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Domain conservation in several volvocalean cell wall proteins

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Abstract

Based on our previous work demonstrating that (SerPro)x epitopes are common to extensin-like cell wall proteins in Chlamydomonas reinhardtii, we looked for similar proteins in the distantly related species C. eugametos. Using a polyclonal antiserum against a (SerPro)10 oligopeptide, we found distinct sets of stage-specific polypeptides immunoprecipitated from in vitro translations of C. eugametos RNA. Screening of a C. eugametos cDNA expression library with the antiserum led to the isolation of a cDNA (WP6) encoding a (SerPro)x-rich multidomain wall protein. Analysis of a similarly selected cDNA (VSP-3) from a C. reinhardtii cDNA expression library revealed that it also coded for a (SerPro)x-rich multidomain wall protein. The C-terminal rod domains of VSP-3 and WP6 are highly homologous, while the N-terminal domains are dissimilar; however, the N-terminal domain of VSP-3 is homologous to the globular domain of a cell wall protein from Volvox carteri. Exon shuffling might be responsible for this example of domain conservation over 350 million years of volvocalean cell wall protein evolution.

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References

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

    PubMed  Google Scholar 

  2. Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ: Basic local alignment search tool. J Mol Biol 215: 403–410 (1990).

    PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  5. Cavalier-Smith, T: Intron phylogeny: a new hypothesis. Trends Genet 7: 145–148 (1991).

    PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  9. Feinberg, AP, Vogelstein, B: A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  11. Fong, C, Kieliszewski, MJ, deZacks, R, Leykam, JF, Lamport, DTA: A gymnosperm extensin contains the serine-tetrahydroxyproline motif. Plant Physiol 99: 548–552 (1992).

    Google Scholar 

  12. Gilbert, W, Marchionni, M, McKnight, G: On the antiquity of introns. Cell 46: 151–154 (1986).

    Article  PubMed  Google Scholar 

  13. Gleeson, PA, Stone, BA, Fincher, GB: Cloning the cDNA for the arabinogalactan-protein from Lolium multiflorum (ryegrass). AGP News 5: 30–36 (1985).

    Google Scholar 

  14. Gleeson, PA, McNamara, M, Wettenhall, EH, Stone, BA, Fincher, GB: Characterization of the hydroxyproline-rich protein core of an arabinogalactan-protein secreted grom suspension-cultured Lolium multiflorum (Italian ryegrass) endosperm cells. Biochem J 264: 857–862 (1989).

    PubMed  Google Scholar 

  15. Goodenough, UW: An essay on the origins and evolution of eukaryotic sex. In: Halvorsen, O, Monroy, A (eds) The Origin and Evolution of Sex, pp. 123–140. Alan R. Liss, New york (1985).

    Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  19. Harris, EH: The Chlamydomonas Sourcebook. Academic Press, San Diego, FL (1989).

    Google Scholar 

  20. Harvey, RJ, Darlison, MG: Random-primed cDNA synthesis facilitates the isolation of multiple 5′-cDNA ends by RACE. Nucl Acids Res 19: 4002 (1991).

    PubMed  Google Scholar 

  21. Hoheisel, J, Pohl, FM: Simplified preparation of unidirectional deletion clones. Nucl Acids Res 14: 3605 (1986).

    PubMed  Google Scholar 

  22. Jacobsen, A: Purification and fractionation of poly(A)+ RNA. Meth Enzymol 152: 254–261 (1987).

    PubMed  Google Scholar 

  23. Jupe, ER, Chapman, RL, Zimmer, EA: Nuclear ribosomal RNA genes and algal phylogeny: the Chlamydomonas example. Biosystems 21: 223–230 (1988).

    Article  PubMed  Google Scholar 

  24. Kieliszewski, MJ, Kamyab, A, Leykam, JF, Lamport, DTA: A histidine-rich extensin from Zea mays is an arabinogalactan protein. Plant Physiol 99: 538–547 (1992).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  26. Kieliszewski, MJ, Showalter, AM, Leykam, JF: Potato lectin: a modular protein sharing sequence similarities with the extensin family, the hevein lectin family, and snake venom disintegrins (platelet aggregation inhibitors). Plant J 5: 849–861 (1994).

    Article  PubMed  Google Scholar 

  27. Kirk, MM, Kirk, DL: Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell 41: 419–428 (1985).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  29. Lefebvre, PA, Silflow, CD, Wieben, EA, Rosenbaum, JL: Increased levels of mRNAs for tubulin and other flagellar proteins after amputation or shortening of Chlamydomonas flagella. Cell 20: 469–477 (1980).

    Article  PubMed  Google Scholar 

  30. Molendijk, AJ, vanEgmond, P, Haring, MA, Klis, FM, van denEnde, H: Characterization of the cell cycle in synchronous cultures of Chlamydomonas eugametos in relation to gametogenesis. J Gen Microbiol 138: 1941–1947 (1992).

    Google Scholar 

  31. Mesland, DAM: Mating in Chlamydomonas eugametos. A scanning electron microscopical study. Arch Microbiol 109: 31–35 (1976).

    PubMed  Google Scholar 

  32. Musgrave, A, deWildt, P, Broekman, R, van denEnde, H: The cell wall of Chlamydomonas eugametos. Immunological aspects. Planta 158: 82–89 (1983).

    Google Scholar 

  33. Musgrave, A, deWildt, P, Crabbendam, K, van denEnde, H: Sexual agglutination in Chlamydomonas eugametos before and after cell fusion. Planta 166: 234–243 (1985).

    Google Scholar 

  34. Patthy, L: Exons-original building blocks of proteins? Bioessays 13: 187–192 (1991).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  36. Raz, R, José, M, Moya, A, Martínez-Izquierdo, JA, Puigdomènech, P: 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 (1992).

    PubMed  Google Scholar 

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

    Google Scholar 

  38. Rogers, JH: The role of introns in evolution. FEBS Lett 268: 339–343 (1990).

    Article  PubMed  Google Scholar 

  39. Sambrook, J, Fritsch, EF, Maniatis, T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  40. Samson, MR, Klis, FM, Homan, WL, vanEgmond, P, Musgrave, A, van denEnde, H: Composition and properties of the sexual agglutinins of the flagellated green alga Chlamydomonas eugametos. Planta 170: 314–321 (1987).

    Google Scholar 

  41. Samson, MR, Klis, FM, van denEnde, H: Cysteine as a fusion inhibitor in the sexual mating reaction of the green alga Chlamydomonas eugametos. Acta Bot Neerl 37: 351–361 (1988).

    Google Scholar 

  42. Sanger, F, Nicklen, S, Coulsen, AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  43. Schloss, JA, Silflow, CD, Rosenbaum, JL: mRNA abundance changes during flagellar regeneration in Chlamydomonas reinhardtii. Mol Cell Biol 4: 424–434 (1984).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  45. Showalter, AM, Rumeau, D: Molecular biology of plant cell wall hydroxyproline-rich glycoproteins. In: Adair, WS, Mecham, RP (eds) Organization and Assembly of Plant and Animal Extracellular Matrix, pp. 247–281. Academic Press, San Diego, FL (1990).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  47. Stafstrom, JP, Staehelin, L: The role of carbohydrate in maintaining extensin in an extended conformation. Plant Physiol 81: 242–246 (1986).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  49. Triemer, RE, Brown, RM: The ultrastructure of fertilization in Chlamydomonas moewusii. Protoplasma 84: 315–325 (1975).

    Google Scholar 

  50. vanHolst, G-J, Varner, JE: Reinforced polyproline II conformation in a hydroxyproline-rich cell wall glycoprotein from carrot root. Plant Physiol 74: 247–251 (1984).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  52. vonHeijne, G: Signal sequences. The limits of variation. J Mol Biol 184: 99–105 (1985).

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  54. Williamson, MP: The structure and function of proline-rich regions in proteins. Biochem J 297: 249–260 (1994).

    PubMed  Google Scholar 

  55. Witman, GB, Carlson, K, Berliner, J, Rosenbaum, JL: Chlamydomonas flagella. I. Isolation and electrophoretic analysis of microtubules, matrix, membranes and mastigonemes. J Cell Biol 54: 507–539 (1972).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  58. Woessner JP, Goodenough UW: Volvocine cell walls and their constituent glycoproteins: an evolutionary perspective. Protoplasma, in press (1994).

  59. Wu, H-M, Zou, J, May, B, Gu, Q, Cheung, AY: A tobacco gene family for flower cell wall proteins with a proline-rich domain and a cysteine-rich domain. Proc Natl Acad Sci USA 90: 6829–6833 (1993).

    PubMed  Google Scholar 

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Woessner, J.P., Molendijk, A.J., van Egmond, P. et al. Domain conservation in several volvocalean cell wall proteins. Plant Mol Biol 26, 947–960 (1994). https://doi.org/10.1007/BF00028861

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