Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1999 Sep;11(9):1717–1730. doi: 10.1105/tpc.11.9.1717

The complete mitochondrial DNA sequences of Nephroselmis olivacea and Pedinomonas minor. Two radically different evolutionary patterns within green algae.

M Turmel 1, C Lemieux 1, G Burger 1, B F Lang 1, C Otis 1, I Plante 1, M W Gray 1
PMCID: PMC144307  PMID: 10488238

Abstract

Green plants appear to comprise two sister lineages, Chlorophyta (classes Chlorophyceae, Ulvophyceae, Trebouxiophyceae, and Prasinophyceae) and Streptophyta (Charophyceae and Embryophyta, or land plants). To gain insight into the nature of the ancestral green plant mitochondrial genome, we have sequenced the mitochondrial DNAs (mtDNAs) of Nephroselmis olivacea and Pedinomonas minor. These two green algae are presumptive members of the Prasinophyceae. This class is thought to include descendants of the earliest diverging green algae. We find that Nephroselmis and Pedinomonas mtDNAs differ markedly in size, gene content, and gene organization. Of the green algal mtDNAs sequenced so far, that of Nephroselmis (45,223 bp) is the most ancestral (minimally diverged) and occupies the phylogenetically most basal position within the Chlorophyta. Its repertoire of 69 genes closely resembles that in the mtDNA of Prototheca wickerhamii, a later diverging trebouxiophycean green alga. Three of the Nephroselmis genes (nad10, rpl14, and rnpB) have not been identified in previously sequenced mtDNAs of green algae and land plants. In contrast, the 25,137-bp Pedinomonas mtDNA contains only 22 genes and retains few recognizably ancestral features. In several respects, including gene content and rate of sequence divergence, Pedinomonas mtDNA resembles the reduced mtDNAs of chlamydomonad algae, with which it is robustly affiliated in phylogenetic analyses. Our results confirm the existence of two radically different patterns of mitochondrial genome evolution within the green algae.

Full Text

The Full Text of this article is available as a PDF (144.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adachi J., Hasegawa M. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol. 1996 Apr;42(4):459–468. doi: 10.1007/BF02498640. [DOI] [PubMed] [Google Scholar]
  2. Boer P. H., Gray M. W. Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell. 1988 Nov 4;55(3):399–411. doi: 10.1016/0092-8674(88)90026-8. [DOI] [PubMed] [Google Scholar]
  3. Boer P. H., Gray M. W. Short dispersed repeats localized in spacer regions of Chlamydomonas reinhardtii mitochondrial DNA. Curr Genet. 1991 Apr;19(4):309–312. doi: 10.1007/BF00355060. [DOI] [PubMed] [Google Scholar]
  4. Boer P. H., Gray M. W. Transfer RNA genes and the genetic code in Chlamydomonas reinhardtii mitochondria. Curr Genet. 1988 Dec;14(6):583–590. doi: 10.1007/BF00434084. [DOI] [PubMed] [Google Scholar]
  5. Bonfield J. K., Smith K. f., Staden R. A new DNA sequence assembly program. Nucleic Acids Res. 1995 Dec 25;23(24):4992–4999. doi: 10.1093/nar/23.24.4992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buchheim M. A., Lemieux C., Otis C., Gutell R. R., Chapman R. L., Turmel M. Phylogeny of the Chlamydomonadales (Chlorophyceae): a comparison of ribosomal RNA gene sequences from the nucleus and the chloroplast. Mol Phylogenet Evol. 1996 Apr;5(2):391–402. doi: 10.1006/mpev.1996.0034. [DOI] [PubMed] [Google Scholar]
  7. Burger G., Plante I., Lonergan K. M., Gray M. W. The mitochondrial DNA of the amoeboid protozoon, Acanthamoeba castellanii: complete sequence, gene content and genome organization. J Mol Biol. 1995 Feb 3;245(5):522–537. doi: 10.1006/jmbi.1994.0043. [DOI] [PubMed] [Google Scholar]
  8. Colleaux L., Michel-Wolwertz M. R., Matagne R. F., Dujon B. The apocytochrome b gene of Chlamydomonas smithii contains a mobile intron related to both Saccharomyces and Neurospora introns. Mol Gen Genet. 1990 Sep;223(2):288–296. doi: 10.1007/BF00265065. [DOI] [PubMed] [Google Scholar]
  9. Côté V., Mercier J. P., Lemieux C., Turmel M. The single group-I intron in the chloroplast rrnL gene of Chlamydomonas humicola encodes a site-specific DNA endonuclease (I-ChuI). Gene. 1993 Jul 15;129(1):69–76. doi: 10.1016/0378-1119(93)90697-2. [DOI] [PubMed] [Google Scholar]
  10. Denovan-Wright E. M., Lee R. W. Comparative structure and genomic organization of the discontinuous mitochondrial ribosomal RNA genes of Chlamydomonas eugametos and Chlamydomonas reinhardtii. J Mol Biol. 1994 Aug 12;241(2):298–311. doi: 10.1006/jmbi.1994.1505. [DOI] [PubMed] [Google Scholar]
  11. Denovan-Wright E. M., Nedelcu A. M., Lee R. W. Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol. 1998 Jan;36(2):285–295. doi: 10.1023/a:1005995718091. [DOI] [PubMed] [Google Scholar]
  12. Dürrenberger F., Rochaix J. D. Chloroplast ribosomal intron of Chlamydomonas reinhardtii: in vitro self-splicing, DNA endonuclease activity and in vivo mobility. EMBO J. 1991 Nov;10(11):3495–3501. doi: 10.1002/j.1460-2075.1991.tb04913.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Felsenstein J. Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet. 1988;22:521–565. doi: 10.1146/annurev.ge.22.120188.002513. [DOI] [PubMed] [Google Scholar]
  14. Fontaine J. M., Rousvoal S., Leblanc C., Kloareg B., Loiseaux-de Goër S. The mitochondrial LSU rDNA of the brown alga Pylaiella littoralis reveals alpha-proteobacterial features and is split by four group IIB introns with an atypical phylogeny. J Mol Biol. 1995 Aug 18;251(3):378–389. doi: 10.1006/jmbi.1995.0441. [DOI] [PubMed] [Google Scholar]
  15. Gray M. W., Cedergren R., Abel Y., Sankoff D. On the evolutionary origin of the plant mitochondrion and its genome. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2267–2271. doi: 10.1073/pnas.86.7.2267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gray M. W., Lang B. F., Cedergren R., Golding G. B., Lemieux C., Sankoff D., Turmel M., Brossard N., Delage E., Littlejohn T. G. Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res. 1998 Feb 15;26(4):865–878. doi: 10.1093/nar/26.4.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hasegawa M., Kishino H., Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22(2):160–174. doi: 10.1007/BF02101694. [DOI] [PubMed] [Google Scholar]
  18. Hayashi-Ishimaru Y., Ohama T., Kawatsu Y., Nakamura K., Osawa S. UAG is a sense codon in several chlorophycean mitochondria. Curr Genet. 1996 Jun;30(1):29–33. doi: 10.1007/s002940050096. [DOI] [PubMed] [Google Scholar]
  19. Kessler U., Zetsche K. Physical map and gene organization of the mitochondrial genome from the unicellular green alga Platymonas (Tetraselmis) subcordiformis (Prasinophyceae). Plant Mol Biol. 1995 Dec;29(5):1081–1086. doi: 10.1007/BF00014979. [DOI] [PubMed] [Google Scholar]
  20. Kroymann J., Zetsche K. The mitochondrial genome of Chlorogonium elongatum inferred from the complete sequence. J Mol Evol. 1998 Oct;47(4):431–440. doi: 10.1007/pl00006400. [DOI] [PubMed] [Google Scholar]
  21. Lang B. F., Burger G., O'Kelly C. J., Cedergren R., Golding G. B., Lemieux C., Sankoff D., Turmel M., Gray M. W. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature. 1997 May 29;387(6632):493–497. doi: 10.1038/387493a0. [DOI] [PubMed] [Google Scholar]
  22. Lonergan K. M., Gray M. W. The ribosomal RNA gene region in Acanthamoeba castellanii mitochondrial DNA. A case of evolutionary transfer of introns between mitochondria and plastids? J Mol Biol. 1994 Jun 17;239(4):476–499. doi: 10.1006/jmbi.1994.1390. [DOI] [PubMed] [Google Scholar]
  23. Ma D. P., King Y. T., Kim Y., Luckett W. S., Jr The group I intron of apocytochrome b gene from Chlamydomonas smithii encodes a site-specific endonuclease. Plant Mol Biol. 1992 Mar;18(5):1001–1004. doi: 10.1007/BF00019218. [DOI] [PubMed] [Google Scholar]
  24. Martin N. C., Lang B. F. Mitochondrial RNase P: the RNA family grows. Nucleic Acids Symp Ser. 1997;(36):42–44. [PubMed] [Google Scholar]
  25. Oda K., Yamato K., Ohta E., Nakamura Y., Takemura M., Nozato N., Akashi K., Kanegae T., Ogura Y., Kohchi T. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol. 1992 Jan 5;223(1):1–7. doi: 10.1016/0022-2836(92)90708-r. [DOI] [PubMed] [Google Scholar]
  26. Palmer J. D. Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet. 1990 Apr;6(4):115–120. doi: 10.1016/0168-9525(90)90125-p. [DOI] [PubMed] [Google Scholar]
  27. Rochaix J. D., Rahire M., Michel F. The chloroplast ribosomal intron of Chlamydomonas reinhardii codes for a polypeptide related to mitochondrial maturases. Nucleic Acids Res. 1985 Feb 11;13(3):975–984. doi: 10.1093/nar/13.3.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Siegel R. W., Banta A. B., Haas E. S., Brown J. W., Pace N. R. Mycoplasma fermentans simplifies our view of the catalytic core of ribonuclease P RNA. RNA. 1996 May;2(5):452–462. [PMC free article] [PubMed] [Google Scholar]
  29. Smith S. W., Overbeek R., Woese C. R., Gilbert W., Gillevet P. M. The genetic data environment an expandable GUI for multiple sequence analysis. Comput Appl Biosci. 1994 Dec;10(6):671–675. doi: 10.1093/bioinformatics/10.6.671. [DOI] [PubMed] [Google Scholar]
  30. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Turmel M., Côté V., Otis C., Mercier J. P., Gray M. W., Lonergan K. M., Lemieux C. Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion). Mol Biol Evol. 1995 Jul;12(4):533–545. doi: 10.1093/oxfordjournals.molbev.a040234. [DOI] [PubMed] [Google Scholar]
  32. Turmel M., Mercier J. P., Côté M. J. Group I introns interrupt the chloroplast psaB and psbC and the mitochondrial rrnL gene in Chlamydomonas. Nucleic Acids Res. 1993 Nov 11;21(22):5242–5250. doi: 10.1093/nar/21.22.5242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Unseld M., Marienfeld J. R., Brandt P., Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997 Jan;15(1):57–61. doi: 10.1038/ng0197-57. [DOI] [PubMed] [Google Scholar]
  34. Vahrenholz C., Riemen G., Pratje E., Dujon B., Michaelis G. Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr Genet. 1993 Sep;24(3):241–247. doi: 10.1007/BF00351798. [DOI] [PubMed] [Google Scholar]
  35. Wakasugi T., Nagai T., Kapoor M., Sugita M., Ito M., Ito S., Tsudzuki J., Nakashima K., Tsudzuki T., Suzuki Y. 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 U S A. 1997 May 27;94(11):5967–5972. doi: 10.1073/pnas.94.11.5967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ward B. L., Anderson R. S., Bendich A. J. The mitochondrial genome is large and variable in a family of plants (cucurbitaceae). Cell. 1981 Sep;25(3):793–803. doi: 10.1016/0092-8674(81)90187-2. [DOI] [PubMed] [Google Scholar]
  37. Weiner J. H., Bilous P. T., Shaw G. M., Lubitz S. P., Frost L., Thomas G. H., Cole J. A., Turner R. J. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell. 1998 Apr 3;93(1):93–101. doi: 10.1016/s0092-8674(00)81149-6. [DOI] [PubMed] [Google Scholar]
  38. Wolff G., Plante I., Lang B. F., Kück U., Burger G. Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. Gene content and genome organization. J Mol Biol. 1994 Mar 18;237(1):75–86. doi: 10.1006/jmbi.1994.1210. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES