Journal of Molecular Evolution

, Volume 29, Issue 3, pp 255–265 | Cite as

Phylogenetic relationships of the green algeVolvox carteri deduced from small-subunit ribosomal RNA comparisons

  • Helmut Rausch
  • Niels Larsen
  • Rüdiger Schmitt


The 1788-nucleotide sequence of the small-subunit ribosomal RNA (srRNA) coding region from the chlorophyteVolvox carteri was determined. The secondary structure bears features typical of the universal model of srRNA, including about 40 helices and a division into four domains. Phylogenetic relationships to 17 other eukaryotes, including two other chlorophytes, were explored by comparing srRNA sequences. Similarity values and the inspection of phylogenetic trees derived by distance matrix methods revealed a close relationship betweenV. carteri andChlamydomonas reinhardtii. The results are consistent with the view that these Volvocales, and the third green alga,Nanochlorum eucaryotum, are more closely related to higher plants than to any other major eukaryotic group, but constitute a distinct lineage that has long been separated from the line leading to the higher plants.

Key words

Green algae Volvox carteri Chlamydomonas reinhardtii Small-subunit rRNA sequence Eukaryotic phylogeny 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Benton WD, Davis RS (1977) Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196:180–183PubMedGoogle Scholar
  2. Bold HC, Wynne MJ (1985) Introduction to the algae, ed 2. Prentice-Hall, Englewood NJGoogle Scholar
  3. Dams E, Hendriks L, Van de Peer Y, Neefs JM, Smits G, Vandenbempt I, DeWachter R (1988) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 7:87–173Google Scholar
  4. Eckenrode V, Arnold J, Meagher RB (1985) Comparison of the nucleotide sequence of soybean 18S rRNA with the sequences of other small-subunit rRNAs. J Mol Evol 21:259–269Google Scholar
  5. Elwood HJ, Olsen GJ, Sogin ML (1985) The small-subunit ribosomal RNA gene sequence from the hypotrichous ciliateOxytricha nova andStylonychia pustulata. Mol Biol Evol 2:399–410PubMedGoogle Scholar
  6. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefPubMedGoogle Scholar
  7. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  8. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284PubMedGoogle Scholar
  9. Fox GE, Stackebrandt E, Hespell RB, Gibson J, Dyer TA, Wolfe RS, Balch WE, Tanner R, Magrum L, Zablen LB, Blakemore R, Gupta R, Bonen L, Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209:457–463PubMedGoogle Scholar
  10. Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7:1869–1885PubMedGoogle Scholar
  11. Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes and oomycetes. Proc Natl Acad Sci USA 84:5823–5827PubMedGoogle Scholar
  12. Gutell RR, Weiser B, Woese CR, Noller HF (1985) Comparative anatomy of 16S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol 32:155–216PubMedGoogle Scholar
  13. Harper JF, Mages W (1988) Organization and structure ofVolvox β-tubulin genes. Mol Gen Genet 213:315–324CrossRefPubMedGoogle Scholar
  14. Heinrich P (1986) Guidelines for quick and simple plasmid sequencing. Boehringer Monograph, MannheimGoogle Scholar
  15. Herzog M, Maroteaux L (1986) Dinoflagellate 17S rRNA sequence inferred from the gene sequence: evolutionary implications. Proc Natl Acad Sci USA 83:8644–8648Google Scholar
  16. Hori H, Osawa S (1979) Evolutioanary change in 5S RNA secondary structure and a phylogenetic tree of 54 5S RNA species. Proc Natl Acad Sci USA 76:381–385PubMedGoogle Scholar
  17. Huysmans E, DeWachter R (1986) Complication of small ribosomal subunit RNA sequences. Nucleic Acids Res 14:r77-r118Google Scholar
  18. Johnson RA, Walseth TF (1979) The enzymatic preparation of [α32P]nucleoside-triphosphates, cyclic [32P]AMP and cyclic [32P]GMP. Biochim Biophys Acta 562:11–23PubMedGoogle Scholar
  19. Kirk DL, Harper JF (1986) Genetic, biochemical, and molecular approaches toVolvox development and evolution. Int Rev Cytol 99:217–293PubMedGoogle Scholar
  20. Kochert G (1973) Colony differentiation in green algae. In: Coward SJ (ed) Developmental regulation. Academic Press, New York, pp 155–167Google Scholar
  21. Leffers H, Kjems J, Ostergaard L, Larsen N, Garrett RA (1987) Evolutionary relationships amongst the archaebacteria. A comparative study of 23S ribosomal RNAs of sulfur dependent extreme thermophile, an extreme halophile and a thermophile methanogene. J Mol Biol 195:43–61PubMedGoogle Scholar
  22. Mages W, Salbaum JM, Harper JF, Schmitt R (1988) Organization and structure ofVolvox α-tubulin genes. Mol Gen Genet 213:449–458CrossRefPubMedGoogle Scholar
  23. Maniatis T, Fritsch EF, Sambrock J (1982) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory. Cold Spring Harbor NYGoogle Scholar
  24. Mankin AS, Skryabin KG, Rubtsov PM (1986) Identification of ten additional nucleotides in the primary structure of yeast 18S rRNA. Gene 44:143–145CrossRefPubMedGoogle Scholar
  25. Matteucci MD, Caruthers MH (1981) Synthesis of deoxyoligonucleotides on a polymer support. J Am Chem Soc 103:3185–3191CrossRefGoogle Scholar
  26. Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base-specific chemical cleavages. Meth Enzymol 65:499–559PubMedGoogle Scholar
  27. McCarrol R, Olsen GJ, Stahl YD, Woese CR, Sogin ML (1983) Nucleotide sequence of theDictyostelium discoideum smallsubunit ribosomal ribonucleic acid inferred from the gene sequence: evolutionary implications. Biochemistry 22:5858–5868CrossRefGoogle Scholar
  28. Messing J, Carlson J, Hagen G, Rubenstein J, Oleson A (1984) Cloning and sequencing of the ribosomal RNA genes in maize: the 17S region. DNA 3:31–40PubMedGoogle Scholar
  29. Müller K, Schmitt R (1988) Histone genes ofVolvox carteri: DNA sequence and organization of two H3-H4 gene loci. Nucleic Acids Res 16:4121–4136PubMedGoogle Scholar
  30. Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86PubMedGoogle Scholar
  31. Raven PH, Evert RF, Eichorn SE (1986) Biology of plants, ed 4. Worth, New York.Google Scholar
  32. Raynal F, Michot B, Bachellerie J-P (1984) Complete nucleotide sequence of mouse 18S rRNA gene: comparison with other available homologs. FEBS Lett 167:263–268CrossRefPubMedGoogle Scholar
  33. Rubtsov PM, Musakhanov MM, Zakhayev VM, Krayev AS, Skryabin KG, Bayev AA (1980) The structure of the yeast ribosomal RNA genes. The complete sequence of the 18S ribosomal RNA gene fromSaccharomyces cerevisiae. Nucleic Acids Res 8:5779–5794PubMedGoogle Scholar
  34. Salim M, Maden BEH (1981) Nucleotide sequence ofXenopus laevis 18S ribosomal RNA inferred from gene sequence. Nature 291:205–208CrossRefPubMedGoogle Scholar
  35. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74:5463–5467PubMedGoogle Scholar
  36. Sargent M, Zahn R, Walters B, Gupta R, Kaine B (1988) Nucleotide sequence of the 18S rDNA from microalgaNanochlorum eucaryotum. Nucleic Acids Res 16:4156PubMedGoogle Scholar
  37. Sogin ML, Elwood HJ (1986) Primary structure of theParamecium tetraurelia small-subunit rRNA coding region: phylogenetic relationships within ciliophora. J Mol Evol 23:53–60PubMedGoogle Scholar
  38. Sogin ML, Elwood HJ, Gunderson JH (1986a) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83:1383–1387PubMedGoogle Scholar
  39. Sogin ML, Swanton MJ, Gunderson JH (1986a) Evolutionary the small-subunit ribosomal RNA gene from the hypotrichous ciliateEuplotes aediculatus. J Protozool 33:26–29PubMedGoogle Scholar
  40. Southern E (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517PubMedGoogle Scholar
  41. Spangler EA, Blackburn EH (1985) The nucleotide sequence of the 17S ribosomal RNA gene ofTetrahymena thermophila and the identification of point mutations resulting in resistance to the antibiotics paromomycin and hygromycin. J Biol Chem 160:6334–6340Google Scholar
  42. Starr RC (1969) Structure, reproduction and differentiation inVolvox carteri f.nagariensis Iyengar, strains HK10 and HK9. Arch Protistenkd 111:204–222Google Scholar
  43. Takaiwa F, Oono K, Sugiura M (1984) The complete nucleotide sequence of a rice 17S rRNA gene. Nucleic Acids Res 12:5441–5448PubMedGoogle Scholar
  44. Vieira J, Messing J (1982) The pUC plasmids an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259–268CrossRefPubMedGoogle Scholar
  45. Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrick BA, Woese CR (1987) Ribosomal RNA sequence suggests Microsporidia are extremely ancient eukaryotes. Nature 326:411–414CrossRefPubMedGoogle Scholar
  46. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedGoogle Scholar
  47. Woese CR, Gutell R, Gupta R, Noller HF (1983) Detailed analysis of the 16S-like ribosomal ribonucleic acids. Microbiol Rev 47:621–669PubMedGoogle Scholar
  48. Yates F, Kochert G (1976) Nucleic acid and protein differences inVolvox carteri cell types. Cytobios 15:7–21PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1989

Authors and Affiliations

  • Helmut Rausch
    • 1
  • Niels Larsen
    • 2
  • Rüdiger Schmitt
    • 1
  1. 1.Lehrstuhl für GenetikUniversität RegensburgRegensburgFederal Republic of Germany
  2. 2.Biostructural Chemistry, Institute of ChemistryAarhus UniversityAarhusDenmark

Personalised recommendations