Skip to main content
Log in

Ribosomal RNA sequence comparisons demonstrate an evolutionary relationship betweenZygnematales and charophytes

  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The nuclear-encoded small subunit ribosomal RNA (rRNA) sequences were determined forGenicularia spirotaenia, Mesotaenium caldariorum, andStaurastrum spec. (Zygnematales) to elucidate the evolutionary position of these green algae. Results of neighbour-joining and maximum parsimony phylogenetic analyses support a monophyletic origin of theZygnematales within the evolutionary assemblage defined by theCharophyceae (sensuMattox & Stewart) and land plants. TheZygnematales/Charophyceae/land plants are evolutionarily distinct from the monophyletic lineage defined by theChlorodendrales, Pseudoscourfieldiales, and theMicrothamniales/Chlorophyceae.

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.

Similar content being viewed by others

References

  • Bakker, M. E., Lokhorst, G. M., 1987: Ultrastructure of mitosis and cytokinesis inZygnema spec. (Zygnematales, Chlorophyta). — Protoplasma138: 105–118.

    Google Scholar 

  • Baldauf, S. L., Manhart, J. R., Palmer, J. D., 1990: Different fates of the chloroplasttufA gene following its transfer to the nucleus in green algae. — Proc. Natl. Acad. Sci. USA87: 5317–5321.

    PubMed  Google Scholar 

  • Bhattacharya, D., Medlin, L., Wainright, P. O., Ariztia, E. V., Bibeau, C., Stickel, S. K., Sogin, M. L., 1992: Algae containing chlorophyll a+c are polyphyletic: molecular evolutionary analysis of theChromophyta. — Evolution46: 1801–1817.

    Google Scholar 

  • Bourrelly, P., 1966: Les algues d'eau douce. I. — Algues vertes — Paris: Boubeé.

    Google Scholar 

  • Bremer, K., Humphries, C. J., Mishler, B. D., Churchill, S. P., 1987: On cladistic relationships in green plants. — Taxon36: 339–349.

    Google Scholar 

  • Cech, T. R., 1988: Conserved sequences and structures of group I introns: building an active site for RNA catalysis — a review. — Gene73: 259–271.

    PubMed  Google Scholar 

  • Chapman, R. L., Buchheim, M. A., 1991: Ribosomal RNA sequences: analysis and significance in the phylogeny and taxonomy of green algae. — Crit. Rev. Pl. Sci.10: 343–368.

    Google Scholar 

  • , 1992: Green algae and the evolution of land plants: inferences from nuclear-encoded rRNA gene sequences. — BioSystems28: 127–137.

    PubMed  Google Scholar 

  • De Jesus, M., Tabatabai, F., Chapman, D. J., 1989: Taxonomic distribution of copperzinc superoxide dismutase in green algae and its phylogenetic importance. — J. Phycol.25: 767–772.

    Google Scholar 

  • Devereux, R., Loeblich III, A. R., Fox, G. E., 1990: Higher plant origins and the phylogeny of green algae. — J. Mol. Evol.31: 18–24.

    PubMed  Google Scholar 

  • Elwood, H. J., Olsen, G. J., Sogin, M. L., 1985: The small subunit ribosomal RNA gene sequences from the hypotrichous ciliatesOxytricha nova andStylonychia pustulata. — Mol. Biol. Evol.2: 399–410.

    PubMed  Google Scholar 

  • Engels, M., Mix, M., 1980: 1. Nachtrag zur Liste der Sammlung von Conjugaten-Kulturen im Institut für Allgemeine Botanik der Universität Hamburg. — Mitt. Inst. Allg. Bot. Hamburg17: 165–171.

    Google Scholar 

  • Fang, G., Hammar, S., Grumet, R., 1992: A quick and inexpensive method for removing polysaccharides from plant genomic DNA. — BioTechniques13: 52–55.

    PubMed  Google Scholar 

  • Felsenstein, J., 1978: Cases in which parsimony and compatibility methods will be positively misleading. — Syst. Zool.27: 401–410.

    Google Scholar 

  • , 1981: Evolutionary trees from DNA sequences: a maximum likelihood approach. — J. Mol. Evol.17: 368–376.

    PubMed  Google Scholar 

  • , 1985: Confidence limits on phylogenies: an approach using the bootstrap. — Evolution39: 783–791.

    Google Scholar 

  • , 1991: PHYLIP (Phylogeny Inference Package); Manual Version 3.4. — Seattle: University of Washington.

    Google Scholar 

  • Frederick, S. E., Gruber, P. J., Tolbert, N. E., 1973: The occurrence of glycolate dehydrogenase and glycolate oxidase in green plants. An evolutionary survey. — Pl. Physiol.52: 318–323.

    Google Scholar 

  • Galway, M. E., Hardham, A. R., 1991: Immunofluorescent localization of microtubules throughout the cell cycle in the green algaMougeotia (Zygnemataceae). — Amer. J. Bot.78: 451–461.

    Google Scholar 

  • Gerrath, F. J., 1993: The biology of desmids: a decade of progress. — InRound, F. E., Chapman, D. J., (Eds): Prog. Phycol. Res.9, pp. 79–192. — Bristol: Biopress.

    Google Scholar 

  • Giddings, T. H., Brower, D. L., Staehelin, L. A., 1980: Visualization of particle complexes in the plasma membrane ofMicrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls. — J. Cell Biol.84: 327–339.

    PubMed  Google Scholar 

  • Graham, L. E., Kaneko, Y., 1991: Subcellular structures of relevance to the origin of the land plants (embryophytes) from green algae. — Crit. Rev. Pl. Sci.10: 323–342.

    Google Scholar 

  • , 1991: Phylogenetic connections between the “green algae” and the “Bryophytes”. — Adv. Bryol.4: 213–244.

    Google Scholar 

  • Gross, W., 1993: Peroxisomes in algae: their distribution, biochemical function and phylogenetic importance. — InRound, F. E., Chapman, D. J., (Eds): Prog. Phycol. Res.9, pp. 47–78. — Bristol: Biopress.

    Google Scholar 

  • Herth, W., 1983: Arrays of plasma-membrane “rosettes” involved in cellulose microfibril formation ofSpirogyra. — Planta159: 347–356.

    Google Scholar 

  • Hillis, D. M., Larson, A., Davis, S. K., Zimmer, E., 1990: Nucleic acids III: sequencing. — InHillis, D. M., Moritz, C. (Eds): Molecular systematics, pp. 318–370. — Sunderland, MA: Sinauer.

    Google Scholar 

  • Hoshaw, R. W., McCourt, R. M., 1988: TheZygnemataceae (Chlorophyta): a twenty-year update of research. — Phycologia27: 511–548.

    Google Scholar 

  • Hotchkiss, A. T. JR., Brown, R. M. JR., 1987: The association of rosette and globule terminal complexes with cellulose microfibril assembly inNitella translucens var.axillaris (Charophyceae). — J. Phycol.23: 229–237.

    Google Scholar 

  • , 1989: The composition and phylogenetic significance of theMougeotia (Charophyceae) cell wall. — J. Phycol.25: 646–654.

    Google Scholar 

  • Hultman, T., Bergh, S., Moks, T., Uhlen, M., 1991: Bidirectional solid-phase sequencing of in vitro-amplified plasmid DNA. — BioTechniques10: 84–93.

    PubMed  Google Scholar 

  • Huss, V. A. R., Sogin, M. L., 1990: Phylogenetic position of someChlorella species within theChlorococcales based upon complete small-subunit ribosomal RNA sequences. — J. Mol. Evol.31: 432–442.

    PubMed  Google Scholar 

  • , 1993: Sequence announcements. — Pl. Mol. Biol.22: 557–560.

    Google Scholar 

  • Jarman, M., Pickett-Heaps, J., 1990: Cell division and nuclear movement in the saccoderm desmidNetrium interruptus. — Protoplasma157: 136–143.

    Google Scholar 

  • Jukes, T. H., Cantor, C. R., 1969: Evolution of protein molecules. — InMunro, H. N., (Ed.): Mammalian protein molecules, pp. 21–132. — New York: Academic Press.

    Google Scholar 

  • Kattner, E., Lorch, D., Weber, A., 1977: Die Bausteine der Zellwand und der Gallerte eines Stammes vonNetrium digitus (Ehrbg.)Itzigs. u.Rothe. — Mitt. Inst. Allg. Bot. Hamburg15: 33–39.

    Google Scholar 

  • Kies, L., 1967: Über Zellteilung und Zygotenbildung beiRoya obtusa (Bre.)West & West. — Mitt. Inst. Allg. Bot. Hamburg12: 35–42.

    Google Scholar 

  • Kouwets, F. A. C., Coesel, P. F. M., 1984: Taxonomic revision of the conjugatophycean familyPeniaceae on the basis of cell wall ultrastructure. — J. Phycol.20: 555–562.

    Google Scholar 

  • Lütkemüller, J., 1902: Die Zellmembran der Desmidiaceen. — Beitr. Biol. Pflanzen8: 347–414.

    Google Scholar 

  • Manhart, J. R., Palmer, J. D., 1990: The gain of two chloroplast tRNA introns mark the green algal ancestors of land plants. — Nature345: 268–270.

    PubMed  Google Scholar 

  • Margulis, L., Corliss, J. O., Melkonian, M., Chapman, D. J., 1990: Handbook of Protoctista. — Boston: Jones and Bartlett.

    Google Scholar 

  • Mattox, K. R., Stewart, K. D., 1984: Classification of the green algae: a concept based on comparative cytology. — InIrvine, D. E. G., John, D. M., (Eds): Systematics of the green algae, pp. 29–72. — London: Academic Press.

    Google Scholar 

  • McFadden, G. I., Melkonian, M., 1986: Use of Hepes buffer for microalgal culture media and fixation for electron microscopy. — Phycologia25: 551–557.

    Google Scholar 

  • Medlin, L., Elwood, H. J., Stickel, S., Sogin, M., 1988: The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. — Gene71: 491–499.

    PubMed  Google Scholar 

  • Melkonian, M., 1990a: PhylumChlorophyta, classChlorophyceae. — InMargulis, L., Corliss, J. O., Melkonian, M., Chapman, D. J., (Eds): Handbook of Protoctista, pp. 608–616. — Boston: Jones and Bartlett.

    Google Scholar 

  • , 1990b: Chlorophyte orders of uncertain affinities: orderMicrothamniales. — InMargulis, L., Corliss, J. O., Melkonian, M., Chapman, D. J., (Eds): Handbook of Protoctista, pp. 652–654. — Boston: Jones and Bartlett.

    Google Scholar 

  • , 1990c: PhylumChlorophyta, classPrasinophyceae. — InMargulis, L., Corliss, J. O., Melkonian, M., Chapman, D. J., (Eds): Handbook of Protoctista, pp. 600–607. — Boston: Jones and Bartlett.

    Google Scholar 

  • Mix, M., 1972: Die Feinstruktur der Zellwände beiMesotaeniaceae undGonatozygaceae mit einer vergleichenden Betrachtung der verschiedenen Wandtypen derConjugatophyceae und über deren systematischen Wert. — Arch. Mikrobiol.81: 197–220.

    Google Scholar 

  • , 1973: Liste der Sammlung von Conjugaten-Kulturen im Institut für Allgemeine Botanik der Universität Hamburg. — Mitt. Staatsinst. Allg. Bot. Hamburg14: 135–169.

    Google Scholar 

  • , 1980: Zur Feinstruktur der Zellwände beiGenicularia spirotaenia (De bary)De bary. — Mitt. Inst. Allg. Bot. Hamburg17: 27–38.

    Google Scholar 

  • Pickett-Heaps, J., 1975: Green algae. Structure, reproduction and evolution in selected genera. — Sunderland, MA: Sinauer.

    Google Scholar 

  • Ruzicka, J., 1970: Zur Taxonomie und Variabilität der FamilieGonatozygaceae 1–2. — Preslia42: 1–15.

    Google Scholar 

  • Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., Erlich, H. A., 1988: Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. — Science239: 487–491.

    PubMed  Google Scholar 

  • Saitou, N., Nei, M., 1987: The neighbor-joining method: a new method for reconstructing phylogenetic trees. — Mol. Biol. Evol.4: 406–425.

    PubMed  Google Scholar 

  • Sanger, F., Nicklen, S., Coulson, A. R., 1977: DNA sequencing with chain-terminating inhibitors. — Proc. Natl. Acad. Sci. USA74: 5463–5467.

    PubMed  Google Scholar 

  • Stabenau, H., 1976: Microbodies fromSpirogyra. — Pl. Physiol.58: 693–695.

    Google Scholar 

  • , 1982: A peroxisomal glycolate oxidase in the algaMougeotia. — Planta154: 165–167.

    Google Scholar 

  • Surek, B., 1983: Mucilage regeneration in the green algaCosmocladium saxonicum De Bary (Desmidiaceae): a light microscopic and quantitative study. — Brit. Phycol. J.18: 73–81.

    Google Scholar 

  • Swofford, D. L., 1990: PAUP: Phylogenetic Analysis Using Parsimony, version 3.0. — Champaign, IL: Illinois Natl. Hist. Surv.

    Google Scholar 

  • Van den Hoek, C., Stam, W. T., Olsen, J. L., 1988: The emergence of a new chlorophytan system, and Dr.Kornmann's contribution thereto. — Helgol. Meeresunters.42: 339–383.

    Google Scholar 

  • West, W., West, G. S., 1904: The BritishDesmidiaceae. 1. — London: Ray Society.

    Google Scholar 

  • West, G. S., Fritsch, F. E., 1927: A treatise on the British freshwater algae. — Cambridge: University Press.

    Google Scholar 

  • Wilcox, L. W., Fuerst, P. A., Floyd, G. L., 1993: Phylogenetic relationships of four charophycean green algae inferred from complete nuclear-encoded small subunit rRNA gene sequences. — Amer. J. Bot.80: 1028–1033.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

In memoriamRobert W. Hoshaw.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Surek, B., Beemelmanns, U., Melkonian, M. et al. Ribosomal RNA sequence comparisons demonstrate an evolutionary relationship betweenZygnematales and charophytes. Pl Syst Evol 191, 171–181 (1994). https://doi.org/10.1007/BF00984663

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00984663

Key words

Navigation