Abstract
The alga Volvox carteri represents one of the simplest multicellular organisms. Its extracellular matrix (ECM) is modified under developmental control, e.g. under the influence of the sex-inducing pheromone that triggers development of males and females at a concentration below 10(-16) M. A novel ECM glycoprotein (pherophorin-S) synthesized in response to this pheromone was identified and characterized. Although being a typical member of the pherophorins, which are identified by a C-terminal domain with sequence homology to the sex-inducing pheromone, pherophorin-S exhibits a completely novel set of properties. In contrast to the other members of the family, which are found as part of the insoluble ECM structures of the cellular zone, pherophorin-S is targeted to the cell-free interior of the spherical organism and remains in a soluble state. A main structural difference is the presence of a polyhydroxyproline spacer in pherophorin-S that is linked to a saccharide containing a phosphodiester bridge between two arabinose residues. Sequence comparisons indicate that the self-assembling proteins that create the main parts of the complex Volvox ECM have evolved from a common ancestral gene.
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Selected References
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- Adams C. R., Stamer K. A., Miller J. K., McNally J. G., Kirk M. M., Kirk D. L. Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet. 1990 Aug;18(2):141–153. doi: 10.1007/BF00312602. [DOI] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Andres D. A., Goldstein J. L., Ho Y. K., Brown M. S. Mutational analysis of alpha-subunit of protein farnesyltransferase. Evidence for a catalytic role. J Biol Chem. 1993 Jan 15;268(2):1383–1390. [PubMed] [Google Scholar]
- Doolittle R. F. The multiplicity of domains in proteins. Annu Rev Biochem. 1995;64:287–314. doi: 10.1146/annurev.bi.64.070195.001443. [DOI] [PubMed] [Google Scholar]
- Ertl H., Hallmann A., Wenzl S., Sumper M. A novel extensin that may organize extracellular matrix biogenesis in Volvox carteri. EMBO J. 1992 Jun;11(6):2055–2062. doi: 10.1002/j.1460-2075.1992.tb05263.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1989 Dec;109(6 Pt 2):3493–3501. doi: 10.1083/jcb.109.6.3493. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
- Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Godl K., Hallmann A., Rappel A., Sumper M. Pherophorins: a family of extracellular matrix glycoproteins from Volvox structurally related to the sex-inducing pheromone. Planta. 1995;196(4):781–787. [PubMed] [Google Scholar]
- Hallmann A., Sumper M. An inducible arylsulfatase of Volvox carteri with properties suitable for a reporter-gene system. Purification, characterization and molecular cloning. Eur J Biochem. 1994 Apr 1;221(1):143–150. doi: 10.1111/j.1432-1033.1994.tb18723.x. [DOI] [PubMed] [Google Scholar]
- Hallmann A., Sumper M. Reporter genes and highly regulated promoters as tools for transformation experiments in Volvox carteri. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11562–11566. doi: 10.1073/pnas.91.24.11562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hallmann A., Sumper M. The Chlorella hexose/H+ symporter is a useful selectable marker and biochemical reagent when expressed in Volvox. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):669–673. doi: 10.1073/pnas.93.2.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harper J. F., Mages W. Organization and structure of Volvox beta-tubulin genes. Mol Gen Genet. 1988 Aug;213(2-3):315–324. doi: 10.1007/BF00339597. [DOI] [PubMed] [Google Scholar]
- Holst O., Christoffel V., Fründ R., Moll H., Sumper M. A phosphodiester bridge between two arabinose residues as a structural element of an extracellular glycoprotein of Volvox carteri. Eur J Biochem. 1989 May 1;181(2):345–350. doi: 10.1111/j.1432-1033.1989.tb14730.x. [DOI] [PubMed] [Google Scholar]
- Kieliszewski M. J., Lamport D. T. Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J. 1994 Feb;5(2):157–172. doi: 10.1046/j.1365-313x.1994.05020157.x. [DOI] [PubMed] [Google Scholar]
- Kirk D. L., Birchem R., King N. The extracellular matrix of Volvox: a comparative study and proposed system of nomenclature. J Cell Sci. 1986 Feb;80:207–231. doi: 10.1242/jcs.80.1.207. [DOI] [PubMed] [Google Scholar]
- Mages H. W., Tschochner H., Sumper M. The sexual inducer of Volvox carteri. Primary structure deduced from cDNA sequence. FEBS Lett. 1988 Jul 18;234(2):407–410. doi: 10.1016/0014-5793(88)80126-1. [DOI] [PubMed] [Google Scholar]
- Mahuran D., Clements P., Carrella M., Strasberg P. M. A high recovery method for concentrating microgram quantities of protein from large volumes of solution. Anal Biochem. 1983 Mar;129(2):513–516. doi: 10.1016/0003-2697(83)90585-7. [DOI] [PubMed] [Google Scholar]
- Mort A. J., Lamport D. T. Anhydrous hydrogen fluoride deglycosylates glycoproteins. Anal Biochem. 1977 Oct;82(2):289–309. doi: 10.1016/0003-2697(77)90165-8. [DOI] [PubMed] [Google Scholar]
- Rausch H., Larsen N., Schmitt R. Phylogenetic relationships of the green alga Volvox carteri deduced from small-subunit ribosomal RNA comparisons. J Mol Evol. 1989 Sep;29(3):255–265. doi: 10.1007/BF02100209. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schiedlmeier B., Schmitt R., Müller W., Kirk M. M., Gruber H., Mages W., Kirk D. L. Nuclear transformation of Volvox carteri. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5080–5084. doi: 10.1073/pnas.91.11.5080. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Selmer T., Hallmann A., Schmidt B., Sumper M., von Figura K. The evolutionary conservation of a novel protein modification, the conversion of cysteine to serinesemialdehyde in arylsulfatase from Volvox carteri. Eur J Biochem. 1996 Jun 1;238(2):341–345. doi: 10.1111/j.1432-1033.1996.0341z.x. [DOI] [PubMed] [Google Scholar]
- Starr R. C. Control of differentiation in Volvox. Symp Soc Dev Biol. 1970;29:59–100. doi: 10.1016/b978-0-12-395534-0.50009-1. [DOI] [PubMed] [Google Scholar]
- Starr R. C., Jaenicke L. Purification and characterization of the hormone initiating sexual morphogenesis in Volvox carteri f. nagariensis Iyengar. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1050–1054. doi: 10.1073/pnas.71.4.1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sumper M., Berg E., Wenzl S., Godl K. How a sex pheromone might act at a concentration below 10(-16) M. EMBO J. 1993 Mar;12(3):831–836. doi: 10.1002/j.1460-2075.1993.tb05723.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wenzl S., Sumper M. Sulfation of a cell surface glycoprotein correlates with the developmental program during embryogenesis of Volvox carteri. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3716–3720. doi: 10.1073/pnas.78.6.3716. [DOI] [PMC free article] [PubMed] [Google Scholar]