Abstract
Syntaxins interact with other SNAREs (soluble NSF-attachment protein receptors) to form structurally related complexes1 that mediate membrane fusion in diverse intracellular trafficking pathways2,3,4,5. The original SNARE hypothesis6 postulated that each type of transport vesicle has its own distinct vesicle-SNARE that pairs up with a unique target-SNARE, or syntaxin, on the target membrane. However, recent evidence suggests that small G-proteins of the Rab family and their effectors mediate the initial contact between donor and acceptor membranes7, providing complementary specificity to SNARE pairing at a later step towards membrane fusion3,4,5. To assess the role of syntaxin specificity in membrane recognition requires a biological assay in which one syntaxin is replaced by other family members that do not normally function in that trafficking pathway. Here, we examine whether membrane fusion in Arabidopsis thaliana cytokinesis, which involves a plant-specific syntaxin, the cell-cycle-regulated KNOLLE (KN) protein8,9, can be mediated by other syntaxins if expressed under the control of KN cis-regulatory sequences. Only a non-essential syntaxin was targeted to the plane of cell division and sufficiently related to KN to perform its function, thus revealing syntaxin specificity of cytokinesis.
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References
Antonin, W., Fasshauer, D., Becker, S., Jahn, R. & Schneider, T.R. Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nature Struct. Biol. 9, 107–111 (2002).
McNew, J.A. et al. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407, 153–159 (2000).
Pelham, H.R. SNAREs and the specificity of membrane fusion. Trends Cell Biol. 11, 99–101 (2001).
Chen, Y.A. & Scheller, R.H. SNARE-mediated membrane fusion. Nature Rev. Mol. Cell Biol. 2, 98–106 (2001).
Jahn, R., Lang, T. & Südhof, T.C. Membrane fusion. Cell 112, 519–533 (2003).
Rothman, J.E. Mechanisms of intracellular protein transport. Nature 372, 55–63 (1994).
Zerial, M. & McBride, H. Rab proteins as membrane organizers. Nature Rev. Mol. Cell Biol. 2, 107–119 (2001).
Lukowitz, W., Mayer, U. & Jürgens, G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84, 61–71 (1996).
Lauber, M.H. et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485–1493 (1997).
Bednarek, S.Y. & Falbel, T.G. Membrane trafficking during plant cytokinesis. Traffic 3, 621–629 (2002).
Staehelin, L.A. & Hepler, P.K. Cytokinesis in higher plants. Cell 84, 821–824 (1996).
Geldner, N., Friml, J., Stierhof, Y.-D., Jürgens, G. & Palme, K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001).
Zuo, J. et al. Korrigan, an Arabidopsis endo-1,4-β-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12, 1137–1152 (2000).
Yokoyama, R. & Nishitani, K. Endoxyloglucan transferase is localized both in the cell plate and in the secretory pathway destined for the apoplast in tobacco cells. Plant Cell Physiol. 42, 292–300 (2001).
Sanderfoot, A.A., Assaad, F.F. & Raikhel, N.V. The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiol. 124, 1558–1569 (2000).
Waizenegger, I. et al. The Arabidopsis KNOLLE and KEULE genes interact to promote vesicle fusion during cytokinesis. Curr. Biol. 10, 1371–1374 (2000).
Völker, A., Stierhof, Y.-D. & Jürgens Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin Knolle results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. G. J. Cell Sci. 114, 3001–3012 (2001).
Bassham, D.C., Gal, S., da Silva Conceicao, A. & Raikhel, N.V. An Arabidopsis syntaxin homologue isolated by functional complementation of a yeast pep12 mutant. Proc. Natl Acad. Sci. USA 92, 7262–7266 (1995).
da Silva Conceicao, A. et al. The syntaxin homolog AtPEP12p resides on a late post-Golgi compartment in plants. Plant Cell 9, 571–582 (1997).
Sanderfoot, A.A., Pilgrim, M., Adam, L. & Raikhel, N.V. Disruption of individual members of Arabidopsis syntaxin gene families indicates each has essential functions. Plant Cell 13, 659–666 (2001).
Leyman, B., Geelen, D. & Blatt, M.R. Localization and control of expression of Nt-Syr1, a tobacco SNARE protein. Plant J. 24, 369–381 (2000).
Mayer, U., Torres-Ruiz, R.A., Berleth, T., Miséra, S. & Jürgens, G. Mutations affecting body organization in the Arabidopsis embryo. Nature 353, 402–407 (1991).
Clough, S.J. & Bent, A.F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).
Grebe, M. et al. A conserved domain of the Arabidopsis GNOM protein mediates subunit interaction and cyclophilin 5 binding. Plant Cell 12, 343–356 (2000).
Sambrook, J., Fritsch, E.F. & Maniatis, T. Molecular Cloning: A Laboratory Manual. 2nd edn (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1989).
Hamann, T., Benkova, E., Bäurle, I., Kientz, M. & Jürgens, G. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 16, 1610–1615 (2002).
Thompson, J.D., Higgins, D.G. & Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673–4680 (1994).
Acknowledgements
We thank C. Brill for in-situ hybridisation, and N. Anders, K. Cornelis, J. Friml, N. Geldner, M. Guttenberger, T. Pacher, D. Weijers and H. Wolters for critical reading of the manuscript. This work was supported by grant Ju 179/10-1 from the Deutsche Forschungsgemeinschaft.
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Müller, I., Wagner, W., Völker, A. et al. Syntaxin specificity of cytokinesis in Arabidopsis. Nat Cell Biol 5, 531–534 (2003). https://doi.org/10.1038/ncb991
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DOI: https://doi.org/10.1038/ncb991
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