Biochemistry of the extracellular matrix of Volvox

International Review of Cytology

Volumn 180, Issue , 1998, Pages 51-85

  Sumper, Manfred ^a   Hallmann, Armin ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Cell wall; Extracellular matrix; Glycoproteins; Green algae; Plant development; Volvocales; Volvox

Indexed keywords

GLYCOPROTEIN; HYDROXYPROLINE; PHEROMONE;

ALGA; BIOCHEMISTRY; CHLAMYDOMONAS; DEVELOPMENT; EXTRACELLULAR MATRIX; FLAGELLUM; METAZOON; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS;

EID: 0031889952     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0074-7696(08)61770-2     Document Type: Review

References (125)

1. Adair, W. S., and 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.
2. Adair, W. S., and Apt, K. E. (1990). Cell wall regeneration in Chlamydomonas: Accumulation of mRNAs encoding cell wall hydroxyproline-rich glycoproteins. Proc. Nail. Acad. Sei. USA 87, 7355-7359.
3. Adair, W. S., and Snell, W. J. (1990). The Chlamydomonas reinhardtii cell wall: Structure, biochemistry, and molecular biology. In "Organization and Assembly of Plant and Animal Extracellular Matrix" (W. S. Adair and R. P. Mecham, eds.), pp. 15-84. Academic Press, San Diego.
4. Adair, W. S., Steinmetz, S. A., Mattson, D. M., Goodenough, U. W., and Heuser, J. E. (1987). Nucleated assembly of Chlamydomonas and Volvox cell walls. J. Cell Biol. 105,2373-2382.
5. Albersheim, P., An, J., Freshour, G., Fuller, M. S., Guillen, R., Harn, K.-S., Hahn, M. G., Huang, J., O'Neill, M., Whitcombe, A., Williams, M. V., York, W. S., and Darvill, A. (1994). Structure and function studies of plant cell wall polysaccharides. Biochem. Soc. Trans. 22, 374-378.
6. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
7. Amon, P., Haas, E., and Sumper, M. (1997). The sexual pheromone and wounding triggers the same set of genes in the multicellular green alga Volvox. Submitted for publicatio n. Beliveau, C., Potvin, C., Trudel, J., Asselin, A., and Bellemare, G. (1991). Cloning, sequencing, and expression in Escherichia coli of a Streptococcus faecalis autolysin. J. Bacterial. 173, 5619-5623.
8. Boiler, T. (1988). Ethylene and the regulation of antifungal hydrolases in plants. In "Surveys of Plant Molecular and Cell Biology" (B. J. Miflin, ed.), Vol. 5, pp. 145-174. Oxford Univ. Press, London.
9. Bowles, D. (1990). Defense-related proteins in higher plants. Anna. Rev. Biochem. 59,873-907.
10. Broekaert, I., Lee, H. I., Rush, A., Chua, N. H., and Raikhel, N. (1990). Wound-induced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis). Proc. Natl. Acad. Sei. USA 87, 7633-7637.
11. Brownlee, C., and Berger, F. (1995). Extracellular matrix and pattern in plant embryos: On the lookout for developmental information. Trends Genet. 11, 344-348.
12. Catt, J. W., Hills, G. J., and Roberts, K. (1976). A structural glycoprotein, containing hydroxyproline, isolated from the cell wall of Chlamydomonas reinhardii. Planta 131, 165-171.
13. Catt, J. W., Hills, G. J., and Roberts, K. (1978). Cell wall glycoproteins from Chlamydomonas reinhardii, and their self-assembly. Planta 138, 91-98.
14. Chu, C. P., Kariyama, R., Daneo-Moore, L., and Shockman, G. D. (1992). Cloning and sequence analysis of the muramidase-2 gene from Enterococcus hirae. J. Bacteriol. 174,1619-1625.
15. Claes, H. (1971). Autolyse der Zellwand bei den Garnelen von Chlamydomonas reinhardii. Arch Mikrobiol. 108, 221-229.
16. Cooper, J. B., Chen, J. A., and Varner, J. E. (1984). The glycoprotein component of plant cell walls. In "Structure, Function, and Biosynthesis of Plant Cell Walls" (W. M. Dugger and S. Bartnicki-Garcia, eds.), pp. 75-88. Waverly Press, Baltimore.
17. Dauwalder, M., Whaley, W. G., and Starr, R. C. (1980). Differentiation and secretion in Volvox. J. Ullrasmict. Res. 70, 318-335.
18. Davies, J. P., and Grossman, A. R. (1994). Sequences controlling transcription of the Chlamydomonas reinhardtii 2-tubulin gene after deflagellation and during the cell cycle. Mol. Cell. Biol. 14, 5165-5174.
19. Davies, J. P., Weeks, D. P., and Grossman, A. R. (1992). Expression of the arylsulfatase gene from the β2-tubulin promoter in Chlamydomonas reinhardtii. Nucleic Acids Res. 20, 2959-2965.
20. Debuchy, R., Purton, S., and Rochaix, J. D. (1989). The argininosuccinate lyase gene of Chlamydomonas reinhardtii: An important tool for nuclear transformation and for correlat-ing the genetic and molecular maps of the ARG7 locus. EMBO J. 8, 2803-2809.
21. Desnitski, A. G. (1995). A review on the evolution of development in Volvox: Morphological and physiological aspects. Eur. J. Protist. 31, 241-247.
22. Poolittle, R. F. (1995). The multiplicity of domains in proteins. Annu. Rev. Biochem. 64, 287-314.
23. Elkins, T., Hortsch, M., Bieber, A. J., Snow, P. M., and Goodman, C. S. (1990). Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting. J. Cell Biot. 110, 1825-1832.
24. Englund, P. T. (1993). The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annu. Rev. Biochem. 62,121-138.
25. Ertl, H., Mengele, R., Wenzl, S., Engel, J., and Sumper, M. (1989). The extracellular matrix of Volvox carterl: Molecular structure of the cellular compartment. J. Cell Biol. 109,3493-3501.
26. Ertl, H., Hallmann, A., Wenzl, S., and Sumper, M. (1992). A novel extensin that may organize extracellular matrix biogenesis in Volvox carteri. EMBO J. 11, 2055-2062.
27. Fry, S. C. (1982). Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein. Biochem. J. 204, 449-455.
28. Fry, S. C, Aldington, S., Hetherington, P. R., and Aitken, J. (1993). Oligosaccharides as signals and substrates in the plant cell wall. Plant Physiol. 103, 1-5.
29. Fuchs, R., and Gassen, H. G. (1989). Nucleotide sequence of human preprocathepsin H, a lysosomal cysteine proteinase. Nucleic Acids Res. 17, 9471.
30. Garvey, K., Saedi, M. S., and Ito, J. (1986). Nucleotide sequence of Bacillus phage phi 29 genes 14 and 15: Homology of gene 15 with other phage lysozymes. Nucleic Acids Res. 14, 10001-10008.
31. Gibeaut, D. M., and Carpita, N. C. (1994). Biosynthesis of plant cell wall polysaccharides. FASEB J. 8, 904-915.
32. Gilles, R., Gilles, C., and Jaenicke, L. (1983). Sexual differentiation of the green alga Volvox carteri: Involvement of extracellular phosphorylated proteins. Natunvissenschaften 70, 571-572.
33. Gilles, R., Gilles, C., and Jaenicke, L. (1984). Pheromone-binding and matrix-mediated events in sexual induction of Volvox carteri. Z. Naturforsch. 39c, 584-592.
34. Godl, K., Hallmann, A., Rappel, A., and Sumper, M. (1995). Pherophorins: A family of extracellular matrix glycoproteins from Volvox structurally related to the sex-inducing pheromone. Planta 196, 781-787.
35. Godl, K., Hallmann, A., Wenzl, S., and Sumper, M. (1997). Differential targeting of closely related ECM glycoproteins: The pherophorin family from Volvox. EMBO J. 16, 25-34.
36. Goodenough, U. W. (1985). An essay on the origins and evolution of eukaryotic sex. In "The Origin and Evolution of Sex" (H. O. Halvorson and S. Segal, eds.), pp. 123-140. A. R. Liss, New York.
37. Goodenough, U. W., and Heuser, J. E. (1985). The Chlamydomonas cell wall and its constituent glycoproteins analyzed by the quick-freeze, deep-etch technique. J. Cell Biol. 101,1550-1568.
38. Goodenough, U. W., and Heuser, J. E. (1988). Molecular organization of cell-wall crystals from Chlamydomonas reinhardtii and Volvox carteri. J. Cell Sci. 90, 717-734.
39. Goodenough, U. W., Gebhart, B., Mecham, R. P., and Heuser, J. E. (1986). Crystals of the Chlamydomonas reinhardtii cell wall: Polymerization, depolymerization, and purification of glycoprotein monomers. J. Cell Biol. 103, 405-417.
40. Görlach, C. (1994). "Biochemische Charakterisierung einer Sexualpheromon-kontrollierten Komponente der Extrazellulären Matrix von Volvox carteri f. nagariensis." Ph.D. thesis, Univ. Regensburg, Regensburg, Germany.
41. Green, K. J., and Kirk, D. L. (1981). Cleavage patterns, cell lineages, and development of a cytoplasmic bridge system in Volvox embryos. J. Cell Biol. 91, 743-755.
42. Gumpel, N. J., Rochaix, J. D., and Purton, S. (1994). Studies on homologous recombination in the green alga Chlamydomonas reinhardtii. Curr. Genet. 26,438-442.
43. Hallmann, A., and Sumper, M. (1994a). An inducible arylsulfatase of Volvox carteri with properties suitable for a reporter-gene system. Purification, characterization and molecular cloning. Eitr. J. Biochem. 221, 143-150.
44. Hallmann, A., and Sumper, M. (1994b). Reporter genes and highly regulated promoters as tools for transformation experiments in Volvox carteri. Proc. Natl. Acad. Sci. USA 91,11562-11566.
45. + symporter is a useful selectable marker and biochemical reagent when expressed in Volvox. Proc. Natl. Acad. Sci. USA 93, 669-673.
46. Hallmann, A., Rappel, A., and Sumper, M. (1997). Gene replacement by homologous recombination in the multicellular green alga Volvox carteri. Proc. Natl. Acad. Sci. USA 94,7469-7474.
47. Hills, G. J., Philipps, J. M., Gay, M. R., and Roberts, K. (1975). Self-assembly of a plant cell wall in vitro. J. Mol. Biol. 96, 431-441.
48. Holm, L., and Sander, C. (1994). Structural similarity of plant chitinase and lysozymes from animals and phage. An evolutionary connection. FEES Lett. 340, 129-132.
49. Holst, O., Christoffel, V., Fründ, R., Moll, H., and 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.
50. Huber, O., and Sumper, M. (1994). Algal-CAMs: Isoforms of a cell adhesion molecule in embryos of the alga Volvox with homology to Drosophila fasciclin I. EMBOJ. 13,4212-4222.
51. Huskey, R. J. (1979). Mutants affecting vegetative cell orientation in Volvox carteri. Dev. Biol. 72, 236-243.
52. Jaenicke, L., and Waffenschmidt, S. (1979). Matrix-lysis and release of daughter spheroids in Volvox carteri-A. proteolytic process. FEBS Lett. 107, 250-253.
53. Jaenicke, L., and Waffenschmidt, S. (1981). Liberation of reproductive units in Volvox and Chlamydomonas: Proteolytic processes. Der. Dtsch. Bot. Ces. 94, 375-386.
54. Jaenicke, L., Kuhne, W., Spessert, R., Wahle, U., and Waffenschmidt, S. (1987). Cell-wall lytic enzymes (autolysins) of Chlamydomonas reinhardtii are (hydroxy)proline-specific proteases. Eur. J. Biochem. 170, 485-491.
55. Joris, B., Englebert, S., Chu, C. P., Kariyama, R., Daneo-Moore, L., Shockman, G. D., and Ghuysen, J. M. (1992). Modular design of the Enterococcus hirae muramidase-2 and Streptococcus faecalis autolysin. FEMS Microbiol. Lett. 70, 257-264.
56. Joseleau, J.-P., Chambat, G., Cortelazzo, A., Faik, A., and Ruel, K. (1994). Putative biological action of oligosaccharides on enzymes involved in cell-wall development. Biochem. Soc. Trans. 22, 403-407.
57. Kieliszewski, M. J., and Lamport, D. T. A. (1994). Extensin: Repetitive motifs, functional sites, posttranslational codes, and phylogeny. Plant J. 5, 157-172.
58. Kindle, K. L. (1990). High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87, 1228-1232.
59. Kindle, K. .L., Schnell, R. A., Fernandez, E., and Lefebvre, P. A. (1989). Stable nuclear transformation of Chlamydomonas using the Chlamydomonas gene for nitrate reductase. J. Cell Biol. 109, 2589-2601.
60. Kinoshita, T., Kukuzawa, H., Shimada, T., Saito, T., and Matsuda, Y. (1992). Primary structure and expression of a gamete lytic enzyme in Chlamydomonas reinhardtii: Similarity of functional domains to matrix metalloproteases. Proc. Natl. Acad. Sci. USA 89, 4693-4697.
61. Kirk, D. L. (1988). The ontogeny and phylogeny of cellular differentiation in Volvox. Trends Genet. 4, 32-36.
62. Kirk, D. L., and Harper, J. F. (1986). Genetic, biochemical and molecular approaches to Volvox development and evolution. Int. Rev. Cytol. 99, 217-293.
63. Kirk, D. L., and Kirk, M. M. (1986). Heat shock elicits production of sexual inducer in Volvox. Science 231, 51-54.
64. Kirk, D. L., Birchem, R., and King, N. (1986). The extracellular matrix of Volvox: A comparative study and proposed system of nomenclature. J. Cell Sci. 80, 207-231.
65. Knox, P. (1995). Developmentally regulated proteoglycans and glycoproteins of the plant cell surface. FASEB J. 9, 1004-1012.
66. Kroger, N., Bergsdorf, C, and Sumper, M. (1994). A new calcium binding glycoprotein family constitutes a major diatom cell wall component. EMBO J. 13, 4676-4683.
67. Kroger, N., Bergsdorf, C, and Sumper, M. (1996). Frustulins: Domain conservation in a protein family associated with diatom cell walls. Eur. J. Biocliem. 239, 259-264.
68. Lane, B. G. (1994). Oxalate, germine, and the extracellular matrix of higher plants. FASEB J. 8, 294-301.
69. Larson, A., Kirk, M. M., and Kirk, D. L. (1992). Molecular phylogeny of the volvocine flagellates. Mol. Biol. Evol. 9, 85-105.
70. Levy, S., and Staehelin, L. A. (1992). Synthesis, assembly and function of plant cell wall macromolecules. Curr. Opin. Cell Biol. 4, 856-862.
71. Linthorst, H. J. M. (1991). Pathogenesis-related proteins of plants. Crit. Rev. Plant Sci. 10, 123-150.
72. Linthorst, H. J. M., Van Loon, L. C, Van Rossum, C. M. A., Mayer, A., Bol, J. F., Van Roekel, J. S. C, Meulenhoff, E. J. S., and Cornelissen, B. J. C. (1990). Analysis of acidic and basic chitinases from tobacco and petunia and their constitutive expression in transgenic tobacco. Mol.-Plant Microb. Interact. 3, 252-258.
73. Mages, H.-W., Tschochner, H., and Sumper, M. (1988). The sexual inducer of Volvox carteri. Primary structure deduced from cDNA sequence. FEBS Lett. 234, 407-410.
74. Matsuda, Y., Yamasaki, A., Saito, T., and Yamaguchi, T. (1984). Purification and characterization of cell wall lytic enzyme released by mating gametes of Chlamydomonas reinliardtii. FEBS Lett. 166, 293-297.
75. Matsuda, Y., Saito, T., Yamaguchi, T., and Kawase, H. (1985). Cell wall lytic enzyme released by mating gametes of Chlamydomonas reinliardtii is a metalloprotease and digests the sodium perchlorate-insoluble component of cell wall. J. Biol. Client. 260, 6373-6377.
76. Matsuda, Y., Saito, T., Yamaguchi, T., Koseki, M., and Hayashi, K. (1987). Topography of cell wall lytic enzyme in Chlamydomonas reinliardtii: Form and location of the stored enzyme in vegetative cell and gamete. J. Cell Biol. 104, 321-329.
77. Matsuda, Y., Koseki, M., Shimada, T., and Saito, T. (1995). Purification and characterization of a vegetative lytic enzyme responsible for liberation of daughter cells during the proliferation of Chlamydomonas reinliardtii. Plant Cell Physiol. 36, 681-689.
78. Mengele, R. (1988). "Versuche zur strukturellen Charakterisierung eines Olykoproteins aus der Extrazellulären Matrix von Volvox carteri." Ph.D. thesis, Univ. Regensburg, Regensburg, Germany.
79. Miller, D. H., Mellman, I. S., Lamport, D. T. A., and Miller, M. (1974). The chemical composition of the cell wall of Chlamydomonas gymnogama and the concept of a plant cell wall protein. J. Cell Biol. 63, 420-429.
80. Mitchell, B. A. (1980). "Evidence for Polyhydroxyproline in the Extracellular Matrix of Volvox." M.S. thesis, Michigan State University, East Lansing, MI.
81. Mort, A. J., and Lamport, D. T. A. (1977). Anhydrous hydrogen fluoride deglycosylates glycoproteins. Anal. Biochem. 82, 289-309.
82. Nelson, J. A., and Lefebvre, P. A. (1995). Targeted disruption of the NIT8 gene in Chlamydomonas reinliardtii. Mol. Cell. Biol. 15, 5762-5769.
83. Nozaki, H. (1996). Morphology and evolution of sexual reproduction in the Volvocaceae (Chlorophyta). J. Plant Res. 109, 353-361.
84. Paces, V., Vlcek, C., and Urbanek, P. (1986). Nucleotide sequence of the late region of Bacillus subtilis phage PZA, a close relative of phi 29. Gene 44, 107-114.
85. Pommerville, J., and Kochert, G. (1982). Effects of senescence on somatic cell physiology in the green alga Volvox carteri. Exp. Cell Res. 140, 39-45.
86. Quinn, J. M., and Merchant, S. (1995). Two copper-responsive elements associated with the Chlamydomonas Cyc6 gene function as targets for transcriptional activators. Plant Cell 7, 623-628.
87. Raikhel, N. V., Lee, H. I., and Broekaert, W. F. (1993). Structure and function of chitinbinding proteins. Anna. Rev. Plant Physiol. Plant Mol. Biol. 44, 591-615.
88. Rausch, H., Larsen, N., and Schmitt. R. (1989). Phylogenetic relationships of the green alga Volvox carteri deduced from small-subunit ribosomal RNA comparisons. J. Mol. Evol. 29, 255-265.
89. Roberts, K. (1974). Crystalline glycoprotein cell walls of algae: Their structure, composition and assembly. Philos. Trans. R. Soc. London, Ser. B 268, 129-146.
90. Roberts, K. (1979). Hydroxyproline: Its asymmetric distribution in a cell wall glycoprotein. Planta 146, 275-279.
91. Roberts, K. (1994). The plant extracellular matrix: In a new expansive mood. Curr, Opin. Cell Biol. 6, 688-694.
92. Roberts, K., Gay, M. R., and Hills, G. J. (1980). Cell wall glycoproteins from Chlamydomonas are sulphated. Physiol. Plant. 49, 421-424.
93. Roberts, K., Hills, G. J., and Shaw, P. J. (1982). The structure of algal cell walls, hi "Electron Microscopy of Proteins" (J. R. Harris, ed.), Vol. 3, pp. 1-40. Academic Press, New York.
94. Roberts, K., Grief, C, Hills, G. J., and Shaw, P. J. (1985). Cell wall glycoproteins: Structure and function. J. Cell Sci. Suppl. 2, 105-127.
95. Schiedlmeier, B., Schmitt, R., Müller, W., Kirk, M. M., Gruber, H., Mages, W., and Kirk, D. L. (1994). Nuclear transformation of Volvox carteri. Proc. Natl. Acad. Sci. USA 91,5080-5084.
96. Schlipfenbacher, R., Wenzl, S., Lottspeich, F., and Sumper, M. (1986). An extremely hydroxyproline-rich glycoprotein is expressed in inverting Volvox embryos. FEBS Lett. 209,57-62.
97. Schlösser, U. G. (1976). Entwicklungsstadien- und sippenspezifische Zellwandautolysine bei der Freisetzung von Fortpflanzungszellen in der Gattung Chlamydomonas. Ber. Dtsch. Bot. Ges. 89, 1-56.
98. Schlösser, U. G. (1981). Algal wall-degrading enzymes-Autolysins. In "Encyclopedia of Plant Physiology New Series" (W. Tanner and F. A. Loewus, eds.), pp. 333-351. Springer-Verlag, Berlin.
99. Schlösser, U. G. (1984). Species-specific sporangium autolysins (cell-wall dissolving enzymes) in the genus Chlamydomonas. In "The Systematics of Green Algae" (D. E. G. Irvine and D. Johns, eds.), pp. 409-418. Academic Press, London.
100. Schmidt, B., Seimer, T., Ingendoh, A., and von Figura, K. (1995). A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell 82, 271-278.
101. Schmitt, R., Fabry, S., and Kirk, D. L. (1992). In search of molecular origins of cellular differentiation in Volvox and its relatives. Int. Rev. Cytol. 139, 189-265.
102. Seimer, T., Hallmann, A., Schmidt, B., Sumper, M., and von Figura, K. (1996). The evolutionary conservation of a novel protein modification, the conversion of cysteine to serinesemialdehyde in arylsulfatase from Volvox carteri. Eur. J. Biochem. 238, 341-345.
103. Showalter, A. M. (1993). Structure and function of plant cell wall proteins. Plant Cell 5,9-23.
104. Showalter, A. M., and Varner, J. E. (1989). Plant hydroxyproline-rich glycoproteins. In "The Biochemistry of Plants" (P. K. Stumpf and E. E. Conn, eds.), Vol. 15, pp. 485-520. Academic Press, New York.
105. Sidhu, S. S., Kalmar, G. B., Willis, L. G., and Borgford, T. J. (1994). Streptomyces griseus protease C. A novel enzyme of the chymotrypsin superfamily. J. Biol. Chem. 269, 20167-20171.
106. Snell, W. J. (1983). Characterization of the fiagellar collar. Cell Motil. 3, 273-280.
107. Sodeinde, O. A., and Kindle, K. L. (1993). Homologous recombination in the nuclear genome of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 90, 9199-9203.
108. Speir, T. W., and Ross, D. J. (1978). Soil phosphatase and sulfatase. In "Soil enzymes" (R. G. Burns, ed.), pp. 197-250. Academic Press, London.
109. Spessert, R., and Waffenschmidt, S. (1990). Studies on the vegetative autolysin during the vegetative life cycle in Chlamydomonas. EUT. J. Cell Biol. 51, IT-22.
110. Stanford, A., Bevan, M., and Northcote, D. (1989). Differential expression within a family of novel wound-induced genes in potato. Mol. Gen. Genet. 215, 200-208.
111. Starr, R. C. (1969). Structure, reproduction, and differentiation in Volvox carter! f. nagariensis lyengar, strains HK9 & 10. Arch. Protistenk. Ill, 204-222.
112. Starr, R. C. (1970). Control of differentiation in Volvox. Dev. Biol. Suppl. 4, 59-100.
113. Stevens, D. R., Rochaix, J. D., and Purton, S. (1996). The bacterial phleomycin resistance gene ble as a dominant selectable marker in Chlamydomonas. Mol. Gen. Genet. 251,23-30.
114. Sumper, M. (1979). Control of differentiation in Volvox carteri: A model explaining pattern formation during embryogenesis. FEES Lett. 107, 241-246.
115. -16 M. EMBO J. 12, 831-836.
116. Tschochner, H., Lottspeich, F., and Sumper, M. (1987). The sexual inducer of Volvox carteri: Purification, chemical characterization and identification of its gene. EMBO J. 6,2203-2207.
117. Varner, J. E., and Lin, L. (1989). Plant cell wall architecture. Cell 56, 231-239.
118. Varner, J. E., and Ye, Z. (1994). Tissue printing. FASEB J. 8, 378-384.
119. Waffenschmidt, S., Knittler, M., and Jaenicke, L. (1990). Characterization of a sperm lysin of Volvox carteri. Sex. Plant Reprod. 3,1-6.
120. Waffenschmidt, S., Woessner, J. P., Beer, K., and Goodenough, U. W. (1993). Isodityrosine crosslinking mediates insolubilization of cell walls in Chlamydomonas. Plant Cell 5,809-820.
121. Wenzl, S., and Sumper, M. (1982). The occurrence of different sulphated cell surface glycoproteins correlates with defined developmental events in Volvox. FEBS Lett. 143, 311-315.
122. Wenzl, S., and Sumper, M. (1986). Early event of sexual induction in Volvox: Chemical modification of the extracellular matrix. Dev. Biol. 115, 119-128.
123. Wenzl, S., Thym, D., and Sumper, M. (1984). Development-dependent modification of the extracellular matrix by a sulphated glycoprotein in Volvox carteri. EMBO J. 3, 739-744.
124. Woessner, J. P., Molendijk, A. J., van Egmond, P., Klis, F. M., Goodenough, U. W., and Haring, M. A. (1994). Domain conservation in several volvocacean cell wall proteins. Plant Mol. Biol. 26, 947-960.
125. Zinn, K., McAllister, L., and Goodman, C. S. (1988). Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell 53, 577-587.