The SEC6 protein is required for contractile vacuole function in Chlamydomonas reinhardtii

Journal of Cell Science

Volumn 125, Issue 12, 2012, Pages 2885-2895

  Komsic Buchmann, Karin ^a   Stephan, Lisa Marie ^a   Becker, Burkhard ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Chlamydomonas; Contractile vacuole; Exocyst; Flagella; Osmoregulation; SEC6

Indexed keywords

ALGAL PROTEIN; EXOCYST; GREEN FLUORESCENT PROTEIN; HYPOTONIC SOLUTION; PROTEIN SEC 6; UNCLASSIFIED DRUG;

ALGAL GENETICS; ARTICLE; CELL FUNCTION; CELL GROWTH; CELL ISOLATION; CELL LINE; CELL MEMBRANE; CELL MUTANT; CELL ORGANELLE; CHLAMYDOMONAS REINHARDTII; CONTRACTILE VACUOLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXOCYTOSIS; FLAGELLUM; GENE OVEREXPRESSION; MEMBRANE FUSION; MICROSCOPY; NONHUMAN; ORGANELLE SHAPE; OSMOREGULATION; PRIORITY JOURNAL;

BIOLOGICAL TRANSPORT; CHLAMYDOMONAS REINHARDTII; EXOCYTOSIS; GREEN FLUORESCENT PROTEINS; PLANT PROTEINS; VACUOLES; WATER-ELECTROLYTE BALANCE;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; PROTISTA;

EID: 84869121384     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.099184     Document Type: Article

References (59)

1. Allen, R. D. (2000). The contractile vacuole and its membrane dynamics. Bioessays 22, 1035-1042.
2. Allen, R. D. and Naitoh, Y. (2002). Osmoregulation and contractile vacuoles of protozoa. Int. Rev. Cytol. 215, 351-394.
3. Anderberg, H. I., Danielson, J. Å. and Johanson, U. (2011). Algal MIPs, high diversity and conserved motifs. BMC Evol. Biol. 11, 110.
4. Becker, B. and Hickisch, A. (2005). Inhibition of contractile vacuole function by brefeldin A. Plant Cell Physiol. 46, 201-212.
5. Berthold, P., Schmitt, R. and Mages, W. (2002). An engineered Streptomyces hygroscopicus aph 70 gene mediates dominant resistance against hygromycin B in Chlamydomonas reinhardtii. Protist 153, 401-412.
6. Bröcker, C., Engelbrecht-Vandré, S. and Ungermann, C. (2010). Multisubunit tethering complexes and their role in membrane fusion. Curr. Biol. 20, R943-R952.
7. Buchmann, K. and Becker, B. (2009). The system of contractile vacuoles in the green alga Mesostigma viride (Streptophyta). Protist 160, 427-443.
8. Bush, J., Nolta, K., Rodriguez-Paris, J., Kaufmann, N., O'Halloran, T., Ruscetti, T., Temesvari, L., Steck, T. and Cardelli, J. (1994). A Rab4-like GTPase in Dictyostelium discoideum colocalizes with V-H(+)-ATPases in reticular membranes of the contractile vacuole complex and in lysosomes. J. Cell Sci. 107, 2801-2812.
9. Coll, J. M. (2006). Methodologies for transferring DNA into eukaryotic microalgae. Span. J. Agric. Res. 4, 316-330.
10. Das, A. and Guo, W. (2011). Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol. 21, 383-386.
11. Fok, A. K., Yamauchi, K., Ishihara, A., Aihara, M. S., Ishida, M. and Allen, R. D. (2002). The vacuolar-atpase of Paramecium multimicronucleatum: gene structure of the B subunit and the dynamics of the V-ATPase-rich osmoregulatory membranes. J. Eukaryot. Microbiol. 49, 185-196.
12. Fuhrmann, M., Oertel, W. and Hegemann, P. (1999). A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J. 19, 353-361.
13. González-Ballester, D., de Montaigu, A., Galván, A. and Fernández, E. (2005). Restriction enzyme site-directed amplification PCR: a tool to identify regions flanking a marker DNA. Anal. Biochem. 340, 330-335.
14. Gonzalez-Ballester, D., Pootakham, W., Mus, F., Yang, W. Q., Catalanotti, C., Magneschi, L., de Montaigu, A., Higuera, J. J., Prior, M., Galván, A. et al. (2011). Reverse genetics in Chlamydomonas: a platform for isolating insertional mutants. Plant Methods 7, 24.
15. Gorman, D. S. and Levine, R. P. (1965). Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc. Natl. Acad. Sci. USA 54, 1665-1669.
16. Grossman, A. R., Harris, E. E., Hauser, C., Lefebvre, P. A., Martinez, D., Rokhsar, D., Shrager, J., Silflow, C. D., Stern, D., Vallon, O. et al. (2003). Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot. Cell 2, 1137-1150.
17. Hála, M., Cole, R., Synek, L., Drdová, E., Pecenková, T., Nordheim, A., Lamkemeyer, T., Madlung, J., Hochholdinger, F., Fowler, J. E. et al. (2008). An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20, 1330-1345.
18. Harris, E., Yoshida, K., Cardelli, J. and Bush, J. (2001). Rab11-like GTPase associates with and regulates the structure and function of the contractile vacuole system in Dictyostelium. J. Cell Sci. 114, 3035-3045.
19. Heuser, J., Zhu, Q. and Clarke, M. (1993). Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J. Cell Biol. 121, 1311-1327.
20. Hoffmann, E. K. (1986). Anion transport systems in the plasma membrane of vertebrate cells. Biochim. Biophys. Acta 864, 1-31.
21. Huang, K., Diener, D. R., Mitchell, A., Pazour, G. J., Witman, G. B. and Rosenbaum, J. L. (2007). Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. J. Cell Biol. 179, 501-514.
22. Kindle, K. L. (1990). High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87, 1228-1232.
23. Kissmehl, R., Schilde, C., Wassmer, T., Danzer, C., Nuehse, K., Lutter, K. and Plattner, H. (2007). Molecular identification of 26 syntaxin genes and their assignment to the different trafficking pathways in Paramecium. Traffic 8, 523-542.
24. Komsic-Buchmann, K. and Becker, B. (2012). Contractile vacuoles in green algae -structure and function. In Advances in Algal Cell Biology (ed. K. Heimann and C. Katsaros). Berlin: Walter de Gruyter.
25. Koumandou, V. L., Dacks, J. B., Coulson, R. M. R. and Field, M. C. (2007). Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol. Biol. 7, 29.
26. Luykx, P., Hoppenrath, M. and Robinson, D. G. (1997a). Osmoregulatory mutants that affect the function of the contractile vacuole in Chlamydomonas reinhardtii. Protoplasma 200, 99-111.
27. Luykx, P., Hoppenrath, M. and Robinson, D. G. (1997b). Structure and behavior of contractile vacuoles in Chlamydomonas reinhardtii. Protoplasma 198, 73-84.
28. Matsuo, T., Okamoto, K., Onai, K., Niwa, Y., Shimogawara, K. and Ishiura, M. (2008). A systematic forward genetic analysis identified components of the Chlamydomonas circadian system. Genes Dev. 22, 918-930.
29. McKanna, J. A. (1973). Fine structure of the contractile vacuole pore in Paramecium. J. Protozool. 20, 631-638.
30. Merchant, S. S., Prochnik, S. E., Vallon, O., Harris, E. H., Karpowicz, S. J., Witman, G. B., Terry, A., Salamov, A., Fritz-Laylin, L. K., Maréchal-Drouard, L. et al. (2007). The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250.
31. Montalvetti, A., Rohloff, P. and Docampo, R. (2004). A functional aquaporin colocalizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi. J. Biol. Chem. 279, 38673-38682.
32. Morgera, F., Sallah, M. R., Dubuke, M. L., Gandhi, P., Brewer, D. N., Carr, C. M. and Munson, M. (2012). Regulation of exocytosis by the exocyst subunit Sec6 and the SM protein Sec1. Mol. Biol. Cell 23, 337-346.
33. Neupert, J., Karcher, D. and Bock, R. (2009). Generation of Chlamydomonas strains that efficiently express nuclear transgenes. Plant J. 57, 1140-1150.
34. Nishihara, E., Yokota, E., Tazaki, A., Orii, H., Katsuhara, M., Kataoka, K., Igarashi, H., Moriyama, Y., Shimmen, T. and Sonobe, S. (2008). Presence of aquaporin and V-ATPase on the contractile vacuole of Amoeba proteus. Biol. Cell 100, 179-188.
35. Patterson, D. J. (1980). Contractile vacuoles and associated structures: their organization and function. Biol. Rev. Camb. Philos. Soc. 55, 1-46.
36. Patterson, D. J. (1981). Contractile vacuole complex behavior as a diagnostic character for free-living amebas. Protistologica (Paris) 17, 243-248.
37. Potenza, M., Bowser, R., Müller, H. and Novick, P. (1992). SEC6 encodes an 85 kDa soluble protein required for exocytosis in yeast. Yeast 8, 549-558.
38. Ralser, M., Querfurth, R., Warnatz, H. J., Lehrach, H., Yaspo, M. L. and Krobitsch, S. (2006). An efficient and economic enhancer mix for PCR. Biochem. Biophys. Res. Commun. 347, 747-751.
39. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
40. Robinson, D. G., Hoppenrath, M., Oberbeck, K., Luyks, P. and Ratajczak, R. (1998). Localization of pyrophosphatase and V-ATPase in Chlamydomonas reinhardtii. Bot. Acta 111, 108-122.
41. Rogers, K. K., Wilson, P. D., Snyder, R. W., Zhang, X., Guo, W., Burrow, C. R. and Lipschutz, J. H. (2004). The exocyst localizes to the primary cilium in MDCK cells. Biochem. Biophys. Res. Commun. 319, 138-143.
42. Rohloff, P. and Docampo, R. (2008). A contractile vacuole complex is involved in osmoregulation in Trypanosoma cruzi. Exp. Parasitol. 118, 17-24.
43. Rohloff, P., Montalvetti, A. and Docampo, R. (2004). Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi. J. Biol. Chem. 279, 52270-52281.
44. Ruiz, F. A., Marchesini, N., Seufferheld, M., Govindjee and Docampo, R. (2001). The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J. Biol. Chem. 276, 46196-46203.
45. Ruiz-Binder, N. E., Geimer, S. and Melkonian, M. (2002). In vivo localization of centrin in the green alga Chlamydomonas reinhardtii. Cell Motil. Cytoskeleton 52, 43-55.
46. Schilde, C., Wassmer, T., Mansfeld, J., Plattner, H. and Kissmehl, R. (2006). A multigene family encoding R-SNAREs in the ciliate Paramecium tetraurelia. Traffic 7, 440-455.
47. Schoppmeier, J., Mages, W. and Lechtreck, K. F. (2005). GFP as a tool for the analysis of proteins in the flagellar basal apparatus of Chlamydomonas. Cell Motil. Cytoskeleton 61, 189-200.
48. Schroda, M. (2006). RNA silencing in Chlamydomonas: mechanisms and tools. Curr. Genet. 49, 69-84.
49. Shimogawara, K., Fujiwara, S., Grossman, A. and Usuda, H. (1998). High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148, 1821-1828.
50. Stavrou, I. and O'Halloran, T. J. (2006). The monomeric clathrin assembly protein, AP180, regulates contractile vacuole size in Dictyostelium discoideum. Mol. Biol. Cell 17, 5381-5389.
51. Stock, C., Grønlien, H. K., Allen, R. D. and Naitoh, Y. (2002). Osmoregulation in Paramecium: in situ ion gradients permit water to cascade through the cytosol to the contractile vacuole. J. Cell Sci. 115, 2339-2348.
52. Taft, M. H., Hartmann, F. K., Rump, A., Keller, H., Chizhov, I., Manstein, D. J. and Tsiavaliaris, G. (2008). Dictyostelium myosin-5b is a conditional processive motor. J. Biol. Chem. 283, 26902-26910.
53. Tominaga, T., Allen, R. D. and Naitoh, Y. (1998). Electrophysiology of the in situ contractile vacuole complex of Paramecium reveals its membrane dynamics and electrogenic site during osmoregulatory activity. J. Exp. Biol. 201, 451-460.
54. Wassmer, T., Froissard, M., Plattner, H., Kissmehl, R. and Cohen, J. (2005). The vacuolar proton-ATPase plays a major role in several membrane-bounded organelles in Paramecium. J. Cell Sci. 118, 2813-2825.
55. Weiss, R. L., Goodenough, D. A. and Goodenough, U. W. (1977). Membrane particle arrays associated with the basal body and with contractile vacuole secretion in Chlamydomonas. J. Cell Biol. 72, 133-143.
56. Zanchi, R., Howard, G., Bretscher, M. S. and Kay, R. R. (2010). The exocytic gene secA is required for Dictyostelium cell motility and osmoregulation. J. Cell Sci. 123, 3226-3234.
57. Zeuthen, T. (1992). From contractile vacuole to leaky epithelia. Coupling between salt and water fluxes in biological membranes. Biochim. Biophys. Acta 1113, 229-258.
58. Zhang, Y., Liu, C. M., Emons, A. M. C. and Ketelaar, T. (2010). The plant exocyst. J. Integr. Plant Biol. 52, 138-146.
59. Zuo, X., Guo, W. and Lipschutz, J. H. (2009). The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol. Biol. Cell 20, 2522-2529.