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Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo

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Tolley, Nicholas, Sparkes, Imogen, Craddock, Christian P., Eastmond, Peter J., Runions, John, Hawes, C. R. and Frigerio, Lorenzo. (2010) Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo. Plant Journal, Volume 64 (Number 3). pp. 411-418. ISSN 0960-7412

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Official URL: http://dx.doi.org/10.1111/j.1365-313X.2010.04337.x

Abstract

Reticulons are integral endoplasmic reticulum (ER) membrane proteins that have the ability to shape the ER into tubules. It has been hypothesized that their unusually long conserved hydrophobic regions cause reticulons to assume a wedge-like topology that induces membrane curvature. Here we provide proof of this hypothesis. When over-expressed, an Arabidopsis thaliana reticulon (RTNLB13) localized to, and induced constrictions in, cortical ER tubules. Ectopic expression of RTNLB13 was sufficient to induce ER tubulation in an Arabidopsis mutant (pah1 pah2) whose ER membrane is mostly present in a sheet-like form. By sequential shortening of the four transmembrane domains (TMDs) of RTNLB13, we show that the length of the transmembrane regions is directly correlated with the ability of RTNLB13 to induce membrane tubulation and to form low-mobility complexes within the ER membrane. We also show that full-length TMDs are necessary for the ability of RTNLB13 to reside in the ER membrane.

Item Type:	Journal Article
Subjects:	Q Science > QH Natural history > QH301 Biology Q Science > QK Botany
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010) Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH):	Endoplasmic reticulum, Plant organelles, Golgi apparatus
Journal or Publication Title:	Plant Journal
Publisher:	Blackwell
ISSN:	0960-7412
Date:	November 2010
Volume:	Volume 64
Number:	Number 3
Number of Pages:	8
Page Range:	pp. 411-418
Identification Number:	10.1111/j.1365-313X.2010.04337.x
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), European Union (EU)
Grant number:	LSH-2002-1.2.5-2 (EU)
References:	Batoko, H., Zheng, H.-Q., Hawes, C. and Moore, I. (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus for normal Golgi movement in plants. Plant Cell 12, 2201-2217. Bernsel, A., Viklund, H., Falk, J., Lindahl, E., von Heijne, G. and Elofsson, A. (2008) Prediction of membrane-protein topology from first principles. Proc Natl Acad Sci USA 105, 7177-7181. Brandizzi, F., Frangne, N., Marc-Martin, S., Hawes, C., Neuhaus, J. M. and Paris, N. (2002) The Destination for Single-Pass Membrane Proteins Is Influenced Markedly by the Length of the Hydrophobic Domain. Plant Cell 14, 1077-1092. Eastmond, P., Quettier, A.-L., Kroon, J., Craddock, C., Adams, N. and Slabas, A. (2010) PHOSPHATIDIC ACID PHOSPHOHYDROLASES1 & 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. Plant Cell 22, in press. Hu, J., Shibata, Y., Voss, C., Shemesh, T., Li, Z., Coughlin, M., Kozlov, M. M., Rapoport, T. A. and Prinz, W. A. (2008) Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319, 1247-50. Nakamura, Y., Koizumi, R., Shui, G., Shimojima, M., Wenk, M. R., Ito, T. and Ohta, H. (2009) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc Natl Acad Sci USA 106, 20978-20983. Nerlich, A., von Orlow, M., Rontein, D., Hanson, A. D. and Dormann, P. (2007) Deficiency in phosphatidylserine decarboxylase activity in the psd1 psd2 psd3 triple mutant of Arabidopsis affects phosphatidylethanolamine accumulation in mitochondria. Plant Physiol 144, 904-14. Nziengui, H., Bouhidel, K., Pillon, D., Der, C., Marty, F. and Schoefs, B. (2007) Reticulon-like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Lett 581, 3356-62. Nziengui, H. and Schoefs, B. (2009) Functions of reticulons in plants: What we can learn from animals and yeasts. Cell Mol Life Sci 66, 584-95. Oertle, T., Klinger, M., Stuermer, C. A. O. and Schwab, M. E. (2003) A reticular rhapsody: phylogenic evolution and nomenclature of the RTN/Nogo gene family. FASEB J. 17, 1238-1247. Pedrazzini, E. (2009) Tail-anchored proteins in plants. J Plant Biol 52, 88-101. Runions, J., Brach, T., Kuhner, S. and Hawes, C. (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 57, 43-50. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D. and Lohmann, J. U. (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37, 501-6. Shibata, Y., Voss, C., Rist, J. M., Hu, J., Rapoport, T. A., Prinz, W. A. and Voeltz, G. K. (2008) The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J Biol Chem 283, 18892-904. Shibata, Y., Hu, J., Kozlov, M. M. and Rapoport, T. A. (2009) Mechanisms shaping the membranes of cellular organelles. Ann Rev Cell Dev Biol 25, 329-354. Sparkes, I., Runions, J., Hawes, C. and Griffing, L. (2009a) Movement and Remodeling of the Endoplasmic Reticulum in Nondividing Cells of Tobacco Leaves. Plant Cell 21, 3937-3949. Sparkes, I., Tolley, N., Aller, I., Svozil, J., Osterrieder, A., Botchway, S., Frigerio, L. and Hawes, C. (2010) Five plant reticulon isoforms share ER location, topology and membrane shaping properties. Plant Cell 22, 1333-1343. Sparkes, I. A., Frigerio, L., Tolley, N. and Hawes, C. (2009b) The plant endoplasmic reticulum: a cell-wide web. Biochem J 423, 145-55. Sparkes, I. A., Runions, J., Kearns, A. and Hawes, C. (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1, 2019-25. Tolley, N., Sparkes, I. A., Hunter, P. R., Craddock, C. P., Nuttall, J., Roberts, L. M., Hawes, C., Pedrazzini, E. and Frigerio, L. (2008) Overexpression of a Plant Reticulon Remodels the Lumen of the Cortical Endoplasmic Reticulum but Does not Perturb Protein Transport. Traffic 9, 94-102. Voeltz, G. K., Prinz, W. A., Shibata, Y., Rist, J. M. and Rapoport, T. A. (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573-586. Yang, Y. S. and Strittmatter, S. M. (2007) The reticulons: a family of proteins with diverse functions. Genome Biol 8, 234. Zimmerberg, J. and Kozlov, M. M. (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7, 9-19.
URI:	http://wrap.warwick.ac.uk/id/eprint/4778