Fluorescent protein tagging as a tool to define the subcellular distribution of proteins in plants

Frontiers in Plant Science

Volumn 4, Issue JUN, 2013, Pages

  Tanz, Sandra K ^a   Castleden, Ian ^a   Small, Ian D ^a   Harvey Millar, A ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Arabidopsis; Database; FP tagging; Subcellular localization; Subcellular proteomics

Indexed keywords

EID: 84887555324     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00214     Document Type: Review

References (89)

1. Asano, T., Yoshioka, Y., Kurei, S., Sakamoto, W., and Machida, Y. (2004). A mutation of the CRUMPLED LEAF gene that encodes a protein localized in the outer envelope membrane of plastids affects the pattern of cell division, cell differentiation, and plastid division in Arabidopsis. Plant J. 38, 448-459. doi: 10.1111/j.1365-313X.2004.02057.x
2. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., et al. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591-602. doi: 10.1016/S0092-8674(03)00924-3
3. Berg, R. H., and Beachy, R. N. (2008). Fluorescent protein applications in plants. Method Cell Biol. 85, 153-177. doi: 10.1016/S0091-679X(08)85008-X
4. Briesemeister, S., Rahnenfuhrer, J., and Kohlbacher, O. (2010). YLoc-an interpretable web server for predicting subcellular localization. Nucleic Acids Res. 38, W497-W502. doi: 10.1093/nar/gkq477
5. Brugiere, S., Kowalski, S., Ferro, M., Seigneurin-Berny, D., Miras, S., Salvi, D., et al. (2004). The hydrophobic proteome of mitochondrial membranes from Arabidopsis cell suspensions. Phytochemistry 65, 1693-1707. doi: 10.1016/j.phytochem.2004.03.028
6. Carrie, C., Kuhn, K., Murcha, M. W., Duncan, O., Small, I. D., O'Toole, N., et al. (2009). Approaches to defining dual-targeted proteins in Arabidopsis. Plant J. 57, 1128-1139. doi: 10.1111/j.1365-313X.2008.03745.x
7. Carrie, C., Murcha, M. W., Kuehn, K., Duncan, O., Barthet, M., Smith, P. M., et al. (2008). Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett. 582, 3073-3079. doi: 10.1016/j.febslet.2008.07.061
8. Carrie, C., and Small, I. (2012). A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochim. Biophys. Acta. 1833, 253-259. doi: 10.1016/j.bbamcr.2012.05.029
9. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W., and Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805. doi: 10.1126/science.8303295
10. Chartrand, P., Meng, X. H., Singer, R. H., and Long, R. M. (1999). Structural elements required for the localization of ASH1 mRNA and of a green fluorescent protein reporter particle in vivo. Curr. Biol. 9, 333-336. doi: 10.1016/S0960-9822(99)80144-4
11. Chew, O., Lister, R., Qbadou, S., Heazlewood, J. L., Soll, J., Schleiff, E., et al. (2004). A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor. FEBS Lett. 557, 109-114. doi: 10.1016/S0014-5793(03)01457-1
12. Chew, O., Rudhe, C., Glaser, E., and Whelan, J. (2003). Characterization of the targeting signal of dual-targeted pea glutathione reductase. Plant Mol. Biol. 53, 341-356. doi: 10.1023/B:PLAN.0000006939.87660.4f
13. Chou, K. C., and Shen, H. B. (2010). Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5:e11335. doi: 10.1371/journal.pone.0011335
14. Cutler, S. R., Ehrhardt, D. W., Griffitts, J. S., and Somerville, C. R. (2000). Random GFP: cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. U.S.A. 97, 3718-3723. doi: 10.1073/pnas.97.7.3718
15. Deblasio, S. L., Sylvester, A. W., and Jackson, D. (2010). Illuminating plant biology: using fluorescent proteins for high-throughput analysis of protein localization and function in plants. Brief. Funct. Genom. 9, 129-138. doi: 10.1093/bfgp/elp060
16. Dixit, R., Cyr, R., and Gilroy, S. (2006). Using intrinsically fluorescent proteins for plant cell imaging. Plant J. 45, 599-615. doi: 10.1111/j.1365-313X.2006.02658.x
17. Duchene, A. M., Giritch, A., Hoffmann, B., Cognat, V., Lancelin, D., Peeters, N. M., et al. (2005). Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 102, 16484-16489. doi: 10.1073/pnas.0504682102
18. Ehrhardt, D. (2003). GFP technology for live cell imaging. Curr. Opin. Plant Biol. 6, 622-628. doi: 10.1016/j.pbi.2003.09.014
19. Escobar, N. M., Haupt, S., Thow, G., Boevink, P., Chapman, S., and Oparka, K. (2003). High-throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell. 15, 1507-1523. doi: 10.1105/tpc.013284
20. Eubel, H., Meyer, E. H., Taylor, N. L., Bussell, J. D., O'Toole, N., Heazlewood, J. L., et al. (2008). Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol. 148, 1809-1829. doi: 10.1104/pp.108.129999
21. Ferro, M., Brugiere, S., Salvi, D., Seigneurin-Berny, D., Court, M., Moyet, L., et al. (2010). AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell Proteome. 9, 1063-1084. doi: 10.1074/mcp.M900325-MCP200
22. Fricker, M., Runions, J., and Moore, I. (2006). Quantitative fluorescence microscopy: from art to science. Annu. Rev. Plant Biol. 57, 79-107. doi: 10.1146/annurev.arplant.57.032905.105239
23. Friso, G., Giacomelli, L., Ytterberg, A. J., Peltier, J. B., Rudella, A., Sun, Q., et al. (2004). In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16, 478-499. doi: 10.1105/tpc.017814
24. Froehlich, J. E., Wilkerson, C. G., Ray, W. K., McAndrew, R. S., Osteryoung, K. W., Gage, D. A., et al. (2003). Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J. Proteome. Res. 2, 413-425. doi: 10.1021/pr034025j
25. Gao, H., Kadirjan-Kalbach, D., Froehlich, J. E., and Osteryoung, K. W. (2003). ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc. Natl. Acad. Sci. U.S.A. 100, 4328-4333. doi: 10.1073/pnas.0530206100
26. Gardiner, J. C., Taylor, N. G., and Turner, S. R. (2003). Control of cellulose synthase complex localization in developing xylem. Plant Cell 15, 1740-1748. doi: 10.1105/tpc.012815
27. Giacomelli, L., Rudella, A., and Van Wijk, K. J. (2006). High light response of the thylakoid proteome in arabidopsis wild type and the ascorbate-deficient mutant vtc2-2. A comparative proteomics study. Plant Physiol. 141, 685-701. doi: 10.1104/pp.106.080150
28. Granlund, I., Kieselbach, T., Alm, R., Schroder, W. P., and Emanuelsson, C. (2011). Clustering of MS spectra for improved protein identification rate and screening for protein variants and modifications by MALDI-MS/MS. J. Proteom. 74, 1190-1200. doi: 10.1016/j.jprot.2011.04.008
29. Hammani, K., Gobert, A., Hleibieh, K., Choulier, L., Small, I., and Giege, P. (2011). An Arabidopsis dual-localized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation. Plant Cell 23, 730-740. doi: 10.1105/tpc.110.081638
30. Hanson, M. R., and Kohler, R. H. (2001). GFP imaging: methodology and application to investigate cellular compartmentation in plants. J. Exp. Bot. 52, 529-539. doi: 10.1093/jexbot/52.356.529
31. Haseloff, J., Siemering, K. R., Prasher, D. C., and Hodge, S. (1997). Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. U.S.A. 94, 2122-2127. doi: 10.1073/pnas.94.6.2122
32. Heazlewood, J. L., Tonti-Filippini, J., Verboom, R. E., and Millar, A. H. (2005). Combining experimental and predicted datasets for determination of the subcellular location of proteins in Arabidopsis. Plant Physiol. 139, 598-609. doi: 10.1104/pp.105.065532
33. Heazlewood, J. L., Verboom, R. E., Tonti-Filippini, J., Small, I., and Millar, A. H. (2007). SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Res. 35, D213-D218. doi: 10.1093/nar/gkl863
34. Hjelmstad, R. H., and Bell, R. M. (1990). The sn-1, 2-diacylglycerol cholinephosphotransferase of Saccharomyces cerevisiae. Nucleotide sequence, transcriptional mapping, and gene product analysis of the CPT1 gene. J. Biol. Chem. 265, 1755-1764.
35. Hooks, K. B., Turner, J. E., Graham, I. A., Runions, J., and Hooks, M. A. (2012). GFP-tagging of Arabidopsis acyl-activating enzymes raises the issue of peroxisome-chloroplast import competition versus dual localization. J. Plant Physiol. 169, 1631-1638. doi: 10.1016/j.jplph.2012.05.026
36. Horton, P., Park, K. J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C. J., et al. (2007). WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585-W587. doi: 10.1093/nar/gkm259
37. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., et al. (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691. doi: 10.1038/nature02026
38. Ito, J., Batth, T. S., Petzold, C. J., Redding-Johanson, A. M., Mukhopadhyay, A., Verboom, R., et al. (2011). Analysis of the Arabidopsis cytosolic proteome highlights subcellular partitioning of central plant metabolism. J. Proteome Res. 10, 1571-1582. doi: 10.1021/pr1009433
39. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., et al. (2007). A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell Proteom. 6, 394-412. doi: 10.1074/mcp.M600250-MCP200
40. Kim, J. Y., Yuan, Z., and Jackson, D. (2003). Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130, 4351-4362. doi: 10.1242/dev.00618
41. Kleffmann, T., Russenberger, D., Von Zychlinski, A., Christopher, W., Sjolander, K., Gruissem, W., et al. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14, 354-362. doi: 10.1016/j.cub.2004.02.039
42. Klodmann, J., Senkler, M., Rode, C., and Braun, H. P. (2011). Defining the protein complex proteome of plant mitochondria. Plant Physiol. 157, 587-598. doi: 10.1104/pp.111.182352
43. Koroleva, O. A., Tomlinson, M. L., Leader, D., Shaw, P., and Doonan, J. H. (2005). High-throughput protein localization in Arabidopsis using Agrobacterium-mediated transient expression of GFP-ORF fusions. Plant J. 41, 162-174. doi: 10.1111/j.1365-313X.2004.02281.x
44. Lazarowitz, S. G., and Beachy, R. N. (1999). Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11, 535-548.
45. Lee, C. P., Eubel, H., O'Toole, N., and Millar, A. H. (2011). Combining proteomics of root and shoot mitochondria and transcript analysis to define constitutive and variable components in plant mitochondria. Phytochemistry 72, 1092-1108. doi: 10.1016/j.phytochem.2010.12.004
46. Lundquist, P. K., Poliakov, A., Bhuiyan, N. H., Zybailov, B., Sun, Q., and Van Wijk, K. J. (2012). The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol. 158, 1172-1192. doi: 10.1104/pp.111.193144
47. Lurin, C., Andres, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyere, C., et al. (2004). Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089-2103. doi: 10.1105/tpc.104.022236
48. Mano, S., Nakamori, C., Kondo, M., Hayashi, M., and Nishimura, M. (2004). An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J. 38, 487-498. doi: 10.1111/j.1365-313X.2004.02063.x
49. Marion, J., Bach, L., Bellec, Y., Meyer, C., Gissot, L., and Faure, J. D. (2008). Systematic analysis of protein subcellular localization and interaction using high-throughput transient transformation of Arabidopsis seedlings. Plant J. 56, 169-179. doi: 10.1111/j.1365-313X.2008.03596.x
50. Meyer, E. H., Taylor, N. L., and Millar, A. H. (2008). Resolving and identifying protein components of plant mitochondrial respiratory complexes using three dimensions of gel electrophoresis. J. Proteome Res. 7, 786-794. doi: 10.1021/pr700595p
51. Miao, Y., and Jiang, L. (2007). Transient expression of fluorescent fusion proteins in protoplasts of suspension cultured cells. Nat. Protoc. 2, 2348-2353. doi: 10.1038/nprot.2007.360
52. Michalecka, A. M., Svensson, A. S., Johansson, F. I., Agius, S. C., Johanson, U., Brennicke, A., et al. (2003). Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol. 133, 642-652. doi: 10.1104/pp.103.024208
53. Millar, A. H., Carrie, C., Pogson, B., and Whelan, J. (2009). Exploring the function-location nexus: using multiple lines of evidence in defining the subcellular location of plant proteins. Plant Cell 21, 1625-1631. doi: 10.1105/tpc.109.066019
54. Mireau, H., Lancelin, D., and Small, I. D. (1996). The same Arabidopsis gene encodes both cytosolic and mitochondrial alanyl-tRNA synthetases. Plant Cell 8, 1027-1039.
55. Mitra, S. K., Walters, B. T., Clouse, S. D., and Goshe, M. B. (2009). An efficient organic solvent based extraction method for the proteomic analysis of Arabidopsis plasma membranes. J. Proteome Res. 8, 2752-2767. doi: 10.1021/pr801044y
56. Mitschke, J., Fuss, J., Blum, T., Hoglund, A., Reski, R., Kohlbacher, O., et al. (2009). Prediction of dual protein targeting to plant organelles. New Phytol. 183, 224-235. doi: 10.1111/j.1469-8137.2009.02832.x
57. Murcha, M. W., Elhafez, D., Lister, R., Tonti-Filippini, J., Baumgartner, M., Philippar, K., et al. (2007). Characterization of the preprotein and amino acid transporter gene family in Arabidopsis. Plant Physiol 143, 199-212. doi: 10.1104/pp.106.090688
58. Nelson, B. K., Cai, X., and Nebenfuhr, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136. doi: 10.1111/j.1365-313X.2007.03212.x
59. Olinares, P. D., Ponnala, L., and Van Wijk, K. J. (2010). Megadalton complexes in the chloroplast stroma of Arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry, and hierarchical clustering. Mol. Cell Proteom. 9, 1594-1615. doi: 10.1074/mcp.M000038-MCP201
60. Palmieri, F., Rieder, B., Ventrella, A., Blanco, E., Do, P. T., Nunes-Nesi, A., et al. (2009). Molecular identification and functional characterization of Arabidopsis thaliana mitochondrial and chloroplastic NAD+ carrier proteins. J. Biol. Chem. 284, 31249-31259. doi: 10.1074/jbc.M109.041830
61. Parry, M. A., Andralojc, P. J., Mitchell, R. A., Madgwick, P. J., and Keys, A. J. (2003). Manipulation of Rubisco: the amount, activity, function and regulation. J. Exp. Bot. 54, 1321-1333. doi: 10.1093/jxb/erg141
62. Peeters, N., and Small, I. (2001). Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta 1541, 54-63. doi: 10.1016/S0167-4889(01)00146-X
63. Peltier, J. B., Cai, Y., Sun, Q., Zabrouskov, V., Giacomelli, L., Rudella, A., et al. (2006). The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol. Cell Proteom. 5, 114-133. doi: 10.1074/mcp.M500180-MCP200
64. Peltier, J. B., Ytterberg, A. J., Sun, Q., and Van Wijk, K. J. (2004). New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J. Biol. Chem. 279, 49367-49383. doi: 10.1074/jbc.M406763200
65. Reumann, S. (2011). Toward a definition of the complete proteome of plant peroxisomes: where experimental proteomics must be complemented by bioinformatics. Proteomics 11, 1764-1779. doi: 10.1002/pmic.201000681
66. Reumann, S., Babujee, L., Ma, C., Wienkoop, S., Siemsen, T., Antonicelli, G. E., et al. (2007). Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19, 3170-3193. doi: 10.1105/tpc.107.050989
67. Reumann, S., Quan, S., Aung, K., Yang, P., Manandhar-Shrestha, K., Holbrook, D., et al. (2009). In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol. 150, 125-143. doi: 10.1104/pp.109.137703
68. Richly, E., and Leister, D. (2004). An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329, 11-16. doi: 10.1016/j.gene.2004.01.008
69. Rouwendal, G. J., Mendes, O., Wolbert, E. J., and Douwe De Boer, A. (1997). Enhanced expression in tobacco of the gene encoding green fluorescent protein by modification of its codon usage. Plant Mol. Biol. 33, 989-999. doi: 10.1023/A:1005740823703
70. Rudhe, C., Chew, O., Whelan, J., and Glaser, E. (2002). A novel in vitro system for simultaneous import of precursor proteins into mitochondria and chloroplasts. Plant J. 30, 213-220. doi: 10.1046/j.1365-313X.2002.01280.x
71. Rutschow, H., Ytterberg, A. J., Friso, G., Nilsson, R., and Van Wijk, K. J. (2008). Quantitative proteomics of a chloroplast SRP54 sorting mutant and its genetic interactions with CLPC1 in Arabidopsis. Plant Physiol. 148, 156-175. doi: 10.1104/pp.108.124545
72. Sedbrook, J. C., Carroll, K. L., Hung, K. F., Masson, P. H., and Somerville, C. R. (2002). The Arabidopsis SKU5 gene encodes an extracellular glycosyl phosphatidylinositol-anchored glycoprotein involved in directional root growth. Plant Cell 14, 1635-1648. doi: 10.1105/tpc.002360
73. Skalitzky, C. A., Martin, J. R., Harwood, J. H., Beirne, J. J., Adamczyk, B. J., Heck, G. R., et al. (2011). Plastids contain a second sec translocase system with essential functions. Plant Physiol. 155, 354-369. doi: 10.1104/pp.110.166546
74. Small, I., Wintz, H., Akashi, K., and Mireau, H. (1998). Two birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol. Biol. 38, 265-277. doi: 10.1023/A:1006081903354
75. Souciet, G., Menand, B., Ovesna, J., Cosset, A., Dietrich, A., and Wintz, H. (1999). Characterization of two bifunctional Arabdopsis thaliana genes coding for mitochondrial and cytosolic forms of valyl-tRNA synthetase and threonyl-tRNA synthetase by alternative use of two in-frame AUGs. Eur. J. Biochem. 266, 848-854. doi: 10.1046/j.1432-1327.1999.00922.x
76. Sun, X., Fu, T., Chen, N., Guo, J., Ma, J., Zou, M., et al. (2010). The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. Plant Physiol. 152, 1263-1273. doi: 10.1104/pp.109.150722
77. Tanz, S. K., Castleden, I., Hooper, C. M., Vacher, M., Small, I., and Millar, H. A. (2013). SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res. 41, D1185-D1191. doi: 10.1093/nar/gks1151
78. Tanz, S. K., and Small, I. (2011). In silico methods for identifying organellar and suborganellar targeting peptides in Arabidopsis chloroplast proteins and for predicting the topology of membrane proteins. Method Mol. Biol. 774, 243-280. doi: 10.1007/978-1-61779-234-2_16
79. Taylor, N. L., Heazlewood, J. L., and Millar, A. H. (2011). The Arabidopsis thaliana 2-D gel mitochondrial proteome: refining the value of reference maps for assessing protein abundance, contaminants and post-translational modifications. Proteomics 11, 1720-1733. doi: 10.1002/pmic.201000620
80. Tian, G. W., Mohanty, A., Chary, S. N., Li, S., Paap, B., Drakakaki, G., et al. (2004). High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 135, 25-38. doi: 10.1104/pp.104.040139
81. Tsuda, K., Qi, Y., Nguyen Le, V., Bethke, G., Tsuda, Y., Glazebrook, J., and Katagiri, F. (2012). An efficient Agrobacterium-mediated transient transformation of Arabidopsis. Plant J. 69, 713-719. doi: 10.1111/j.1365-313X.2011.04819.x
82. Ueki, S., and Citovsky, V. (2011). To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants. Mol. Plant 4, 782-793. doi: 10.1093/mp/ssr060
83. Yang, Y., Li, R., and Qi, M. (2000). In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J. 22, 543-551. doi: 10.1046/j.1365-313x.2000.00760.x
84. Yoo, S. D., Cho, Y. H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572. doi: 10.1038/nprot.2007.199
85. Yu, F., Liu, X., Alsheikh, M., Park, S., and Rodermel, S. (2008). Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell 20, 1786-1804. doi: 10.1105/tpc.107.054965
86. Zacharias, D. A., and Tsien, R. Y. (2006). Molecular biology and mutation of green fluorescent protein. Method Biochem. Anal. 47, 83-120.
87. Zhang, Z. J., and Peck, S. C. (2011). Simplified enrichment of plasma membrane proteins for proteomic analyses in Arabidopsis thaliana. Proteomics 11, 1780-1788. doi: 10.1002/pmic.201000648
88. Zhou, R., Benavente, L. M., Stepanova, A. N., and Alonso, J. M. (2011). A recombineering-based gene tagging system for Arabidopsis. Plant J. 66, 712-723. doi: 10.1111/j.1365-313X.2011.04524.x
89. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., et al. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3:e1994. doi: 10.1371/journal.pone.0001994