Skip to main content
Log in

Evolution of linear mitochondrial DNA in three known lineages of Polytomella

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Although DNA sequences of linear mitochondrial genomes are available for a wide variety of species, sequence and conformational data from the extreme ends of these molecules (i.e., the telomeres) are limited. Data on the telomeres is important because it can provide insights into how linear genomes overcome the end-replication problem. This study explores the evolution of linear mitochondrial DNAs (mtDNAs) in the green-algal genus Polytomella (Chlorophyceae, Chlorophyta), the members of which are non-photosynthetic. Earlier works analyzed the linear and linear-fragmented mitochondrial genomes of Polytomella capuana and Polytomella parva. Here we present the mtDNA sequence for Polytomella strain SAG 63-10 [also known as Polytomella piriformis (Pringsheim 1963)], which is the only known representative of a mostly unexplored Polytomella lineage. We show that the P. piriformis mtDNA is made up of two linear fragments of 13 and 3 kb. The telomeric sequences of the large and small fragments are terminally inverted, and appear to end in vitro with either closed (hairpin-loop) or open (nicked-loop) structures as also shown here for P. parva and shown earlier for P. capuana. The structure of the P. piriformis mtDNA is more similar to that of P. parva, which is also fragmented, than to that of P. capuana, which is contained in a single chromosome. Phylogenetic analyses reveal high substitution rates in the mtDNA of all three Polytomella species relative to other chlamydomonadalean algae. These elevated rates could be the result of a greater number of vegetative cell divisions and/or small population sizes in Polytomella species as compared with other chlamydomonadalean algae.

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

Access this article

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

Similar content being viewed by others

References

  • Bah A, Bachand F, Clair E, Autexier C, Wellinger RJ (2004) Humanized telomeres and an attempt to express a functional human telomerase in yeast. Nucleic Acids Res 32:1917–1927

    Article  CAS  PubMed  Google Scholar 

  • Baroudy BM, Venkatesan S, Moss B (1983) Structure and replication of vaccinia virus telomeres. Cold Spring Harb Symp Quant Biol 47:723–729

    PubMed  Google Scholar 

  • Bateman AJ (1975) Simplification of palindromic telomere theory. Nature 253:379–380

    Article  CAS  PubMed  Google Scholar 

  • Borza T, Redmond EK, Laflamme M, Lee RW (2009) Mitochondrial DNA in the Oogamochlamys clade (Chlorophyceae): high GC content and unique genome architecture for green algae. J Phycol 45:1323–1334

    Article  CAS  Google Scholar 

  • Boudreau E, Turmel M (1995) Gene rearrangements in Chlamydomonas chloroplast DNAs are accounted for by inversions and by the expansion/contraction of the inverted repeat. Plant Mol Biol 27:351–364

    Article  CAS  PubMed  Google Scholar 

  • Boudreau E, Otis C, Turmel M (1994) Conserved gene clusters in the highly rearranged chloroplast genomes of Chlamydomonas moewusii and Chlamydomonas reinhardtii. Plant Mol Biol 24:585–602

    Article  CAS  PubMed  Google Scholar 

  • Burger G, Zhu Y, Littlejohn TG, Greenwood SJ, Schnare MN, Lang BF, Gray MW (2000) Complete sequence of the mitochondrial genome of Tetrahymena pyriformis and comparison with Paramecium aurelia mitochondrial DNA. J Mol Biol 297:365–380

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1974) Palindromic base sequences and replication of eukaryote chromosome ends. Nature 250:467–470

    Article  CAS  PubMed  Google Scholar 

  • Coleman AW, Thompson WF, Coff LJ (1991) Identification of the mitochondrial genome in the chrysophyte alga Ochromonas danica. J Protozool 38:129–135

    CAS  Google Scholar 

  • Denovan-Wright EM, Nedelcu AM, Lee RW (1998) Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol 36:285–295

    Article  CAS  PubMed  Google Scholar 

  • Dinouël N, Drissi R, Miyakawa I, Sor F, Rousset S, Fukuhara H (1993) Linear mitochondrial DNAs of yeasts: closed-loop structure of the termini and possible linear-circular conversion mechanisms. Mol Cell Biol 13:2315–2323

    PubMed  Google Scholar 

  • Fan J, Lee RW (2002) Mitochondrial genome of the colorless green alga Polytomella parva: two linear DNA molecules with homologous inverted repeat termini. Mol Biol Evol 19:999–1007

    CAS  PubMed  Google Scholar 

  • Förstemann K, Höss M, Lingner J (2000) Telomerase-dependent repeat divergence at the 3′ ends of yeast telomeres. Nucleic Acids Res 28:2690–2694

    Article  PubMed  Google Scholar 

  • González A, Talavera A, Almendral JM, Viñuela E (1986) Hairpin loop structure of African swine fever virus DNA. Nucleic Acids Res 14:6835–6844

    Article  PubMed  Google Scholar 

  • Gray MW, Boer PH (1988) Organization and expression of algal (Chlamydomonas reinhardtii) mitochondrial DNA. Philos Trans R Soc B 319:135–147

    Article  CAS  Google Scholar 

  • Handa H (2007) Linear plasmids in plant mitochondria: peaceful coexistences or malicious invasions? Mitochondrion 8:15–25

    Article  Google Scholar 

  • Hinnebusch J, Barbour AG (1991) Linear plasmids of Borrelia burgdorferi have a telomeric structure and sequence similar to those of a eukaryotic virus. J Bacteriol 173:7233–7239

    CAS  PubMed  Google Scholar 

  • Kairo A, Fairlamb AH, Gobright E, Nene V (1994) A 7.1 kb linear DNA molecule of Theileria parva has scrambled rDNA sequences and open reading frames for mitochondrially encoded proteins. EMBO J 13:898–905

    CAS  PubMed  Google Scholar 

  • Katz LA, Curtis EA, Pfunder M, Landweber LF (2000) Characterization of novel sequences from distantly related taxa by walking PCR. Mol Phylogenet Evol 14:318–321

    Article  CAS  PubMed  Google Scholar 

  • Kayal E, Lavrov DV (2008) The mitochondrial genome of Hydra oligactis (Cnidaria, Hydrozoa) sheds new light on animal mtDNA evolution and cnidarian phylogeny. Gene 410:177–186

    Article  CAS  PubMed  Google Scholar 

  • Kroymann J, Zetsche K (1998) The mitochondrial genome of Chlorogonium elongatum inferred from the complete sequence. J Mol Evol 47:431–440

    Article  CAS  PubMed  Google Scholar 

  • Laflamme M, Lee RW (2003) Mitochondrial genome conformation among CW-group chlorophycean algae. J Phycol 39:213–220

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mallet MA, Lee RW (2006) Identification of three distinct Polytomella lineages based on mitochondrial DNA features. J Eukaryot Microbiol 53:79–84

    Article  CAS  PubMed  Google Scholar 

  • Michaelis G, Vahrenholz C, Pratje E (1990) Mitochondrial DNA of Chlamydomonas reinhardtii: the gene for apocytochrome b and the complete functional map of the 15.8 kb DNA. Mol Gen Genet 223:211–216

    CAS  PubMed  Google Scholar 

  • Miyashita S, Hirochika H, Ikeda JE, Hashiba T (1990) Linear plasmid DNAs of the plant pathogenic fungus Rhizoctonia solani with unique terminal structures. Mol Gen Genet 220:165–171

    Article  CAS  PubMed  Google Scholar 

  • Moore LJ, Coleman AW (1989) The linear 20 kb mitochondrial genome of Pandorina morum (Volvocaceae, Chlorophyta). Plant Mol Biol 13:459–465

    Article  CAS  PubMed  Google Scholar 

  • Nakada T, Misawa K, Nozaki H (2008) Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Mol Phylogenet Evol 48:281–291

    Article  CAS  PubMed  Google Scholar 

  • Nash EA, Barbrook AC, Edwards-Stuart RK, Bernhardt K, Howe CJ, Nisbet RE (2007) Organization of the mitochondrial genome in the dinoflagellate Amphidinium carterae. Mol Biol Evol 24:1528–1536

    Article  CAS  PubMed  Google Scholar 

  • Nedelcu AM, Lee RW, Lemieux C, Gray MW, Burger G (2000) The complete mitochondrial DNA sequence of Scenedesmus obliquus reflects an intermediate stage in the evolution of the green algal mitochondrial genome. Genome Res 10:819–831

    Article  CAS  PubMed  Google Scholar 

  • Nosek J, Tomáska L (2002) Mitochondrial telomeres: alternative solutions to the end-replication problem. In: Krupp G, Parwaresch R (eds) Telomerases telomeres and cancer. Kluwer/Plenum Publishers, New York, pp 396–417

    Google Scholar 

  • Nosek J, Tomáska L (2003) Mitochondrial genome diversity: evolution of the molecular architecture and replication strategy. Curr Genet 44:73–84

    Article  CAS  PubMed  Google Scholar 

  • Nosek J, Tomáska L, Kucejová B (2004a) The chromosome end replication: lessons from mitochondrial genetics. J Appl Biomed 2:71–79

    CAS  Google Scholar 

  • Nosek J, Novotna M, Hlavatovicova Z, Ussery DW, Fajkus J, Tomáska L (2004b) Complete DNA sequence of the linear mitochondrial genome of the pathogenic yeast Candida parapsilosis. Mol Genet Genom 272:173–180

    CAS  Google Scholar 

  • Olovnikov AM (1971) Principle of marginotomy in template synthesis of polynucleotides. Dokl Akad Nauk SSSR 201:1496–1499

    CAS  PubMed  Google Scholar 

  • Popescu CE, Lee RW (2007) Mitochondrial genome sequence evolution in Chlamydomonas. Genetics 175:819–826

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pringsheim EG (1955) The Genus Polytomella. J Protozool 2:137–145

    Google Scholar 

  • Pringsheim EG (1963) Farblose Algen. Ein Beitrag zur Evolutionsforschung. Gustav Fischer, Stuttgart

    Google Scholar 

  • Pritchard AE, Cummings DJ (1981) Replication of linear mitochondrial DNA from Paramecium: sequence and structure of the initiation-end crosslink. Proc Natl Acad Sci USA 78:7341–7345

    Article  CAS  PubMed  Google Scholar 

  • Pröschold T, Marin B, Schlösser UG, Melkonian M (2001) Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152:265–300

    Article  PubMed  Google Scholar 

  • Rohozinski J, Girton LE, Van Etten JL (1989) Chlorella viruses contain linear nonpermuted double-stranded DNA genomes with covalently closed hairpin ends. Virology 168:363–369

    Article  CAS  PubMed  Google Scholar 

  • Ryan R, Grant D, Chiang KS, Swift H (1978) Isolation and characterization of mitochondrial DNA from Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 75:3268–3272

    Article  CAS  PubMed  Google Scholar 

  • Shao Z, Graf S, Chaga OY, Lavrov DV (2006) Mitochondrial genome of the moon jelly Aurelia aurita (Cnidaria, Scyphozoa): a linear DNA molecule encoding a putative DNA-dependent DNA polymerase. Gene 381:92–101

    Article  CAS  PubMed  Google Scholar 

  • Shukla GC, Nene V (1998) Telomeric features of Theileria parva mitochondrial DNA derived from cycle sequence data of total genomic DNA. Mol Biochem Parasitol 95:159–163

    Article  CAS  PubMed  Google Scholar 

  • Smith DR, Lee RW (2008a) Nucleotide diversity in the mitochondrial and nuclear compartments of Chlamydomonas reinhardtii: investigating the origins of genome architecture. BMC Evol Biol 8:156

    Article  PubMed  Google Scholar 

  • Smith DR, Lee RW (2008b) Mitochondrial genome of the colorless green alga Polytomella capuana: a linear molecule with an unprecedented GC content. Mol Biol Evol 25:487–496

    Article  CAS  PubMed  Google Scholar 

  • Smith DR, Lee RW (2009) The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA. BMC Genom 10:132

    Article  Google Scholar 

  • Smith DR, Lee RW (2010) Low nucleotide diversity for the expanded organelle and nuclear genomes of Volvox carteri supports the mutational-hazard hypothesis. Mol Biol Evol 27:1–13

    Article  Google Scholar 

  • Smith DR, Lee RW, Cushman JC, Magnuson JK, Tran D, Polle JEW (2010) The Dunaliella salina organelle genomes: large sequences, inflated with intronic and intergenic DNA. BMC Plant Biol 10:83

    Article  PubMed  Google Scholar 

  • Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V (1999) Plant mitochondrial RNA editing. J Mol Evol 48:303–312

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (and other methods, 4.0 Beta. Sinauer Associates, Sunderland

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Traktman P (1996) Poxvirus DNA replication. In: DePamphilis ML (ed) DNA replication in eukaryotic cells. Cold Spring Harbour Laboratory Press, Cold Spring Harbor, pp 775–798

    Google Scholar 

  • Turmel M, Otis C, Lemieux C (2010) A deviant genetic code in the reduced mitochondrial genome of the picoplanktonic green alga Pycnococcus provasolii. J Mol Evol 70:203–214

    Article  CAS  Google Scholar 

  • Vahrenholz C, Riemen G, Pratje E, Dujon B, Michaelis G (1993) Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr Genet 24:241–247

    Article  CAS  PubMed  Google Scholar 

  • Voigt O, Erpenbeck D, Wörheide G (2008) A fragmented metazoan organellar genome: the two mitochondrial chromosomes of Hydra magnipapillata. BMC Genom 9:350

    Article  Google Scholar 

  • Watson JD (1972) Origin of concatemeric T7 DNA. Nat New Biol 239:197–201

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Tudor Borza for insightful discussions during the data analysis. This work was supported by a grant to RWL from the Natural Sciences and Engineering Research Council (NSERC) of Canada. DRS is an Izaak Walton Killam Memorial Scholar and holds a Canada Graduate Scholarship from NSERC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Roy Smith.

Additional information

Communicated by L. Tomaska.

Sequence data from this article have been deposited in GenBank under accession numbers GU108480 and GU108481.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, D.R., Hua, J. & Lee, R.W. Evolution of linear mitochondrial DNA in three known lineages of Polytomella . Curr Genet 56, 427–438 (2010). https://doi.org/10.1007/s00294-010-0311-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-010-0311-5

Keywords

Navigation