Abstract
The mitochondrial genome displays a highly plastic architecture in the green algal division comprising the classes Prasinophyceae, Trebouxiophyceae, Ulvophyceae, and Chlorophyceae (Chlorophyta). The compact mitochondrial DNAs (mtDNAs) of Nephroselmis (Prasinophyceae) and Prototheca (Trebouxiophyceae) encode about 60 genes and have been ascribed an ‘ancestral’ pattern of evolution, whereas those of chlorophycean green algae are much more reduced in gene content and size. Although the mtDNA of the early-diverging ulvophyte Pseudendoclonium contains 57 conserved genes, it differs from ‘ancestral’ chlorophyte mtDNAs by its unusually large size (96 kb) and long intergenic spacers. To gain insights into the evolutionary trends of mtDNA in the Ulvophyceae, we have determined the complete mtDNA sequence of Oltmannsiellopsis viridis, an ulvophyte belonging to a distinct, early-diverging lineage. This 56,761 bp genome harbours 54 conserved genes, numerous repeated sequences, and only three introns. From our comparative analyses with Pseudendoclonium mtDNA, we infer that the mitochondrial genome of the last common ancestor of the two ulvophytes closely resembled that of the trebouxiophyte Prototheca in terms of gene content and gene density. Our results also provide strong evidence for the intracellular, interorganellar transfer of a group I intron and for two distinct events of intercellular, horizontal DNA transfer.
Similar content being viewed by others
Abbreviations
- DHE:
-
Double-hairpin element
- LSU:
-
Large subunit
- mtDNA:
-
Mitochondrial DNA
- ORF:
-
Open reading frame
- SDRs:
-
Short dispersed repeats
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Belfort M, Roberts RJ (1997) Homing endonucleases: keeping the house in order. Nucleic Acids Res 25:3379–3388
Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201
Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA 101:17747–17752
Boer PH, Gray MW (1991) Short dispersed repeats localized in spacer regions of Chlamydomonas reinhardtii mitochondrial DNA. Curr Genet 19:309–312
Burger G, Saint-Louis D, Gray MW, Lang BF (1999) Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11:1675–1694
Burke JM, Belfort M, Cech TR, Davies RW, Schweyen RJ, Shub DA, Szostak JW, Tabak HF (1987) Structural conventions for group I introns. Nucleic Acids Res 15:7217–7221
Chihara M, Inouye I, Takahata N (1986) Oltmannsiellopsis, a new genus of marine flagellate (Dunaliellaceae, Chlorophyceae). Arch Protistenkd 132:313–324
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
Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678
Denovan-Wright EM, Nedelcu AM, Lee RW (1998) Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol 36:285–295
Fluit AC, Schmitz FJ (1999) Class 1 integrons, gene cassettes, mobility, and epidemiology. Eur J Clin Microbiol Infect Dis 18:761–770
Fontaine JM, Goux D, Kloareg B, Loiseaux-de Goer S (1997) The reverse-transcriptase-like proteins encoded by group II introns in the mitochondrial genome of the brown alga Pylaiella littoralis belong to two different lineages which apparently coevolved with the group II ribosyme lineages. J Mol Evol 44:33–42
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
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hargraves PE, Steele RL (1980) Morphology and ecology of Oltmannsiella virida, sp. nov. (Chlorophyceae: Volvocales). Phycologia 19:96–102
Hauth AM, Maier UG, Lang BF, Burger G (2005) The Rhodomonas salina mitochondrial genome: bacteria-like operons, compact gene arrangement and complex repeat region. Nucleic Acids Res 33:4433–4442
Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638
Kroymann J, Zetsche K (1998) The mitochondrial genome of Chlorogonium elongatum inferred from the complete sequence. J Mol Evol 47:431–440
Kück U, Jekosch K, Holzamer P (2000) DNA sequence analysis of the complete mitochondrial genome of the green alga Scenedesmus obliquus: evidence for UAG being a leucine and UCA being a non-sense codon. Gene 253:13–18
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
Lang BF, Gray MW, Burger G (1999) Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet 33:351–397
Lazowska J, Jacq C, Slonimski PP (1980) Sequence of introns and flanking exons in wild-type and box3 mutants of cytochrome b reveals an interlaced splicing protein coded by an intron. Cell 22:333–348
Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556
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
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
Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30
Mower JP, Stefanovic S, Young GJ, Palmer JD (2004) Plant genetics: gene transfer from parasitic to host plants. Nature 432:165–166
Nakayama T, Watanabe S, Inouye I (1996) Phylogeny of wall-less green flagellates inferred from 18S rDNA sequence data. Phycol Res 44:151–161
Nedelcu AM (1997) Fragmented and scrambled mitochondrial ribosomal RNA coding regions among green algae: a model for their origin and evolution. Mol Biol Evol 14:506–517
Nedelcu AM (1998) Contrasting mitochondrial genome organizations and sequence affiliations among green algae: potential factors, mechanisms, and evolutionary scenarios. J Phycol 34:16–28
Nedelcu AM, Lee RW (1998) Short repetitive sequences in green algal mitochondrial genomes: potential roles in mitochondrial genome evolution. Mol Biol Evol 15:690–701
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
Nelson MJ, Green BR (2005) Double hairpin elements and tandem repeats in the non-coding region of Adenoides eludens chloroplast gene minicircles. Gene 358:102–110
O’Brien EA, Badidi E, Barbasiewicz A, deSousa C, Lang BF, Burger G (2003) GOBASE—a database of mitochondrial and chloroplast information. Nucleic Acids Res 31:176–178
Paquin B, Laforest MJ, Lang BF (2000) Double-hairpin elements in the mitochondrial DNA of Allomyces: evidence for mobility. Mol Biol Evol 17:1760–1768
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
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
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
Roberts RJ, Belfort M, Bestor T, Bhagwat AS, Bickle TA, Bitinaite J, Blumenthal RM, Degtyarev S, Dryden DT, Dybvig K, Firman K, Gromova ES, Gumport RI, Halford SE, Hattman S, Heitman J, Hornby DP, Janulaitis A, Jeltsch A, Josephsen J, Kiss A, Klaenhammer TR, Kobayashi I, Kong H, Kruger DH, Lacks S, Marinus MG, Miyahara M, Morgan RD, Murray NE, Nagaraja V, Piekarowicz A, Pingoud A, Raleigh E, Rao DN, Reich N, Repin VE, Selker EU, Shaw PC, Stein DC, Stoddard BL, Szybalski W, Trautner TA, Van Etten JL, Vitor JM, Wilson GG, Xu SY (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31:1805–1812
Turmel M, Lemieux C, Burger G, Lang BF, Otis C, Plante I, Gray MW (1999) The complete mitochondrial DNA sequences of Nephroselmis olivacea and Pedinomonas minor. Two radically different evolutionary patterns within green algae. Plant Cell 11:1717–1729
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
Wolff G, Plante I, Lang BF, Kück U, Burger G (1994) Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. J Mol Biol 237:75–86
Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA 100:10824–10829
Acknowledgements
We are grateful to Patrick Charlebois for his help with the analysis of conserved gene clusters. This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (to M.T. and C.L.). Nucleotide sequence data reported are available in the GenBank database under the accession number DQ365900.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Bock
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Pombert, JF., Beauchamp, P., Otis, C. et al. The complete mitochondrial DNA sequence of the green alga Oltmannsiellopsis viridis: evolutionary trends of the mitochondrial genome in the Ulvophyceae. Curr Genet 50, 137–147 (2006). https://doi.org/10.1007/s00294-006-0076-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-006-0076-z