Skip to main content
SpringerLink
Log in

Distinctive architecture of the chloroplast genome in the chlorophycean green alga Stigeoclonium helveticum

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The chloroplast genome has experienced many architectural changes during the evolution of chlorophyte green algae, with the class Chlorophyceae displaying the lowest degree of ancestral traits. We have previously shown that the completely sequenced chloroplast DNAs (cpDNAs) of Chamydomonas reinhardtii (Chlamydomonadales) and Scenedesmus obliquus (Sphaeropleales) are highly scrambled in gene order relative to one another. Here, we report the complete cpDNA sequence of Stigeoclonium helveticum (Chaetophorales), a member of a third chlorophycean lineage. This genome, which encodes 97 genes and contains 21 introns (including four putatively trans-spliced group II introns inserted at novel sites), is remarkably rich in derived features and extremely rearranged relative to its chlorophycean counterparts. At 223,902 bp, Stigeoclonium cpDNA is the largest chloroplast genome sequenced thus far, and in contrast to those of Chlamydomonas and Scenedesmus, features no large inverted repeat. Interestingly, the pattern of gene distribution between the DNA strands and the bias in base composition along each strand suggest that the Stigeoclonium genome replicates bidirectionally from a single origin. Unlike most known trans-spliced group II introns, those of Stigeoclonium exhibit breaks in domains I and II. By placing our comparative genome analyses in a phylogenetic framework, we inferred an evolutionary scenario of the mutational events that led to changes in genome architecture in the Chlorophyceae.

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
Fig. 5

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Bremer K (1985) Summary of green plant phylogeny and classification. Cladistics 1:369–385

    Article  Google Scholar 

  • Buchheim MA, Michalopulos EA, Buchheim JA (2001) Phylogeny of the Chlorophyceae with special reference to the Sphaeropleales: a study of 18S and 26S rDNA data. J Phycol 37:819–835

    Article  CAS  Google Scholar 

  • de Cambiaire JC, Otis C, Lemieux C, Turmel M (2006) The complete chloroplast genome sequence of the chlorophycean green alga Scenedesmus obliquus reveals a compact gene organization and a biased distribution of genes on the two DNA strands. BMC Evol Biol 6:37

    Article  PubMed  CAS  Google Scholar 

  • Côté V, Mercier J-P, Lemieux C, Turmel M (1993) The single group-I intron in the chloroplast rrnL gene of Chlamydomonas humicola encodes a site-specific DNA endonuclease (I-ChuI). Gene 129:69–76

    Article  PubMed  Google Scholar 

  • Cui L, Leebens-Mack J, Wang L-S, Tang J, Rymarquis L, Stern DB, dePamphilis CW (2006) Adaptive evolution of chloroplast genome structure inferred using a parametric bootstrap approach. BMC Evol Biol 6:13

    Article  PubMed  CAS  Google Scholar 

  • Durocher V, Gauthier A, Bellemare G, Lemieux C (1989) An optional group I intron between the chloroplast small subunit rRNA genes of Chlamydomonas moewusii and C. eugametos. Curr Genet 15:277–282

    Article  PubMed  CAS  Google Scholar 

  • Friedl T (1997) The evolution of the green algae. Plant Syst Evol 11(Suppl):87–101

    CAS  Google Scholar 

  • Friedl T, O’Kelly CJ (2002) Phylogenetic relationships of green algae assigned to the genus Planophila (Chlorophyta): evidence from 18S rDNA sequence data and ultrastructure. Eur J Phycol 37:373–384

    Article  Google Scholar 

  • Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix JD (1991) A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65:135–143

    Article  PubMed  CAS  Google Scholar 

  • Grigoriev A (1998) Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res 26:2286–2290

    Article  PubMed  CAS  Google Scholar 

  • Guy L, Roten CA (2004) Genometric analyses of the organization of circular chromosomes: a universal pressure determines the direction of ribosomal RNA genes transcription relative to chromosome replication. Gene 340:45–52

    Article  PubMed  CAS  Google Scholar 

  • Heinhorst S, Cannon GC (1993) DNA replication in chloroplasts. J Cell Sci 104:1–9

    CAS  Google Scholar 

  • Knoop V, Altwasser M, Brennicke A (1997) A tripartite group II intron in mitochondria of an angiosperm plant. Mol Gen Genet 255:269–276

    Article  PubMed  CAS  Google Scholar 

  • Koller B, Delius H (1982) Origin of replication in chloroplast DNA of Euglena gracilis located close to the region of variable size. EMBO J 1:995–998

    PubMed  CAS  Google Scholar 

  • de Koning AP, Keeling PJ (2006) The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol 4:12

    Article  PubMed  CAS  Google Scholar 

  • Kück U (1989) The intron of a plastid gene from a green alga contains an open reading frame for a reverse transcriptase-like enzyme. Mol Gen Genet 218:257–265

    Article  PubMed  Google Scholar 

  • Kück U, Choquet Y, Schneider M, Dron M, Bennoun P (1987) Structural and transcription analysis of two homologous genes for the P700 chlorophyll a-apoproteins in Chlamydomonas reinhardii: evidence for in vivo trans-splicing. EMBO J 6:2185–2195

    PubMed  Google Scholar 

  • Kunnimalaiyaan M, Nielsen BL (1997) Chloroplast DNA replication: mechanism, enzymes and replication origins. J Plant Biochem Biotechnol 6:1–7

    CAS  Google Scholar 

  • Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642

    Article  PubMed  CAS  Google Scholar 

  • Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556

    Article  Google Scholar 

  • Lidholm J, Szmidt AE, Hällgren J-E, Gustafsson P (1988) The chloroplast genomes of conifers lack one of the rRNA-encoding inverted repeats. Mol Gen Genet 212:6–10

    Article  CAS  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  PubMed  CAS  Google Scholar 

  • Malek O, Knoop V (1998) Trans-splicing group II introns in plant mitochondria: the complete set of cis-arranged homologs in ferns, fern allies, and a hornwort. RNA 4:1599–1609

    Article  PubMed  CAS  Google Scholar 

  • Malek O, Brennicke A, Knoop V (1997) Evolution of trans-splicing plant mitochondrial introns in pre-Permian times. Proc Natl Acad Sci USA 94:553–558

    Article  PubMed  CAS  Google Scholar 

  • Mattox KR, Stewart KD (1984) Classification of the green algae: a concept based on comparative cytology. In: Irvine DEG, John DM (eds) The systematics of the green algae. Academic, London, pp 29–72

    Google Scholar 

  • Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH, Stern DB (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659–2679

    Article  PubMed  CAS  Google Scholar 

  • McCracken DA, Nadakavukaren MJ, Cain JR (1980) A biochemical and ultrastructural evaluation of the taxonomic position of Glaucosphaera vacuolata Korsch. New Phytol 86:39–44

    Article  CAS  Google Scholar 

  • Michel F, Ferat J-L (1995) Structure and activities of group II introns. Annu Rev Biochem 64:435–461

    Article  PubMed  CAS  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 

  • Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30

    Article  PubMed  CAS  Google Scholar 

  • Morton BR (1999) Strand asymmetry and codon usage bias in the chloroplast genome of Euglena gracilis. Proc Natl Acad Sci USA 96:5123–5128

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Bogorad L, Vasil I (eds) The molecular biology of plastids. Cell culture and somatic cell genetics of plants. Academic, San Diego, pp 5–53

    Google Scholar 

  • Palmer JD, Thompson WF (1981) Rearrangements in the chloroplast genomes of mung bean and pea. Proc Natl Acad Sci USA 78:5533–5537

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD, Thompson WF (1982) Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost. Cell 29:537–550

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD, Osorio B, Aldrich J, Thompson WF (1987) Chloroplast DNA evolution among legumes: loss of a large inverted repeat occurred prior to other sequence rearrangements. Curr Genet 11:275–286

    Article  CAS  Google Scholar 

  • Pombert JF, Otis C, Lemieux C, Turmel M (2004) The complete mitochondrial DNA sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) highlights distinctive evolutionary trends in the Chlorophyta and suggests a sister-group relationship between the Ulvophyceae and Chlorophyceae. Mol Biol Evol 21:922–935

    Article  PubMed  CAS  Google Scholar 

  • Pombert JF, Otis C, Lemieux C, Turmel M (2005) The chloroplast genome sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) reveals unusual structural features and new insights into the branching order of chlorophyte lineages. Mol Biol Evol 22:1903–1918

    Article  PubMed  CAS  Google Scholar 

  • Pombert JF, Lemieux C, Turmel M (2006) The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinctive quadripartite architecture in the chloroplast genome of early diverging ulvophytes. BMC Biol 4:3

    Article  PubMed  CAS  Google Scholar 

  • Ravel-Chapuis P, Heizmann P, Nigon V (1982) Electron microscopic localization of the replication origin of Euglena gracilis chloroplast DNA. Nature 300:78–81

    Article  CAS  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277

    Article  PubMed  CAS  Google Scholar 

  • Schwartz S, Zhang Z, Frazer KA, Smit A, Riemer C, Bouck J, Gibbs R, Hardison R, Miller W (2000) PipMaker—a web server for aligning two genomic DNA sequences. Genome Res 10:577–586

    Article  PubMed  CAS  Google Scholar 

  • Shoup S, Lewis LA (2003) Polyphyletic origin of parallel basal bodies in swimming cells of chlorophycean green algae (Chlorophyta). J Phycol 39:789–796

    Article  CAS  Google Scholar 

  • Sluiman HJ (1985) A cladistic evaluation of the lower and higher green plants (Viridiplantae). Plant Syst Evol 149:217–232

    Article  Google Scholar 

  • Stoddard BL (2005) Homing endonuclease structure and function. Q Rev Biophys 38:49–95

    Article  PubMed  CAS  Google Scholar 

  • Strauss SH, Palmer JD, Howe GT, Doerksen AH (1988) Chloroplast genomes of two conifers lack a large inverted repeat and are extensively rearranged. Proc Natl Acad Sci USA 85:3898–3902

    Article  PubMed  CAS  Google Scholar 

  • Tesler G (2002) GRIMM: genome rearrangements web server. Bioinformatics 18:492–493

    Article  PubMed  CAS  Google Scholar 

  • Tillier ER, Collins RA (2000a) Genome rearrangement by replication-directed translocation. Nat Genet 26:195–197

    Article  PubMed  CAS  Google Scholar 

  • Tillier ER, Collins RA (2000b) The contributions of replication orientation, gene direction, and signal sequences to base-composition asymmetries in bacterial genomes. J Mol Evol 50:249–257

    PubMed  CAS  Google Scholar 

  • Turmel M, Boulanger J, Lemieux C (1989) Two group I introns with long internal open reading frames in the chloroplast psbA gene of Chlamydomonas moewusii. Nucleic Acids Res 17:3875–3887

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Boulanger J, Schnare MN, Gray MW, Lemieux C (1991) Six group I introns and three internal transcribed spacers in the chloroplast large subunit ribosomal RNA gene of the green alga Chlamydomonas eugametos. J Mol Biol 218:293–311

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Gutell RR, Mercier J-P, Otis C, Lemieux C (1993a) Analysis 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

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Mercier JP, Côté MJ (1993b) Group I introns interrupt the chloroplast psaB and psbC and the mitochondrial rrnL gene in Chlamydomonas. Nucleic Acids Res 21:5242–5250

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Choquet Y, Goldschmidt-Clermont M, Rochaix JD, Otis C, Lemieux C (1995a) The trans-spliced intron 1 in the psaA gene of the Chlamydomonas chloroplast: a comparative analysis. Curr Genet 27:270–279

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Côté V, Otis C, Mercier J-P, Gray MW, Lonergan KM, Lemieux C (1995b) Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion). Mol Biol Evol 12:533–545

    PubMed  CAS  Google Scholar 

  • Turmel M, Lemieux C, Burger G, Lang BF, Otis C, Plante I, Gray MW (1999a) The complete mitochondrial DNA sequences of Nephroselmis olivacea and Pedinomonas minor. Two radically different evolutionary patterns within green algae. Plant Cell 11:1717–1729

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (1999b) The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci USA 96:10248–10253

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2002) 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. Proc Natl Acad Sci USA 99:11275–11280

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2005) The complete chloroplast DNA sequences of the charophycean green algae Staurastrum and Zygnema reveal that the chloroplast genome underwent extensive changes during the evolution of the Zygnematales. BMC Biol 3:22

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23:1324–1338

    Article  PubMed  CAS  Google Scholar 

  • Volfovsky N, Haas BJ, Salzberg SL (2001) A clustering method for repeat analysis in DNA sequences. Genome Biol 2:Research0027

    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

    Article  PubMed  CAS  Google Scholar 

  • Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA 94:5967–5972

    Article  PubMed  CAS  Google Scholar 

  • Watanabe S, Floyd GL (1989) Ultrastructure of the quadriflagellate zoospores of the filamentous green algae Chaetophora incrassata and Pseudoschizomeris caudata (Chaetophorales, Chlorophyceae) with emphasis on the flagellar apparatus. Bot Mag Tokyo 102:533–546

    Article  Google Scholar 

Download references

Acknowledgments

We thank Jean-François Pombert and Jean-Charles de Cambiaire for their help with the sequence analyses and for critical reading of the manuscript. This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (to C.L. and M.T.).

Author information

Authors and Affiliations

  1. Département de biochimie et de microbiologie, Pavillon Charles-Eugène Marchand, Université Laval, Quebec City, QC, Canada, G1K 7P4

    Anne-Sophie Bélanger, Jean-Simon Brouard, Patrick Charlebois, Christian Otis, Claude Lemieux & Monique Turmel

Authors
  1. Anne-Sophie Bélanger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Simon Brouard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrick Charlebois
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Otis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Claude Lemieux
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Monique Turmel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Monique Turmel.

Additional information

Communicated by R. Herrmann.

Nucleotide sequence data reported are available in the GenBank database under the accession number DQ630521.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bélanger, AS., Brouard, JS., Charlebois, P. et al. Distinctive architecture of the chloroplast genome in the chlorophycean green alga Stigeoclonium helveticum . Mol Genet Genomics 276, 464–477 (2006). https://doi.org/10.1007/s00438-006-0156-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-006-0156-2

Keywords

Search

Navigation