a manual insertion of gaps always seem needed at first glance. In subsequent phylogenetic analyses, minute inversion may overweight a particular mutation by interpreting the single inversion event as multiple apomorphic substitutions, which is particularly problematic since such inversion events are known to often be highly homoplastic. In the present study we use the psbT-N spacer as an example to quantify the effect of such small inversions, contrasting the phylogenetic structure obtained with and without information from the hairpin loop. We show that obscured minute inversions can highly significantly reduce the robustness of the phylogenetic hypothesis inferred from the data set.

Key words

Dyad symmetrical elements - inversions - repeats - noncoding chloroplast DNA - molecular evolution - phylogenetics - promoter - 3′ UTR.

References

  • 1 Barkan A.. Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs.  European Molecular Biology Organization Journal. (1988);  7 2637-2644
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 4 Crayn D. M., Quinn C. J.. The evolution of the atpB-rbcL intergeneic spacer in the epacrids (Ericales) and its systematic and evoluionary implications.  Molecular Phylogenetics and Evolution. (2000);  16 238-252
    CrossrefPubMedGoogle Scholar
  • 5 Dixit R., Trivedi P. K., Nath P., Sane P. V.. Organization and post-transcriptional processing of the psbB operon from chloroplasts of Populus deltoids.  Current Genetics. (1999);  36 165-172
    CrossrefPubMedGoogle Scholar
  • 6 Downie S. R., Palmer J. D.. Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. Soltis, P. S. et al., eds. Molecular Systematics of Plants. New York; Chapman and Hall (1992): 14-35
    Google Scholar
  • 7 Dumolin-Lapègue S., Pemonge M. H., Petit R. J.. Association between chloroplast and mitochondrial lineages in oaks.  Molecular Biology and Evolution. (1998);  15 1321-1331
    PubMedGoogle Scholar
  • 8 Farris J. S.. The retention index and the rescaled consistency index.  Cladistics. (1989);  5 417-419
    PubMedGoogle Scholar
  • 9 Golenberg E. M., Clegg M. T., Durbin M. L., Doebley J., Ma D. P.. Evolution of a noncoding region of the chloroplast genome.  Molecular Phylogenetics and Evolution. (1993);  2 52-64
    CrossrefPubMedGoogle Scholar
  • 10 Graham S. W., Olmstead R. G.. Evolutionary significance of an unusual chloroplast DNA inversion found in two basal angiosperm lineages.  Current Genetics. (2000 a);  37 183-188
    CrossrefPubMedGoogle Scholar
  • 11 Graham S. W., Olmstead R. G.. Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms.  American Journal of Botany. (2000 b);  87 1712-1730
    PubMedGoogle Scholar
  • 12 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
    CrossrefPubMedGoogle Scholar
  • 13 Gruissem W.. Chloroplast gene expression: how plants turn their plastids on.  Cell. (1989);  56 161-170
    CrossrefPubMedGoogle Scholar
  • 14 He-Nygrén X.-L., Piippo S.. hylogenetic relationships of generic complex Chiloscyphus-Lophocolea-Heteroscyphus (Geocalycaceae, Hepaticae): Insights from three chloroplast genes and morphology.  Annales Botanici Fennici. (2003);  in press
    PubMedGoogle Scholar
  • 15 Hiratsuka J., Shimada H., Whittier R., Ishibashi T., Sakamoto M., Mori M., Kondo C., Honji Y., Sun C. R., Meng B. Y., Li Y. Q., Kanno A., Nishizawa Y., Hirai A., Shinozaki K., Sugiura M.. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals.  Molecular and General Genetics. (1989);  217 185-194
    PubMedGoogle Scholar
  • 16 Hong H., Hallik R. B.. Gene structure and expression of a novel Euglena gracilis chloroplast operon encoding cytochrome b6 and the b and e subunits of the H+-ATP synthase complex.  Current Genetics. (1994);  25 270-281
    CrossrefPubMedGoogle Scholar
  • 17 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
    PubMedGoogle Scholar
  • 18 Hupfer H., Swiatek M., Hornung S., Herrmann R. G., Maier R. M., Chiu W. L., Sears B.. Complete nucleotide sequence of the Oenothera elata plastid chromosome, representing plastome I of the five distinguishable euoenothera plastomes.  Molecular and General Genetics. (2000);  263 581-585
    PubMedGoogle Scholar
  • 19 Ignatov M., Huttunen S.. Brachytheciaceae (Bryophyta) - a family of sibling genera.  Arctoa. (2002);  11 245-296
    PubMedGoogle Scholar
  • 20 Johnson C. H., Schmidt G. W.. The psbB gene cluster of the Clamydomonas reinhardtii chloroplast: sequence and transcriptional analyses of psbN and psbH. .  Plant Molecular Biology. (1993);  22 645-658
    CrossrefPubMedGoogle Scholar
  • 21 Kato T., Kaneko T., Sato S., Nakamura Y., Tabata S.. Complete structure of the chloroplast genome of a legume, Lotus japonicus. .  DNA Research. (2000);  7 323-330
    PubMedGoogle Scholar
  • 22 Kelchner S. A., Wendel J. F.. Hairpins create minute inversions in non-coding regions of chloroplast DNA.  Current Genetics. (1996);  30 259-262
    CrossrefPubMedGoogle Scholar
  • 23 Kelchner S. A., Clark L. G.. Molecular evolution and phylogenetic utility of the chloroplast rpl16 intron in Chusquea and the Bambusoideae (Poaceae).  Molecular Phylogenetics and Evolution. (1997);  8 385-397
    CrossrefPubMedGoogle Scholar
  • 24 Kelchner S. A.. The Evolution of non-coding chloroplast DNA and its application in plant systematics.  Annals of the Missouri Botanical Gardens. (2000);  87 482-498
    PubMedGoogle Scholar
  • 25 Kluge A. G., Farris J. S.. Quantitative phyletics and the evolution of anurans.  Systematic Zoology. (1969);  18 1-32
    PubMedGoogle Scholar
  • 26 Kohchi T., Yoshida T., Komano T., Ohyama K.. Divergent mRNA transcription in the chloroplast psbB operon.  European Molecular Biology Organization Journal. (1988);  7 885-891
    PubMedGoogle Scholar
  • 27 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
    CrossrefPubMedGoogle Scholar
  • 28 Maier R. M., Neckermann K., Igloi G. L., Kossel H.. Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing.  Journal of Molecular Biology. (1995);  251 614-628
    CrossrefPubMedGoogle Scholar
  • 29 Mathews D. H., Zuker M., Turner D. H.. RNA structure 3.6. http//www.bioinfo.math.edu . (2001)
    Google Scholar
  • 30 Mes T. H. M., Kuperus P., Kirschner J., Štìpánek J., Oosterveld P., Štorchová H., den Nijs J. C. M.. Hairpins involving both inverted and direct repeats are associated with homoplasious indels in non-coding chloroplast DNA of Taraxacum (Lactuceae: Asteraceae).  Genome. (2000);  43 634-641
    CrossrefPubMedGoogle Scholar
  • 31 Müller J., Müller K.. QuickAlign: a new alignment editor.  Plant Molecular Biology Reporter. (2003);  21 5
    PubMedGoogle Scholar
  • 32 Müller K.. PRAT: Computer program for phylogeneticanalysis of large data sets. Program distributed by the author. Bonn; Botanical Institute, University of Bonn (2002)
    Google Scholar
  • 33 Nixon K. C.. The Parsimony Ratchet, a new method for rapid parsimony analysis.  Cladistics. (1999);  15 407-414
    PubMedGoogle Scholar
  • 34 Ogihara Y., Isono K., Kojima T., Endo A., Hanaoka M., Shiina T., Terachi T., Utsugi S., Murata M., Mori M., Takumi S., Ikeo K., Gojobori T., Murai R., Murai K., Matsuoka Y., Ohnishi Y., Tajiri H., Tsunewaki K.. Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA.  Molecular Genetics and Genomics. (2002);  266 740-746
    CrossrefPubMedGoogle Scholar
  • 35 Ohyama K., Fukuzawa H., Kohchi T., Shirai H., Sano T., Sano S., Umesono K., Shiki Y., Takeuchi M., Chang Z., Aota S., Inokuchi H., Ozeki H.. Chloroplast gene organization deduced from complete sequence of the liverwort Marchantia polymorpha chloroplast DNA.  Nature. (1986);  322 572-574
    CrossrefPubMedGoogle Scholar
  • 36 Quandt D.. Molecular evolution and phylogenetic utility of non-coding DNA: addressing relationships among pleurocarpous mosses. Bonn; University of Bonn (2002)
    Google Scholar
  • 38 Sang T., Crawford D. J., Stuessy T.. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeonicaeae).  American Journal of Botany. (1997);  84 1120-1136
    CrossrefPubMedGoogle Scholar
  • 39 Sato S., Nakamura Y., Kaneko A., Asamizu E., Tabata S.. Complete structure of the chloroplast genome of Arabidopsis thaliana. .  DNA Research. (1999);  6 283-290
    PubMedGoogle Scholar
  • 40 Schmitz-Linneweber C., Maier R. M., Alcaraz J. P., Cottet A., Herrmann R. G., Mache R.. The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization.  Plant Molecular Biology. (2001);  45 307-315
    CrossrefPubMedGoogle Scholar
  • 41 Shaw A. J.. Phylogeny of the Sphagnopsida based on chloroplast and nuclear DNA sequences.  Bryologist. (2000);  103 277-306
    PubMedGoogle Scholar
  • 42 Shinozaki K., Ohme M., Tanaka M., Wakasugi T., Hayashida N., Matsubayashi T., Zaita N., Chunwongse J., Obokata J., Yamaguchi-Shinozaki K., Ohto C., Torazawa K., Meng B. Y., Sugita M., Deno H., Kamogashira T., Yamada K., Kusuda J., Takaiwa F., Kato T., Tohdoh N., Shimada H., Sugiura M.. The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression.  European Molecular Biology Organization Journal. (1986);  5 2043-2049
    PubMedGoogle Scholar
  • 43 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.  Australian Journal of Botany. (2003);  in press
    PubMedGoogle Scholar
  • 44 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
    CrossrefPubMedGoogle Scholar
  • 45 Stern D. B., Jones H., Gruissem W.. Function of plastid mRNA 3′ inverted repeats. RNA stabilization and gene-specific protein binding.  Journal of Biological Chemistry. (1989);  264 18742-18750
    PubMedGoogle Scholar
  • 46 Stern D. B., Radwanski E. R., Kindle K. L.. A 3′ stem/loop structure of Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. .  Plant Cell. (1991);  3 285-297
    CrossrefPubMedGoogle Scholar
  • 47 Swofford D. L.. PAUP*4b10. Phylogenetic Analysis Using Parsimony (*and other Methods). Sunderland; Sinauer Associates (2002)
    Google Scholar
  • 48 Tsudzuki J., Nakashima K., Tsudzuki T., Hiratsuka J., Shibata M., Wakasugi T., Sugiura M.. Chloroplast DNA of black pine retains a residual inverted repeat lacking rRNA genes: nucleotide sequences of trnQ, trnK, psbA, trnI and trnH and the absence of rps16. .  Molecular and General Genetics. (1992);  232 206-214
    PubMedGoogle Scholar
  • 49 Turmel M., Otis C., Lemieux C.. The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: Insights into the architecture of ancestral chloroplast genomes.  Proceedings of the National Academy of Sciences USA. (1999);  96 10248-10253
    CrossrefPubMedGoogle Scholar
  • 50 Umesono K., Ozeki H.. Chloroplast gene organization in plants.  Trends in Genetics. (1987);  3 281-287
    CrossrefPubMedGoogle Scholar
  • 51 Wakasugi T., Tsudzuki J., Ito S., Nakashima K., Tsudzuki J., Sugiura M.. Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. .  Proceedings of the National Academy of Sciences USA. (1994);  91 9794-9798
    PubMedGoogle Scholar
  • 52 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
    CrossrefPubMedGoogle Scholar
  • 53 Wakasugi T., Nishikawa A., Yamada K., Sugiura M.. Complete nucleotide sequence of the chloroplast genome from a fern, Psilotum nudum. GenBank. NC 003386. (2002)
    Google Scholar
  • 54 Westhoff P., Herrmann R. G.. Complex RNA maturation in chloroplasts. The psbB operon from spinach.  European Journal of Biochemistry. (1988);  171 551-564
    CrossrefPubMedGoogle Scholar

D. Quandt

Rheinische Friedrich-Wilhelms-Universität Bonn
Botanisches Institut und Botanischer Garten, AG Bryologie

Meckenheimer Allee 170

53115 Bonn

Germany

Email: d.quandt@uni-bonn.de

Section Editor: F. Salamini

      >