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The Protistan Cell Surface pp 245–258Cite as

Volvocine cell walls and their constituent glycoproteins: an evolutionary perspective

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Summary

Similarities in the composition of the extracellular matrix suggest that only some species of the unicellular Chlamydomonas are closely related to the colonial and multicellular flagellated members of the family Volvocaceae. The cell walls from all of the algae in this volvocine group contain a crystalline layer. This lattice structure can be used as a phylogenetic marker to divide Chlamydomonas species into distinct classes, only one of which includes the volvocacean algae. Similarly, not all species of Chlamydomonas are sensitive to each other’s cell wall lytic enzymes, implying divergence of the enzyme’s inner wall substrate. Interspecific reconstitution of the crystalline layer is possible between C. reinhardtii and the multicellular Volvox carteri, but not between C. reinhardtii and C. eugametos. The hydroxyproline-rich glycoproteins (HRGPs) which make up the crystalline layer in genera which have a similar crystal structure exhibit many homologies. Interestingly, the evolutionarily distant cell walls of C. reinhardtii and C. eugametos also contain some HRGPs displaying a few morphological and amino acid sequence homologies. The morphological similarities between the flagellar agglutinins (HRGPs responsible for sexual recognition and adhesion during the mating reaction) and the cell wall HRGPs leads to the proposal of a superfamily from which novel HRGPs (designed for self-assembly/recognition) can constantly evolve. Just as variations in the wall HRGPs can lead to unique wall structures, new agglutinins facilitate sexual isolation of new species. Thus, the HRGPs could emerge as valuable phylogenetic markers.

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Abbreviations

GLE:

gametic lytic enzyme

GP:

glycoprotein

HRGP:

hydroxyproline-rich glycoprotein

SDS PAGE:

sodium dodecyl sulfate polyacrylamide gel electrophoresis

VLE:

vegetative lytic enzyme

VSP:

vegetative serine/proline-rich

WP:

wall protein

ZSP:

zygotic serine/proline-rich

References

  • Adair WS (1985) Characterization of Chlamydomonas sexual agglutinins. J Cell Sci [Suppl] 2: 233–260

    CAS  Google Scholar 

  • Adair WS, Appel H (1989) Identification of a highly conserved hydroxyproline-rich glycoprotein in the cell walls of Chlamydomonas reinhardtii and two other Volvocales. Planta 179: 381–386

    Article  CAS  Google Scholar 

  • Adair WS, Apt KE (1990) Cell wall regeneration in Chlamydomonas: accumulation of mRNAs encoding cell wall HRGPs. Proc Natl Acad Sci USA 87: 7355–7359

    Article  PubMed  CAS  Google Scholar 

  • Adair WS, Snell WJ (1990) The Chlamydomonas reinhardtii cell wall: structure, biochemistry, and molecular biology. In: Adair WS, Mecham RP (eds) Organization and assembly of plant and animal extracellular matrix. Academic Press, San Diego, pp 15–84

    Google Scholar 

  • Adair WS, Steinmetz SA, Mattson DM, Goodenough UW, Heuser JE (1987) Nucleated assembly of Chlamydomonas and Volvox cell walls. J Cell Biol 105: 2373–2382

    Article  PubMed  CAS  Google Scholar 

  • Buchheim MA, Chapman RL (1991) Phylogeny of the colonial green flagellates: a study of 18 S and 26 S rRNA sequence data. BioSystems 25: 85–100

    Article  PubMed  CAS  Google Scholar 

  • Buchheim MA, Turmel M, Zimmer EA, Chapman RL (1990) Phylogeny of Chlamydomonas (Chlorophyta) based on cladistic analysis of nuclear 18 S rRNA sequence data. J Phycol 26: 689–699

    Article  Google Scholar 

  • Cavalier-Smith T (1976) Electron microscopy of zygospore formation in Chlamydomonas reinhardtii. Protoplasma 87: 297–315

    Article  PubMed  CAS  Google Scholar 

  • Claes H (1971) Autolyse der Zellwand bei den Gameten von Chlamydomonas reinhardtii Arch Mikrobiol 78: 180–188

    CAS  Google Scholar 

  • Cooper JB, Adair WS, Mecham RP, Heuser JE, Goodenough UW (1983) Chlamydomonas agglutinin is a hydroxyproline-rich glycoprotein. Proc Natl Acad Sci USA 80: 5898–5901

    Article  PubMed  CAS  Google Scholar 

  • Epstein L, Lamport DTA (1984) An intramolecular linkage involving isodityrosine in extensin. Phytochemistry 23: 1241–1246

    Article  CAS  Google Scholar 

  • Ertl H, Mengele R, Wenzl S, Engel J, Sumper M (1989) The extracellular matrix of Volvox carteri: molecular structure of cellular compartment. J Cell Biol 109: 3493–3501

    Article  PubMed  CAS  Google Scholar 

  • Ertl H, Hallmann A, Wenzl S, Sumper M (1992) A novel extensin that may organize extracellular matrix biogenesis in Volvox carteri. EMBO J 11: 2055–2062

    PubMed  CAS  Google Scholar 

  • Ettl H (1976) Die Gattung Chlamydomonas Ehrenberg. Nova Hedwigia 49: 1–1122

    Google Scholar 

  • Ferris PJ, Goodenough UW (1987) Transcription of novel genes, including a gene linked to the mating-type locus, induced by Chlamydomonas fertilization. Mol Cell Biol 7: 2360–2366

    PubMed  CAS  Google Scholar 

  • Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol 37: 165–186

    Article  CAS  Google Scholar 

  • Goodenough UW (1985) An essay on the origins and evolution of eukaryotic sex. In: Halvorson HO, Monroy A (eds) The origin and evolution of sex. AR Liss, New York, pp 123–140

    Google Scholar 

  • Goodenough UW, (1991) Chlamydomonas mating interactions. In: Dworkin M (ed) Microbial cell-cell interactions. American Society for Microbiology, Washington, DC, pp 71–112

    Google Scholar 

  • Goodenough UW, Heuser JE (1985) The Chlamydomonas cell wall and its constituent glycoproteins analyzed by the quick-freeze deep-etch technique. J Cell Biol 101: 1550–1568

    Article  PubMed  CAS  Google Scholar 

  • Goodenough UW, (1988 a) Molecular organization of cell-wall crystals from Chlamydomonas reinhardtii and Volvox carteri. J Cell Sci 90: 717–733

    CAS  Google Scholar 

  • Goodenough UW (1988 b) Molecular organization of the cell wall and cell-wall crystals from Chlamydomonas eugametos. J Cell Sci 90: 735–750

    CAS  Google Scholar 

  • Goodenough UW, Gebhart B, Mecham RP, Heuser JE (1986 a) Crystals of the Chlamydomonas reinhardtii cell wall: polymerization, depolymerization, and purification of glycoprotein monomers. J Cell Biol 103: 403–417

    Article  Google Scholar 

  • Goodenough UW, Adair WS, Collin-Osdoby P, Heuser JE ( 1986 b) Chlamydomonas cells in contact. In: Gall E, Edelman GM (eds) Cells in contact. Wiley, New York, pp 111–135

    Google Scholar 

  • Grief C, O’Neill MA, Shaw PJ (1987) The zygote cell wall of Chlamydomonas reinhardtii: a structural, chemical, and immunological approach. Planta 170: 433–445

    Article  CAS  Google Scholar 

  • Harris EH (1989) The Chlamydomonas sourcebook. Academic Press, San Diego

    Google Scholar 

  • Hills GJ (1973) Cell wall assembly in vitro from Chlamydomonas reinhardtii. Planta 115: 17–23

    Article  Google Scholar 

  • Hills GJ, Phillips JM, Gay MR, Roberts K (1975) Self-assembly of a plant cell wall in vitro. J Mol Biol 96: 431–444

    Article  PubMed  CAS  Google Scholar 

  • Hoist O, Christoffel V, Frund R, Moll H, Sumper M (1989) A phosphodiester bridge between two arabinose residues as a structural element of an extracellular glycoprotein of Volvox carteri. Eur J Biochem 181: 345–350

    Article  Google Scholar 

  • Imam SH, Snell WJ (1988) The Chlamydomonas cell wall degrading enzyme, lysin, acts on two domains within the framework of the wall. J Cell Biol 106: 2211–2221

    Article  PubMed  CAS  Google Scholar 

  • Kieliszewski M, Lamport DTA (1994) Extensin: repetitive motifs, functional motifs, post-translational codes and phylogeny. Plant J 5: 157–172

    Article  PubMed  CAS  Google Scholar 

  • Kieliszewski M, Leykam JF, Lamport DTA (1990) Structure of the threonine-rich extensin from Zea mays. Plant Physiol 92: 316–326

    Article  PubMed  CAS  Google Scholar 

  • Kieliszewski M, de Zacks R, Leykam JF, Lamport DTA (1992) A repetitive proline-rich protein from the gymnosperm Douglas Fir is a hydroxyproline-rich glycoprotein. Plant Physiol 98: 919–926

    Article  PubMed  CAS  Google Scholar 

  • Kirk DL, Birchem R, King N (1986) The extracellular matrix of Volvox: a comparative study and proposed system of nomenclature. J Cell Sci 80: 207–231

    PubMed  CAS  Google Scholar 

  • Lamport DTA (1977) Structure, biosynthesis, and significance of cell wall glycoproteins. Rec Adv Phytochem 11: 79–115

    CAS  Google Scholar 

  • Larson A, Kirk MM, Kirk DL (1992) Molecular phylogeny of the volvocine flagellates. Mol Biol Evol 9: 85–105

    PubMed  CAS  Google Scholar 

  • Matsuda Y, Musgrave A, van den Ende H, Roberts K (1987) Cell walls of algae in the Volvocales: their sensitivity to a cell wall lytic enzyme and labeling with an anti-cell wall glycopeptide of Chlamydomonas reinhardtii. Bot Mag 100: 373–384

    Article  Google Scholar 

  • Minami S, Goodenough UW (1978) Novel glycopolypeptide synthesis induced by gametic cell fusion in Chlamydomonas reinhardtii J Cell Biol 77: 165–181

    CAS  Google Scholar 

  • Monk BC (1988) The cell wall of Chlamydomonas reinhardtii gametes: composition, structure and autolysin-mediated shedding and dissolution. Planta 176: 441–450

    Article  CAS  Google Scholar 

  • Musgrave A, van Eijk E, te Welscher R, Broekman R, Lens PF, Homan WL, van den Ende H (1991) Sexual agglutination factor from Chlamydomonas eugametos. Planta 153: 362–369

    Article  Google Scholar 

  • Rausch H, Larsen N, Schmitt R (1989) Phylogenetic relationships of the green alga Volvox carteri deduced from small-subunit ribosomal RNA comparisons. J Mol Evol 29: 255–265

    Article  PubMed  CAS  Google Scholar 

  • Raz R, José M, Moya A, Martínez-Izquierdo JA, Puigdoménech P (1992) Different mechanisms generating sequence variability are revealed in distinct regions of the hydroxyproline-rich glycoprotein gene from maize and related species. Mol Gen Genet 233: 252–259

    Article  PubMed  CAS  Google Scholar 

  • Roberts K (1974) Crystalline glycoproteins of algae: their structure, composition, and assembly. Philos Trans R Soc Lond [Biol] 268: 129–146

    Article  CAS  Google Scholar 

  • Roberts K (1981) Visualizing an insoluble glycoprotein. Micron 12: 185–186

    Google Scholar 

  • Roberts K, Hills GJ, Shaw P (1982) Structure of algal cell walls. In: Harris JR (eds) Electron microscopy of proteins, vol 3. Academic Press, New York, pp 1–140

    Google Scholar 

  • Roberts K, Grief C, Hills J, Shaw PJ (1985 a) Cell wall glycoproteins: structure and function. J Cell Sci [Suppl] 2: 105–127

    CAS  Google Scholar 

  • Roberts K, Phillips J, Shaw P, Grief C, Smith E ( 1985 b) An immunological approach to the plant cell wall. In: Brett CT, Hillman JR (eds) Biochemistry of plant cell walls. Cambridge University Press, New York, pp 125–154

    Google Scholar 

  • Samson MR, Klis FM, Homan WL, van Egmond P, Musgrave A, van den Ende H (1987) Composition and properties of the sexual agglutinins of the flagellated green algae Chlamydomonas eugametos. Planta 170: 314–321

    Article  CAS  Google Scholar 

  • Schlösser UG (1966) Enzymatisch gesteuerte Freisetzung von Zoosporea bei Chlamydomonas reinhardtii dangeard in Synchronkultur. Arch Mikrobiol 54: 129–159

    Article  Google Scholar 

  • Schlösser UG (1976) Entwicklungsstadien- und sippenspezifische Zellwand-Lysine bei der Freisetzung von Fortpflanzungszellen in der Gattung Chlamydomonas. Ber Deutsch Bot Ges 89: 1–56

    Google Scholar 

  • Schlösser UG (1984) Species-specific sporangium autolysins (cell-wall dissolving enzymes) in the genus Chlamydomonas. In: Irvine DEG, John D (eds) The systematics of green algae. Academic Press, London, pp 409–418

    Google Scholar 

  • Schmitt R, Fabry S, Kirk DL (1992) In search of molecular origins of cellular differentiation in Volvox and its relatives. Int Rev Cytol 139: 189–265

    Article  PubMed  CAS  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5: 9–23

    Article  PubMed  CAS  Google Scholar 

  • Su X, Kaska DD, Gibor A (1990) Induction of cytosine-rich poly (A)+ RNAs in Chlamydomonas reinhardtii by cell wall removal. Exp Cell Res 187: 54–58

    Article  PubMed  CAS  Google Scholar 

  • Van den Ende H, Klis FM, Musgrave A (1988) The role of flagella in sexual reproduction of Chlamydomonas eugametos. Acta Bot Neerl 37: 327–350

    Google Scholar 

  • Varner JE, Lin L-S (1989) Plant cell wall architecture. Cell 56: 231–239

    Article  PubMed  CAS  Google Scholar 

  • Waffenschmidt S, Spessert R, Jaenicke L (1988) Oligosaccharide side chains are essential for cell wall lysis in Chlamydomonas reinhardtii. Pianta 175: 513–519

    CAS  Google Scholar 

  • Waffenschmidt S, Woessner JP, Beer K, Goodenough UW (1993) Isodityrosine cross-linking mediates cell wall insolubilization in Chlamydomonas. Plant Cell 5: 809–820

    Article  PubMed  CAS  Google Scholar 

  • Woessner JP, Goodenough UW (1989) Molecular characterization of a zygote wall protein: an extensin-like molecule in Chlamydomonas reinhardtii. Plant Cell 1: 901–911

    Article  PubMed  CAS  Google Scholar 

  • Woessner JP, Goodenough UW (1992) Zygote and vegetative cell wall proteins in Chlamydomonas reinhardtii share a common epitope, (SerPro)x. Plant Sci 83: 65–76

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Washington University, Box 1229, St. Louis, Missouri, 63130, USA

    J. P. Woessner & Ursula W. Goodenough

Authors
  1. J. P. Woessner
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  2. Ursula W. Goodenough
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Editors and Affiliations

  1. School of Botany, University of Melbourne, Parkville, Victoria, Australia

    Richard Wetherbee  & Jeremy D. Pickett-Heaps  & 

  2. Provasoli-Guillard Center for Culture of Marine Phytoplankton, Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, Maine, USA

    Robert A. Andersen

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© 1994 Springer-Verlag

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Woessner, J.P., Goodenough, U.W. (1994). Volvocine cell walls and their constituent glycoproteins: an evolutionary perspective. In: Wetherbee, R., Pickett-Heaps, J.D., Andersen, R.A. (eds) The Protistan Cell Surface. Springer, Vienna. https://doi.org/10.1007/978-3-7091-9378-5_14

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  • DOI: https://doi.org/10.1007/978-3-7091-9378-5_14

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