Free-Flow Electrophoresis of Plasma Membrane Vesicles Enriched by Two-Phase Partitioning Enhances the Quality of the Proteome from Arabidopsis Seedlings

Journal of Proteome Research

Volumn 15, Issue 3, 2016, Pages 900-913

  De Michele, Roberto ^a,b   McFarlane, Heather E ^c,d   Parsons, Harriet T ^e,f   Meents, Miranda J ^c   Lao, Jeemeng ^e   González Fernández Niño, Susana M ^e   Petzold, Christopher J ^e   Frommer, Wolf B ^a   Samuels, A Lacey ^c   Heazlewood, Joshua L ^e,g  

^a GEOPHYSICAL LABORATORY   (United States)

^b CNR   (Italy)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Arabidopsis; free flow electrophoresis; plasma membrane

Indexed keywords

CELL MEMBRANE PROTEIN; FLUORESCENT DYE; MEMBRANE PROTEIN; PROTEIN; PROTEOME; ARABIDOPSIS PROTEIN;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ELECTROPHORESIS; FIELD FLOW FRACTIONATION; MEMBRANE VESICLE; MOLECULAR DYNAMICS; NONHUMAN; PEPTIDE LIBRARY; PHASE PARTITIONING; PLANT CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEOMICS; SEEDLING; TANDEM MASS SPECTROMETRY; ISOLATION AND PURIFICATION; METABOLISM; TRANSPORT VESICLE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; ELECTROPHORESIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MEMBRANE PROTEINS; PROTEOME; SEEDLINGS; TANDEM MASS SPECTROMETRY; TRANSPORT VESICLES;

EID: 84960374877     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00876     Document Type: Article

References (94)

1. Kota, U.; Goshe, M. B. Advances in qualitative and quantitative plant membrane proteomics Phytochemistry 2011, 72, 1040-1060 10.1016/j.phytochem.2011.01.027
2. Komatsu, S. Plasma membrane proteome in Arabidopsis and rice Proteomics 2008, 8, 4137-4145 10.1002/pmic.200800088
3. Tan, S.; Tan, H. T.; Chung, M. C. Membrane proteins and membrane proteomics Proteomics 2008, 8, 3924-3932 10.1002/pmic.200800597
4. Chevalier, A. S.; Bienert, G. P.; Chaumont, F. A new LxxxA motif in the transmembrane Helix3 of maize aquaporins belonging to the plasma membrane intrinsic protein PIP2 group is required for their trafficking to the plasma membrane Plant Physiol. 2014, 166, 125-138 10.1104/pp.114.240945
5. Yadeta, K. A.; Elmore, J. M.; Coaker, G. Advancements in the analysis of the Arabidopsis plasma membrane proteome Front. Plant Sci. 2013, 4, 86 10.3389/fpls.2013.00086
6. Vertommen, A.; Panis, B.; Swennen, R.; Carpentier, S. C. Challenges and solutions for the identification of membrane proteins in non-model plants J. Proteomics 2011, 74, 1165-1181 10.1016/j.jprot.2011.02.016
7. Hodges, T. K.; Mills, D. Isolation of the plasma membrane Methods Enzymol. 1986, 118, 41-54 10.1016/0076-6879(86)18063-3
8. Bardy, N.; Carrasco, A.; Galaud, J. P.; Pont-Lezica, R.; Canut, H. Free-flow electrophoresis for fractionation of Arabidopsis thaliana membranes Electrophoresis 1998, 19, 1145-1153 10.1002/elps.1150190715
9. Santoni, V. Plant plasma membrane protein extraction and solubilization for proteomic analysis. In Methods of Molecular Biology; Thiellement, H.; Zivy, M.; Dmerval, C.; Machin, V., Eds.; Humana Press: New York, 2007; Vol. 355, pp 93-109.
10. Larsson, C.; Widell, S.; Sommarin, M. Inside-out plant plasma-membrane vesicles of high-purity obtained by aqueous 2-phase partitioning FEBS Lett. 1988, 229, 289-292 10.1016/0014-5793(88)81142-6
11. Benschop, J. J.; Mohammed, S.; O'Flaherty, M.; Heck, A. J. R.; Slijper, M.; Menke, F. L. H. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis Mol. Cell. Proteomics 2007, 6, 1198-1214 10.1074/mcp.M600429-MCP200
12. Elmore, J. M.; Liu, J.; Smith, B.; Phinney, B.; Coaker, G. Quantitative proteomics reveals dynamic changes in the plasma membrane during Arabidopsis immune signaling Mol. Cell. Proteomics 2012, 11, M111.014555 10.1074/mcp.M111.014555
13. Marmagne, A.; Ferro, M.; Meinnel, T.; Bruley, C.; Kuhn, L.; Garin, J.; Barbier-Brygoo, H.; Ephritikhine, G. A high content in lipid-modified peripheral proteins and integral receptor kinases features in the Arabidopsis plasma membrane proteome Mol. Cell. Proteomics 2007, 6, 1980-1996 10.1074/mcp.M700099-MCP200
14. Nühse, T. S.; Stensballe, A.; Jensen, O. N.; Peck, S. C. Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry Mol. Cell. Proteomics 2003, 2, 1234-1243 10.1074/mcp.T300006-MCP200
15. Schindler, J.; Nothwang, H. G. Aqueous polymer two-phase systems: Effective tools for plasma membrane proteomics Proteomics 2006, 6, 5409-5417 10.1002/pmic.200600243
16. Nühse, T. S.; Stensballe, A.; Jensen, O. N.; Peck, S. C. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database Plant Cell 2004, 16, 2394-2405 10.1105/tpc.104.023150
17. Elortza, F.; Nuhse, T. S.; Foster, L. J.; Stensballe, A.; Peck, S. C.; Jensen, O. N. Proteomic analysis of glycosylphosphatidylinositol-anchored membrane proteins Mol. Cell. Proteomics 2003, 2, 1261-1270 10.1074/mcp.M300079-MCP200
18. Keinath, N. F.; Kierszniowska, S.; Lorek, J.; Bourdais, G.; Kessler, S. A.; Shimosato-Asano, H.; Grossniklaus, U.; Schulze, W. X.; Robatzek, S.; Panstruga, R. PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity J. Biol. Chem. 2010, 285, 39140-39149 10.1074/jbc.M110.160531
19. Li, B.; Takahashi, D.; Kawamura, Y.; Uemura, M. Comparison of plasma membrane proteomic changes of Arabidopsis suspension-cultured cells (T87 Line) after cold and ABA treatment in association with freezing tolerance development Plant Cell Physiol. 2012, 53, 543-554 10.1093/pcp/pcs010
20. Mitra, S. K.; Walters, B. T.; Clouse, S. D.; Goshe, M. B. An efficient organic solvent based extraction method for the proteomic analysis of Arabidopsis plasma membranes J. Proteome Res. 2009, 8, 2752-2767 10.1021/pr801044y
21. Tanz, S. K.; Castleden, I.; Hooper, C. M.; Vacher, M.; Small, I.; Millar, H. a. SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis Nucleic Acids Res. 2013, 41, D1185-D1191 10.1093/nar/gks1151
22. Parsons, H. T.; Christiansen, K.; Knierim, B.; Carroll, A.; Ito, J.; Batth, T. S.; Smith-Moritz, A. M.; Morrison, S.; McInerney, P.; Hadi, M. Z.; Auer, M.; Mukhopadhyay, A.; Petzold, C. J.; Scheller, H. V.; Loqué, D.; Heazlewood, J. L. Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel targets involved in plant cell wall biosynthesis Plant Physiol. 2012, 159, 12-26 10.1104/pp.111.193151
23. Eubel, H.; Heazlewood, J. L.; Millar, A. H. Isolation and subfractionation of plant mitochondria for proteomic analysis. In Plant Proteomics: Methods and Protocols; Thiellement, H.; Zivy, M.; Damerval, C.; Méchin, V., Eds.; Humana Press Inc: Totowa, NJ, 2007; Vol. 335, pp 49-62.
24. Lalonde, S.; Sero, A.; Pratelli, R.; Pilot, G.; Chen, J.; Sardi, M. I.; Parsa, S. A.; Kim, D. Y.; Acharya, B. R.; Stein, E. V.; Hu, H. C.; Villiers, F.; Takeda, K.; Yang, Y.; Han, Y. S.; Schwacke, R.; Chiang, W.; Kato, N.; Loque, D.; Assmann, S. M.; Kwak, J. M.; Schroeder, J. I.; Rhee, S. Y.; Frommer, W. B. A membrane protein/signaling protein interaction network for Arabidopsis version AMPv2 Front. Physiol. 2010, 1, 24 10.3389/fphys.2010.00024
25. Lao, J.; Oikawa, A.; Bromley, J. R.; McInerney, P.; Suttangkakul, A.; Smith-Moritz, A. M.; Plahar, H.; Chiu, T.-Y.; González Fernández-Niño, S. M.; Ebert, B.; Yang, F.; Christiansen, K. M.; Hansen, S. F.; Stonebloom, S.; Adams, P. D.; Ronald, P. C.; Hillson, N. J.; Hadi, M. Z.; Vega-Sanchez, M. E.; Loqué, D.; Scheller, H. V.; Heazlewood, J. L. The plant glycosyltransferase clone collection for functional genomics Plant J. 2014, 79, 517-529 10.1111/tpj.12577
26. Schneider, C. A.; Rasband, W. S.; Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis Nat. Methods 2012, 9, 671-675 10.1038/nmeth.2089
27. Russell, W. K.; Park, Z. Y.; Russell, D. H. Proteolysis in mixed organic-aqueous solvent systems: applications for peptide mass mapping using mass spectrometry Anal. Chem. 2001, 73, 2682-2685 10.1021/ac001332p
28. Shilov, I. V.; Seymour, S. L.; Patel, A. A.; Loboda, A.; Tang, W. H.; Keating, S. P.; Hunter, C. L.; Nuwaysir, L. M.; Schaeffer, D. A. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra Mol. Cell. Proteomics 2007, 6, 1638-1655 10.1074/mcp.T600050-MCP200
29. Vizcaino, J. A.; Deutsch, E. W.; Wang, R.; Csordas, A.; Reisinger, F.; Rios, D.; Dianes, J. A.; Sun, Z.; Farrah, T.; Bandeira, N.; Binz, P. A.; Xenarios, I.; Eisenacher, M.; Mayer, G.; Gatto, L.; Campos, A.; Chalkley, R. J.; Kraus, H. J.; Albar, J. P.; Martinez-Bartolome, S.; Apweiler, R.; Omenn, G. S.; Martens, L.; Jones, A. R.; Hermjakob, H. ProteomeXchange provides globally coordinated proteomics data submission and dissemination Nat. Biotechnol. 2014, 32, 223-226 10.1038/nbt.2839
30. Vizcaino, J. A.; Cote, R. G.; Csordas, A.; Dianes, J. A.; Fabregat, A.; Foster, J. M.; Griss, J.; Alpi, E.; Birim, M.; Contell, J.; O'Kelly, G.; Schoenegger, A.; Ovelleiro, D.; Perez-Riverol, Y.; Reisinger, F.; Rios, D.; Wang, R.; Hermjakob, H. The Proteomics Identifications (PRIDE) database and associated tools: status in 2013 Nucleic Acids Res. 2013, 41, D1063-D1069 10.1093/nar/gks1262
31. Lundgren, D. H.; Hwang, S. I.; Wu, L.; Han, D. K. Role of spectral counting in quantitative proteomics Expert Rev. Proteomics 2010, 7, 39-53 10.1586/epr.09.69
32. Berardini, T. Z.; Mundodi, S.; Reiser, L.; Huala, E.; Garcia-hernandez, M.; Zhang, P.; Mueller, L. A.; Yoon, J.; Doyle, A.; Lander, G.; Moseyko, N.; Yoo, D.; Xu, I.; Zoeckler, B.; Montoya, M.; Miller, N.; Weems, D.; Rhee, S. Y.; Biology, P.; California, T. Z. B. Functional annotation of the Arabidopsis genome using controlled vocabularies Plant Physiol. 2004, 135, 745-755 10.1104/pp.104.040071
33. Alexandersson, E.; Saalbach, G.; Larsson, C.; Kjellbom, P. Arabidopsis plasma membrane proteomics identifies components of transport, signal transduction and membrane trafficking Plant Cell Physiology 2004, 45, 1543-1556 10.1093/pcp/pch209
34. Dunkley, T. P. J.; Hester, S.; Shadforth, I. P.; Runions, J.; Weimar, T.; Hanton, S. L.; Griffin, J. L.; Bessant, C.; Brandizzi, F.; Hawes, C.; Watson, R. B.; Dupree, P.; Lilley, K. S. Mapping the Arabidopsis organelle proteome Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 6518-6523 10.1073/pnas.0506958103
35. Marmagne, A.; Rouet, M.-A.; Ferro, M.; Rolland, N.; Alcon, C.; Joyard, J.; Garin, J.; Barbier-Brygoo, H.; Ephritikhine, G. Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome Mol. Cell. Proteomics 2004, 3, 675-691 10.1074/mcp.M400001-MCP200
36. Nelson, C. J.; Hegeman, A. D.; Harms, A. C.; Sussman, M. R. A quantitative analysis of Arabidopsis plasma membrane using trypsin-catalyzed (18)O labeling Mol. Cell. Proteomics 2006, 5, 1382-1395 10.1074/mcp.M500414-MCP200
37. Borner, G. H. H.; Lilley, K. S.; Stevens, T. J.; Dupree, P.; Centre, C. Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis Plant Physiol. 2003, 132, 568-577 10.1104/pp.103.021170
38. Elortza, F.; Mohammed, S.; Bunkenborg, J.; Foster, L. J.; Nuhse, T. S.; Brodbeck, U.; Peck, S. C.; Jensen, O. N. Modification-specific proteomics of plasma membrane proteins: Identification and characterization of glycosylphosphatidylinositol-anchored proteins released upon phospholipase D treatment J. Proteome Res. 2006, 5, 935-943 10.1021/pr050419u
39. Hemsley, P. a.; Weimar, T.; Lilley, K. S.; Dupree, P.; Grierson, C. S. A proteomic approach identifies many novel palmitoylated proteins in Arabidopsis New Phytol. 2013, 197, 805-814 10.1111/nph.12077
40. Podell, S.; Gribskov, M. Predicting N-terminal myristoylation sites in plant proteins BMC Genomics 2004, 5, 37 10.1186/1471-2164-5-37
41. Bayer, E. M.; Bottrill, A. R.; Walshaw, J.; Vigouroux, M.; Naldrett, M. J.; Thomas, C. L.; Maule, A. J. Arabidopsis cell wall proteome defined using multidimensional protein identification technology Proteomics 2006, 6, 301-311 10.1002/pmic.200500046
42. Fernandez-calvino, L.; Faulkner, C.; Walshaw, J.; Saalbach, G.; Benitez-alfonso, Y.; Maule, A.; Bayer, E. Arabidopsis plasmodesmal proteome PLoS One 2011, 6, e18880 10.1371/journal.pone.0018880
43. Borner, G. H. H.; Sherrier, D. J.; Weimar, T.; Michaelson, L. V.; Hawkins, N. D.; Macaskill, A.; Napier, J. A.; Beale, M. H.; Lilley, K. S.; Dupree, P. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts Plant Physiol. 2005, 137, 104-116 10.1104/pp.104.053041
44. Mizrachi, E.; Mansfield, S. D.; Myburg, A. A. Cellulose factories: advancing bioenergy production from forest trees New Phytol. 2012, 194, 54-62 10.1111/j.1469-8137.2011.03971.x
45. Shin-Han, S.; Bleecker, A. B. Expansion of the receptor-like kinase/pelle gene family and receptor-like proteins in Arabidopsis Plant Physiol. 2003, 132, 530-543 10.1104/pp.103.021964
46. Kang, J.; Park, J.; Choi, H.; Burla, B.; Kretzschmar, T.; Lee, Y.; Martinoia, E. Plant ABC Transporters Arabidopsis Book 2011, 9, 1-25 10.1199/tab.0153
47. Carroll, A.; Heazlewood, J. L.; Ito, J.; Millar, A. H. Analysis of the Arabidopsis cytosolic ribosome proteome by tandem mass spectrometry provides detailed insights into its protein complement and their post-translational modification Mol. Cell. Proteomics 2007, 7, 347-369 10.1074/mcp.M700052-MCP200
48. Sonnhammer, E. L. L.; von Heijne, G.; Krogh, A. A hidden Markov model for predicting transmembrane helices in protein sequences Proceedings of ISMB-98 1998, 6, 175-182
49. Craigon, D. J.; James, N.; Okyere, J.; Higgins, J.; Jotham, J.; May, S. NASCArrays: a repository for microarray data generated by NASC's transcriptomics service Nucleic Acids Res. 2004, 32, 575D-577 10.1093/nar/gkh133
50. Delker, C.; Pöschl, Y.; Raschke, A.; Ullrich, K.; Ettingshausen, S.; Hauptmann, V.; Grosse, I.; Quint, M. Natural variation of transcriptional auxin response networks in Arabidopsis thaliana Plant Cell 2010, 22, 2184-2200 10.1105/tpc.110.073957
51. Canut, H.; Bauer, J.; Weber, G. Separation of plant membranes by electromigration techniques J. Chromatogr., Biomed. Appl. 1999, 722, 121-139 10.1016/S0378-4347(98)00484-8
52. Thimm, O.; Blasing, O.; Gibon, Y.; Nagel, A.; Meyer, S.; Kruger, P.; Selbig, J.; Muller, L. A.; Rhee, S. Y.; Stitt, M. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes Plant J. 2004, 37, 914-939 10.1111/j.1365-313X.2004.02016.x
53. Campos-Soriano, L.; Gomez-Ariza, J.; Bonfante, P.; San Segundo, B. A rice calcium-dependent protein kinase is expressed in cortical root cells during the presymbiotic phase of the arbuscular mycorrhizal symbiosis BMC Plant Biol. 2011, 11, 90 10.1186/1471-2229-11-90
54. Fu, Y.; Li, H.; Yang, Z. B. The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis Plant Cell 2002, 14, 777-794 10.1105/tpc.001537
55. Nikolovski, N.; Rubtsov, D.; Segura, M. P.; Miles, G. P.; Stevens, T. J.; Dunkley, T. P.; Munro, S.; Lilley, K. S.; Dupree, P. Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics Plant Physiol. 2012, 160, 1037-1051 10.1104/pp.112.204263
56. Monneuse, J. M.; Sugano, M.; Becue, T.; Santoni, V.; Hem, S.; Rossignol, M. Towards the profiling of the Arabidopsis thaliana plasma membrane transportome by targeted proteomics Proteomics 2011, 11, 1789-1797 10.1002/pmic.201000660
57. Santoni, V.; Vinh, J.; Pflieger, D.; Sommerer, N.; Maurel, C. A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots Biochem. J. 2003, 373, 289-296 10.1042/bj20030159
58. Canut, H.; Brightman, A.; Boudet, A. M.; Morre, D. J. Plasma-membrane vesicles of opposite sidedness from soybean hypocotyls by preparative Free-Flow Electrophoresis Plant Physiol. 1988, 86, 631-637 10.1104/pp.86.2.631
59. Millar, A. H.; Taylor, N. L. Subcellular proteomics-where cell biology meets protein chemistry Front. Plant Sci. 2014, 5, 55 10.3389/fpls.2014.00055
60. Greenbaum, D.; Colangelo, C.; Williams, K.; Gerstein, M. Comparing protein abundance and mRNA expression levels on a genomic scale Genome Biol. 2003, 4, 1-8 10.1186/gb-2003-4-9-117
61. Wasteneys, G. O.; Ambrose, J. C. Spatial organization of plant cortical microtubules: close encounters of the 2D kind Trends Cell Biol. 2009, 19, 62-71 10.1016/j.tcb.2008.11.004
62. Ambrose, J. C.; Wasteneys, G. O. CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules Mol. Biol. Cell 2008, 19, 4730-4737 10.1091/mbc.E08-06-0665
63. Zhang, Z. J.; Peck, S. C. Simplified enrichment of plasma membrane proteins for proteomic analyses in Arabidopsis thaliana Proteomics 2011, 11, 1780-1788 10.1002/pmic.201000648
64. Gu, Y.; Kaplinsky, N.; Bringmann, M.; Cobb, A.; Carroll, A.; Sampathkumar, A.; Baskin, T. I.; Persson, S.; Somerville, C. R. Identification of a cellulose synthase-associated protein required for cellulose biosynthesis Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 12866-12871 10.1073/pnas.1007092107
65. Mei, Y.; Gao, H. B.; Yuan, M.; Xue, H. W. The Arabidopsis ARCP protein, CSI1, which is required for microtubule stability, is necessary for root and anther development Plant Cell 2012, 24, 1066-1080 10.1105/tpc.111.095059
66. Wang, P. W.; Hawkins, T. J.; Richardson, C.; Cummins, I.; Deeks, M. J.; Sparkes, I.; Hawes, C.; Hussey, P. J. The Plant Cytoskeleton, NET3C, and VAP27 Mediate the Link between the Plasma Membrane and Endoplasmic Reticulum Curr. Biol. 2014, 24, 1397-1405 10.1016/j.cub.2014.05.003
67. Pérez-Sancho, J.; Vanneste, S.; Lee, E.; McFarlane, H. E.; Esteban del Valle, A.; Valpuesta, V.; Friml, J.; Botella, M. A.; Rosado, A. The Arabidopsis Synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses Plant Physiol. 2015, 168, 132-143 10.1104/pp.15.00260
68. Hala, M.; Cole, R.; Synek, L.; Drdova, E.; Pecenkova, T.; Nordheim, A.; Lamkemeyer, T.; Madlung, J.; Hochholdinger, F.; Fowler, J. E.; Zarsky, V. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco Plant Cell 2008, 20, 1330-1345 10.1105/tpc.108.059105
69. Zhang, Y.; Liu, C. M.; Emons, A. M.; Ketelaar, T. The plant exocyst J. Integr. Plant Biol. 2010, 52, 138-146 10.1111/j.1744-7909.2010.00929.x
70. Gadeyne, A.; Sanchez-Rodriguez, C.; Vanneste, S.; Di Rubbo, S.; Zauber, H.; Vanneste, K.; Van Leene, J.; De Winne, N.; Eeckhout, D.; Persiau, G.; Van De Slijke, E.; Cannoot, B.; Vercruysse, L.; Mayers, J. R.; Adamowski, M.; Kania, U.; Ehrlich, M.; Schweighofer, A.; Ketelaar, T.; Maere, S.; Bednarek, S. Y.; Friml, J.; Gevaert, K.; Witters, E.; Russinova, E.; Persson, S.; De Jaeger, G.; Van Damme, D. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants Cell 2014, 156, 691-704 10.1016/j.cell.2014.01.039
71. Rutherford, S.; Moore, I. The Arabidopsis Rab GTPase family: another enigma variation Curr. Opin. Plant Biol. 2002, 5, 518-528 10.1016/S1369-5266(02)00307-2
72. Nielsen, E.; Cheung, A. Y.; Ueda, T. The regulatory RAB and ARF GTPases for vesicular trafficking Plant Physiol. 2008, 147, 1516-1526 10.1104/pp.108.121798
73. Heard, W.; Sklenar, J.; Tome, D. F. A.; Robatzek, S.; Jones, A. M. E. Identification of regulatory and cargo proteins of endosomal and secretory pathways in Arabidopsis thaliana by proteomic dissection Mol. Cell. Proteomics 2015, 14, 1796-1813 10.1074/mcp.M115.050286
74. Jang, J. Y.; Kim, D. G.; Kim, Y. O.; Kim, J. S.; Kang, H. S. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana Plant Mol. Biol. 2004, 54, 713-725 10.1023/B:PLAN.0000040900.61345.a6
75. Palmgren, M. G. Plant plasma membrane H+-ATPases: Powerhouses for nutrient uptake Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52, 817-845 10.1146/annurev.arplant.52.1.817
76. Enns, L. C.; Kanaoka, M. M.; Torii, K. U.; Comai, L.; Okada, K.; Cleland, R. E. Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility Plant Mol. Biol. 2005, 58, 333-349 10.1007/s11103-005-4526-7
77. Chen, X. Y.; Liu, L.; Lee, E.; Han, X.; Rim, Y.; Chu, H.; Kim, S. W.; Sack, F.; Kim, J. Y. The Arabidopsis callose synthase gene GSL8 Is required for cytokinesis and cell patterning Plant Physiol. 2009, 150, 105-113 10.1104/pp.108.133918
78. Töller, A.; Brownfield, L.; Neu, C.; Twell, D.; Schulze-Lefert, P. Dual function of Arabidopsis glucan synthase-like genes GSL8 and GSL10 in male gametophyte development and plant growth Plant J. 2008, 54, 911-923 10.1111/j.1365-313X.2008.03462.x
79. Barral, P.; Suarez, C.; Batanero, E.; Alfonso, C.; Alche, J. D.; Rodriguez-Garcia, M. I.; Villalba, M.; Rivas, G.; Rodriguez, R. An olive pollen protein with allergenic activity, Ole e 10, defines a novel family of carbohydrate-binding modules and is potentially implicated in pollen germination Biochem. J. 2005, 390, 77-84 10.1042/BJ20050456
80. Mansoori, N.; Timmers, J.; Desprez, T.; Kamei, C. L.; Dees, D. C.; Vincken, J. P.; Visser, R. G.; Hofte, H.; Vernhettes, S.; Trindade, L. M. KORRIGAN1 interacts specifically with integral components of the cellulose synthase machinery PLoS One 2014, 9, e112387 10.1371/journal.pone.0112387
81. Desprez, T.; Juraniec, M.; Crowell, E. F.; Jouy, H.; Pochylova, Z.; Parcy, F.; Hofte, H.; Gonneau, M.; Vernhettes, S. Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 15572-15577 10.1073/pnas.0706569104
82. Persson, S.; Paredez, A.; Carroll, A.; Palsdottir, H.; Doblin, M.; Poindexter, P.; Khitrov, N.; Auer, M.; Somerville, C. R. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 15566-15571 10.1073/pnas.0706592104
83. Taylor, N. G. Cellulose biosynthesis and deposition in higher plants New Phytol. 2008, 178, 239-252 10.1111/j.1469-8137.2008.02385.x
84. Worden, N.; Wilkop, T. E.; Esteve, V. E.; Jeannotte, R.; Lathe, R.; Vernhettes, S.; Weimer, B.; Hicks, G.; Alonso, J.; Labavitch, J.; Persson, S.; Ehrhardt, D.; Drakakaki, G. CESA TRAFFICKING INHIBITOR inhibits cellulose deposition and interferes with the trafficking of cellulose synthase complexes and their associated proteins KORRIGAN1 and POM2/CELLULOSE SYNTHASE INTERACTIVE PROTEIN1 Plant Physiol. 2015, 167, 381-U609 10.1104/pp.114.249003
85. Yin, Y. B.; Huang, J. L.; Xu, Y. The cellulose synthase superfamily in fully sequenced plants and algae BMC Plant Biol. 2009, 9, 99 10.1186/1471-2229-9-99
86. Liepman, A. H.; Wilkerson, C. G.; Keegstra, K. Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 2221-2226 10.1073/pnas.0409179102
87. Dhugga, K. S.; Barreiro, R.; Whitten, B.; Stecca, K.; Hazebroek, J.; Randhawa, G. S.; Dolan, M.; Kinney, A. J.; Tomes, D.; Nichols, S.; Anderson, P. Guar seed beta-mannan synthase is a member of the cellulose synthase super gene family Science 2004, 303, 363-366 10.1126/science.1090908
88. Yin, L.; Verhertbruggen, Y.; Oikawa, A.; Manisseri, C.; Knierim, B.; Prak, L.; Jensen, J. K.; Knox, J. P.; Auer, M.; Willats, W. G. T.; Scheller, H. V. The cooperative activities of CSLD2, CSLD3, and CSLD5 are required for normal Arabidopsis development Mol. Plant 2011, 4, 1024-1037 10.1093/mp/ssr026
89. Elkins, T.; Hortsch, M.; Bieber, A. J.; Snow, P. M.; Goodman, C. S. Drosophila fasciclin-I is a novel homophilic adhesion molecule that along with fasciclin-III can mediate cell sorting J. Cell Biol. 1990, 110, 1825-1832 10.1083/jcb.110.5.1825
90. Harpaz-Saad, S.; McFarlane, H. E.; Xu, S. L.; Divi, U. K.; Forward, B.; Western, T. L.; Kieber, J. J. Cellulose synthesis via the FEI2 RLK/SOS5 pathway and CELLULOSE SYNTHASE 5 is required for the structure of seed coat mucilage in Arabidopsis Plant J. 2011, 68, 941-953 10.1111/j.1365-313X.2011.04760.x
91. MacMillan, C. P.; Mansfield, S. D.; Stachurski, Z. H.; Evans, R.; Southerton, S. G. Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus Plant J. 2010, 62, 689-703 10.1111/j.1365-313X.2010.04181.x
92. Johnson, K. L.; Jones, B. J.; Bacic, A.; Schultz, C. J. The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules Plant Physiol. 2003, 133, 1911-1925 10.1104/pp.103.031237
93. Song, D.; Shen, J.; Li, L. Characterization of cellulose synthase complexes in Populus xylem differentiation New Phytol. 2010, 187, 777-790 10.1111/j.1469-8137.2010.03315.x
94. Stanislas, T.; Bouyssie, D.; Rossignol, M.; Vesa, S.; Fromentin, J.; Morel, J.; Pichereaux, C.; Monsarrat, B.; Simon-Plas, F. Quantitative proteomics reveals a dynamic association of proteins to detergent-resistant membranes upon elicitor signaling in tobacco Mol. Cell. Proteomics 2009, 8, 2186-2198 10.1074/mcp.M900090-MCP200