Modulation of endomembranes morphodynamics in the secretory/retrograde pathways depends on lipid diversity

Current Opinion in Plant Biology

Volumn 22, Issue , 2014, Pages 22-29

  Boutté, Yohann ^a   Moreau, Patrick ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE LIPID;

CELL MEMBRANE; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; SECRETORY PATHWAY;

CELL MEMBRANE; LIPID METABOLISM; MEMBRANE LIPIDS; SECRETORY PATHWAY;

EID: 84907457427     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.08.004     Document Type: Review

References (75)

1. Hölzl G., Witt S., Gaude N., Melzer M., Schöttler M.A., Dörmann P. The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiol 2009, 150:1147-1159.
2. Pineau B., Bourge M., Marion J., Mauve C., Gilard F., Maneta-Peyret L., Moreau P., Satiat-Jeunemaître B., Brown S.C., De Paepe R., Danon A. The importance of cardiolipin synthase for mitochondrial ultrastructure, respiratory function, plant development, and stress responses in Arabidopsis. Plant Cell 2013, 25:4195-4208.
3. Pan R., Jones A.D., Hu J. Cardiolipin-mediated mitochondrial dynamics and stress responses in Arabidopsis. Plant Cell 2014, 26:391-409.
4. Nováková P., Hirsch S., Feraru E., Tejos R., van Wijk R., Viaene T., Heilmann M., Lerche J., De Rycke R., Feraru M.I., et al. SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis. Proc Natl Acad Sci USA 2014, 111:2818-2823.
5. Lippincott-Schwartz J., Phair R.D. Lipids and cholesterol as regulators of traffic in the endomembrane system. Annu Rev Biophys 2010, 39:559-578.
6. Melser S., Molino D., Batailler B., Peypelut M., Laloi M., Wattelet-Boyer V., Bellec Y., Faure J.D., Moreau P. Links between lipid homeostasis, organelle morphodynamics and protein trafficking in eukaryotic and plant secretory pathways. Plant Cell Rep 2011, 30:177-193. (Erratum in Plant Cell Rep 2011, 30:675-676).
7. Bankaitis V.A., Garcia-Mata R., Mousley C.J. Golgi membrane dynamics and lipid metabolism. Curr Biol 2012, 22:R414-R424.
8. Surma M.A., Klose C., Simons K. Lipid-dependent protein sorting at the trans-Golgi network. Biochim Biophys Acta 2012, 1821:1059-1067.
9. Voeltz G.K., Prinz W.A. Sheets, ribbons and tubules-how organelles get their shape. Nature 2007, 8:258-264.
10. Kirchhausen T. Bending membranes. Nature 2012, 14:906-908.
11. Stachowiak J.C., Brodsky F.M., Miller E.A. A cost-benefit analysis of the physical mechanisms of membrane curvature. Nat Cell Biol 2013, 15:1019-1027.
12. Stefano G., Renna L., Moss T., McNew J.A., Brandizzi F. In Arabidopsis, the spatial and dynamic organization of the endoplasmic reticulum and Golgi apparatus is influenced by the integrity of the C-terminal domain of RHD3, a non-essential GTPase. Plant J 2012, 69:957-966.
13. Lee H., Sparkes I., Gattolin S., Dzimitrowicz N., Roberts L.M., Hawes C., Frigerio L. An Arabidopsis reticulon and the atlastin homologue RHD3-like2 act together in shaping the tubular endoplasmic reticulum. New Phytol 2013, 197:481-489.
14. West M., Zurek N., Hoenger A., Voeltz G.K. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol 2011, 193:333-346.
15. Okamoto M., Kurokawa K., Matsuura-Tokita K., saito C., Hirata R., Nakano A. High-curvature domains of the ER are important for the organization of ER exit sites in Saccharomyces cerevisiae. J Cell Sci 2012, 125:3412-3420.
16. Bagatolli L.A., Mouritsen O.G. Is the fluid mosaic (and the accompanying raft hypothesis) a suitable model to describe fundamental features of biological membranes? What may be missing?. Front Plant Sci 2013, 4:457.
17. Wang L., Shen W., Kazachkov M., Chen G., Chen Q., Carlsson A.S., Stymne S., Weselake R.J., Zou J. Metabolic interactions between the Lands cycle and the Kennedy pathway of glycerolipid synthesis in Arabidopsis developing seeds. Plant Cell 2012, 24:4652-4669.
18. Ha K.D., Clarke B.A., Brown W.J. Regulation of the Golgi complex by phospholipid remodeling enzymes. Biochim Biophys Acta 2012, 1821:1078-1088.
19. Yang J.S., Valente C., Polishchuk R.S., Turacchio G., Layre E., Moody D.B., Leslie C.C., Gelb M.H., Brown W.J., Corda D., Luini A., Hsu V.W. COPI acts in both vesicular and tubular transport. Nat Cell Biol 2011, 13:996-1003.
20. Arouri A., Mouritsen O.G. Membrane-perturbing effect of fatty acids and lysolipids. Prog Lipid Res 2013, 52:130-140.
21. Kurokawa K., Okamoto M., Nakano A. Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER. Nat Commun 2014, 5:3653. doi: 10.1038/ncomms4653.
22. 2 is required for PIN-FORMED protein trafficking to the plasma membrane in the Arabidopsis root. Plant Cell 2010, 22:1812-1825.
23. 2 plays critical roles in Arabidopsis pollen development and germination. Plant Cell 2011, 23:94-110.
24. Li M., Bahn S.C., Guo L., Musgrave W., berg H., Welti R., Wang X. Patatin-related phospholipase pPLAIIIβ-induced changes in lipid metabolism alter cellulose content and cell elongation in Arabidopsis. Plant Cell 2011, 23:1107-1123.
25. Li G., Xue H.W. Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. Plant Cell 2007, 19:281-295.
26. Pleskot R., Pejchar P., Bezvoda R., Lichtscheidl I.K., Wolters-Arts M., Marc J., Zarsky V., Potocky M. Turnover of phosphatidic acid through distinct signaling pathways affects multiple aspects of pollen tube growth in tobacco. Front Plant Sci 2012, 3:54.
27. Sarri E., Sicart A., Lazaro-Dieguez F., Egea G. Phospholipid synthesis participates in the regulation of diacylglycerol required for membrane trafficking at the Golgi complex. J Biol Chem 2011, 286:28632-28643.
28. Men S., Boutté Y., Ikeda Y., Li X., Palme K., Stierhof Y.D., Hartmann M.A., Moritz T., Grebe M. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 2008, 10:237-244.
29. Boutté Y., Frescatada-Rosa M., Men S., Chow C.M., Ebine K., Gustavsson A., Johansson L., Ueda T., Moore I., Jürgens G. Grebe endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J 2010, 29:546-558.
30. Zhou Y., Peisker H., Weth A., Baumgartner W., Dörmann P., Frentzen M. Extraplastidial cytidinediphosphate diacylglycerol synthase activity is required for vegetative development in Arabidopsis thaliana. Plant J 2013, 75:867-879.
31. Luo Y., Qin G., Zhang J., Liang Y., Song Y., Zhao M., Tsuge T., Aoyama T., Liu J., Gu H., Qu L.J. D-myo-inositol-3-phosphate affects phosphatidylinositol-mediated endomembrane function in Arabidopsis and is essential for auxin-regulated embryogenesis. Plant Cell 2011, 23:1352-1372.
32. Eastmond P.J., Quettier A.L., Kroon J.T.M., Craddock C., Adams N., Slabas A.R. Phosphatidic acid phosphohydrolase 1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. Plant Cell 2010, 22:2796-2811.
33. Melser S., Batailler B., Peypelut M., Poujol C., Bellec Y., Wattelet-Boyer V., Maneta-Peyret L., Faure J.D., Moreau P. Glucosylceramide biosynthesis is involved in Golgi morphology and protein secretion in plant cells. Traffic 2010, 11:479-490.
34. Markham J.E., Lynch D.V., Napier J.A., Dunn T.M., Cahoon E.B. Plant sphingolipids: function follows form. Curr Opin Plant Biol 2013, 16:350-357.
35. Roudier F., Gissot L., Beaudoin F., Haslam R., Michaelson L., Marion J., Molino D., Lima A., Bach L., Morin H., et al. Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. The Plant Cell 2010, 22:364-375.
36. Markham J.E., Molino D., Gissot L., Bellec Y., hematy K., Marion J., Belcram K., Palauqui J.C., Satiat-Jeunemaitre B., Faure J.D. Sphingolipids containing very-long-chain fatty acids define a secretory pathway for specific polar plasma membrane protein targeting in Arabidopsis. Plant Cell 2011, 23:2362-2378.
37. West G., Viitanen L., Alm C., Mattjus P., Salminen T.A., Edqvist J. Identification of a glycosphingolipid transfer protein GLTP1 in Arabidopsis thaliana. FEBS J 2008, 275:3421-3437.
38. D'Angelo G., Rega L.R., De Matteis M.A. Connecting vesicular transport with lipid synthesis: FAPP2. Biochim Biophys Acta 2012, 1821:1089-1095.
39. Vicogne J., Vollenweider D., Smith J.R., Huang P., Frohman M.A., Pessin J.E. Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc Natl Acad Sci USA 2006, 103:14761-14766.
40. Sebastian T.T., Baldridge R.D., Xu P., Graham T.R. Phospholipid flippases: building asymmetric membranes and transport vesicles. Biochim Biophys Acta 2012, 1821:1068-1077.
41. Xu H., Su W., Cai M., Jiang J., Zeng X., Wang H. The asymmetrical structure of Golgi apparatus membranes revealed by in situ atomic force microscope. PLoS One 2013, 8:e61596.
42. 4-ATPase ALA3 localizes to the Golgi and requires a β-subunit to function in lipid translocation and secretory vesicle formation. Plant Cell 2008, 20:658-676.
43. Sorre B., Callan-Jones A., Manneville J.B., Nassoy P., Joanny J.F., Prost J., Goud B., Bassereau P. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc Natl Acad Sci USA 2009, 106:5622-5626.
44. Laloi M., Perret A.M., Chatre L., Melser S., Cantrel C., Vaultier M.N., Zachowski A., Bathany K., Schmitter J.M., Vallet M., et al. Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 2007, 143:1-12.
45. Cacas J.L., Furt F., Le Guédard M., Schmitter J.M., Buré C., Gerbeau-Pissot P., Moreau P., Bessoule J.J., Simon-Plas F., Mongrand S. Lipids of plant membrane rafts. Prog Lipid Res 2012, 51:272-299.
46. Duran J.M., Campelo F., van Galen J., Sachsenheimer T., Sot J., Egorov M.V., Rentero C., Enrich C., Polishchuk R.S., Goni F.M., et al. Sphingomyelin organization is required for vesicle biogenesis at the Golgi complex. EMBO J 2012, 31:4535-4546.
47. Furt F., König S., Bessoule J.J., Sargueil F., Zallot R., Stanislas T., Noirot E., Lherminier J., Simon-Plas F., Heilmann I., Mongrand S. Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane. Plant Physiol 2010, 152:2173-2187.
48. 2e drives recycling through the clathrin-independent endocytic route. J Cell Sci 2014, 127:977-993.
49. Munnik T., Nielsen E. Green light for polyphosphoinositide signals in plants. Curr Op Plant Biol 2011, 14:489-497.
50. Mei Y., Jia W.J., Chu Y.J., Xue H.W. Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins. Cell Res 2012, 22:581-597.
51. Ischebeck T., Werner S., Krishnamoorthy P., Lerche J., Meijón M., Stenzel I., Löfke C., Wiessner T., Im Y.J., Perera I.Y., et al. Phosphatidylinositol 4,5-bisphosphate influences PIN polarization by controlling clathrin-mediated membrane trafficking in Arabidopsis. Plant Cell 2013, 25:4894-4911.
52. Tejos R., Sauer M., Vanneste S., Palacios-Gomez M., Li H., Heilmann M., van Wijk R., Vermeer J.E., Heilmann I., Munnik T., Friml J. Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 2014, 26:2114-2128.
53. Kang B.H., Nielsen E., Preuss M.L., Mastronarde D., Staehelin L.A. Electron tomography of RabA4b- and PI-4Kβ1-labeled trans Golgi network compartments in Arabidopsis. Traffic 2011, 12:313-329.
54. Löfke C., Ischebeck T., König S., Freitag S., Heilmann I. Alternative metabolic fates of phosphatidylinositol produced by phosphatidylinositol synthase isoforms in Arabidopsis thaliana. Biochem J 2008, 413:115-124.
55. Ischebeck T., Vua L.H., Jina X., Stenzela I., Löfke C., Heilmann I. Functional cooperativity of enzymes of phosphoinositide conversion according to synergistic effects on pectin secretion in tobacco pollen tubes. Mol Plant 2010, 3:870-881.
56. Mukherjee S., Soe T.T., Maxfield F.R. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J Cell Biol 1999, 144:1271-1284.
57. Cho H., Kim Y.A., HOWK Phosphate number and acyl chain length determine the subcellular location and lateral mobility of phosphoinositides. Mol Cells 2006, 22:97-103.
58. Ahyayauch H., Villar A.V., Alonso A., Goñi F.M. Modulation of PI-specific phospholipase C by membrane curvature and molecular order. Biochemistry 2005, 44:11592-11600.
59. Kim Y.J., Guzman-Hernandez M.L., Balla T. A highly dynamic ER-derived phosphatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev Cell 2011, 21:813-824.
60. English A.R., Voeltz G.K. Rab10 GTPase regulates ER dynamics and morphology. Nat Cell Biol 2013, 15:169-178.
61. Gidda S.K., Shockey J.M., Falcone M., Kim P.K., Rothstein S.J., Andrews D.W., Dyer J.M., Mullen R.T. Hydrophobic-domain-dependent protein-protein interactions mediate the localization of GPAT enzymes to ER subdomains. Traffic 2011, 12:452-472.
62. Klinkenberg D., long K.R., Shome K., Watkins S.C., Aridor M. A cascade of ER exit site assembly that is regulated by p125A and lipid signals. J Cell Sci 2014, 127:1765-1778.
63. Maeda K., Anand K., Chiapparino A., Kumar A., Poletto M., Kaksonen M., Gavin A.C. Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 2013, 501:257-261.
64. Kajiwara K., Ikedo A., Aguilera-Romero A., Castillon G.A., Kagiwada S., Hanada K., Riezman H., Muniz M., Funato K. Osh proteins regulate COPII-mediated vesicular transport of ceramide from the endoplasmic reticulum in budding yeast. J Cell Sci 2014, 127:376-387.
65. Contreras F.X., Ernst A.M., Haberkant P., Björkholm P., Lindahl E., Gönen B., Tischer C., Elofsson A., von Heijne G., Thiele C., et al. Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 2012, 481:525-529.
66. Surma M.A., Klose C., Klemm R.W., Ejsing C.S., Simons K. Generic sorting of raft lipids into secretory vesicles in yeast. Traffic 2011, 12:1139-1147.
67. Zauber H., Burgos A., garapati P., Schulze W.X. Plasma membrane lipid-protein interactions affect signaling processes in sterol-biosynthesis mutants in Arabidopsis thaliana. Front Plant Sci 2014, 5:78.
68. McLoughlin F., Arisz S.A., Dekker H.L., Kramer G., de Koster C.G., Haring M.A., Munnik T., Testerink C. Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem J 2013, 450:573-581.
69. Haberkant P., Raijmakers R., Wildwater M., Sachsenheimer T., Brügger B., Maeda K., Houweling M., Gavin A.C., Schultz C., van Meer G., Heck A.J.R., Holthuis J.C.M. In vivo profiling and visualization of cellular protein-lipid interactions using bifunctional fatty acids. Angew Chem Int Ed 2013, 52:4033-4038.
70. Blachutzik J.O., Demir F., Kreuzer I., Hedrich R., Harms G.S. Methods of staining and visualization of sphingolipid enriched and non-enriched plasma membrane regions of Arabidopsis thaliana with fluorescent dyes and lipid analogues. Plant Methods 2012, 8:28.
71. Honigmann A., Mueller V., Hell S.W., Eggeling C. STED microscopy detects and quantifies liquid phase separation in lipid membranes using a new far-red emitting fluorescent phosphoglycerolipid analogue. Faraday Discuss 2013, 161:77-89.
72. Owen D.M., Gaus K. Imaging lipid domains in cell membranes: the advent of super-resolution fluorescence microscopy. Front Plant Sci 2013, 4:503.
73. Simon M.L.A., platre M.P., Assil S., van Wijk R., Chen W.Y., Chory J., Dreux M., Munnik T., Jaillais Y. A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J 2014, 77:322-337.
74. Potocký M., Pleskot R., Pejchar P., Vitale N., Kost B., Zárský V. Live-cell imaging of phosphatidic acid dynamics in pollen tubes visualized by Spo20p-derived biosensor. New Phytol 2014, doi:10.1111/nph.12814.
75. Peddie C.J., Blight K., Wilson E., Melia C., Marrison J., Carzaniga R., Domart M.C., O'Toole P., Larijani B., Collinson L.M. Correlative and integrated light and electron microscopy of in-resin GFP fluorescence, used to localize diacylglycerol in mammalian cells. Ultramicroscopy 2014, 143:3-14.