Proteomic analysis of chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components

Plant Physiology

Volumn 160, Issue 2, 2012, Pages 708-725

  Barsan, Cristina ^a,b   Zouine, Mohamed ^a,b   Maza, Elie ^a,b   Bian, Wanping ^a,b   Egea, Isabel ^a,b   Rossignol, Michel ^c,d   Bouyssie, David ^d   Pichereaux, Carole ^c,d   Purgatto, Eduardo ^e   Bouzayen, Mondher ^a,b   Latché, Alain ^a,b   Pech, Jean Claude ^a,b  

^a Centre National de la Recherche Scientifique   (France)

^b CEMAGREF   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

LYCOPERSICON ESCULENTUM;

EID: 84867115856     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.203679     Document Type: Article

References (112)

1. Alba R, Fei Z, Payton P, Liu Y, Moore SL, Debbie P, Cohn J, D'Ascenzo M, Gordon JS, Rose JK, et al (2004) ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J 39: 697-714.
2. Aldridge C, Maple J, Møller SG (2005) The molecular biology of plastid division in higher plants. J Exp Bot 56: 1061-1077.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Andersson MX, Dörmann P (2009) Chloroplast membrane lipid biosynthesis and transport. In AS Sandelius, H Aronson, eds, The Chloroplast; Interactions with the Environment. Springer-Verlag, Berlin, pp 125-158.
5. Andon NL, Hollingworth S, Koller A, Greenland AJ, Yates JR III, Haynes PA (2002) Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics 2: 1156-1168.
6. Armbruster U, Pesaresi P, Pribil M, Hertle A, Leister D (2011) Update on chloroplast research: new tools, new topics, and new trends. Mol Plant 4: 1-16.
7. Asano T, Yoshioka Y, Kurei S, Sakamoto W, Machida Y, Sodmergen (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.
8. Baginsky S, Siddique A, Gruissem W (2004) Proteome analysis of tobacco bright yellow-2 (BY-2) cell culture plastids as a model for undifferentiated heterotrophic plastids. J Proteome Res 3: 1128-1137.
9. Balmer Y, Vensel WH, DuPont FM, Buchanan BB, Hurkman WJ (2006) Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. J Exp Bot 57: 1591-1602.
10. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18: 298-305.
11. Barry CS, Aldridge GM, Herzog G, Ma Q, McQuinn RP, Hirschberg J, Giovannoni JJ (2012) Altered chlorolast development and delayed fruit ripening caused by mutations in a zinc metalloprotease at the lutescent2 locus of tomato. Plant Physiol 159: 1086-1098.
12. Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, Zouine M, Latché A, Bouzayen M, Pech JC (2010) Characteristics of the tomato chromoplast revealed by proteomic analysis. J Exp Bot 61: 2413-2431.
13. Benjamini Y, Hachberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289-300.
14. Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25: 71-91.
15. Bian W, Barsan C, Egea I, Purgatto E, Chervin C, Zouine M, Latché A, Bouzayen M, Pech JC (June 3, 2011) Metabolic and molecular events occurring during chromoplast biogenesis: review article. J Bot http://dx.doi.org/10.1155/2011/289859.
16. Birtić S, Ginies C, Causse M, Renard CM, Page D (2009) Changes in volatiles and glycosides during fruit maturation of two contrasted tomato (Solanum lycopersicum) lines. J Agric Food Chem 57: 591-598.
17. Blanke MM, Lenz F (1989) Fruit photosynthesis. Plant Cell Environ 12: 31-46.
18. Booth JG, Eilertson KE, Olinares PD, Yu H (2011) A bayesian mixture model for comparative spectral count data in shotgun proteomics. Mol Cell Proteomics 10: M110. 007203.
19. Botella-Pavía P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A, Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40: 188-199.
20. Bouvier F, Camara B (2007) The role of plastids in ripening fruits. In RR Wise, JK Hoober, eds, The Structure and Functions of Plastids. Springer, Dordrecht, The Netherlands, pp 419-432.
21. Bouyssié D, Gonzalez de Peredo A, Mouton E, Albigot R, Roussel L, Ortega N, Cayrol C, Burlet-Schiltz O, Girard JP, Monsarrat B (2007) Mascot file parsing and quantification (MFPaQ), a new software to parse, validate, and quantify proteomics data generated by ICAT and SILAC mass spectrometric analyses: application to the proteomics study of membrane proteins from primary human endothelial cells. Mol Cell Proteomics 6: 1621-1637.
22. Bramley PM (2002) Regulation of carotenoid formation during tomato fruit ripening and development. J Exp Bot 53: 2107-2113.
23. Bräutigam A, Hoffmann-Benning S, Weber APM (2008) Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol 148: 568-579.
24. Cai W, Ma J, Chi W, Zou M, Guo J, Lu C, Zhang L (2010) Cooperation of LPA3 and LPA2 is essential for photosystem II assembly in Arabidopsis. Plant Physiol 154: 109-120.
25. Camara B, Hugueney P, Bouvier F, Kuntz M, Monéger R (1995) Biochemistry and molecular biology of chromoplast development. Int Rev Cytol 163: 175-247.
26. Chen G, Bi YR, Li N (2005) EGY1 encodes a membrane-associated and ATP-independent metalloprotease that is required for chloroplast development. Plant J 41: 364-375.
27. Chen G, Hackett R, Walker D, Taylor A, Lin Z, Grierson D (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 136: 2641-2651.
28. Cho MH, Jang A, Bhoo SH, Jeon JS, Hahn TR (2012) Manipulation of triose phosphate/phosphate translocator and cytosolic fructose-1,6-bisphosphatase, the key components in photosynthetic sucrose synthesis, enhances the source capacity of transgenic Arabidopsis plants. Photosynth Res 111: 261-268.
29. Deborde C, Maucourt M, Baldet P, Bernillon S, Biais B, Talon G, Ferrand C, Jacob D, Ferry Dumazet H, de Daruvar A, et al (2009) Proton NMR quantitative profiling for quality assessment of greenhouse-grown tomato fruit. Metabolomics 5: 183-198.
30. Delmar P, Robin S, Daudin JJ (2005a) VarMixt: efficient variance modelling for the differential analysis of replicated gene expression data. Bioinformatics 21: 502-508.
31. Delmar P, Robin S, Tronik-Le Roux D, Daudin JJ (2005b) Mixture model on the variance for differential analysis of gene abundance data. JR Stat Soc 54: 31-50.
32. Demartini DG, Jain R, Agrawal G, Thelen JJ (2011) A proteomic comparison of plastids from developing embryos and leaves of Brassica napus. J Prot Res 10: 2226-2237.
33. Dieterle F, Ross A, Schlotterbeck G, Senn H (2006) Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures: application in 1H NMR metabonomics. Anal Chem 78: 4281-4290.
34. Egea I, Barsan C, Bian W, Purgatto E, Latché A, Chervin C, Bouzayen M, Pech JC (2010) Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51: 1601-1611.
35. Egea I, Bian W, Barsan C, Jauneau A, Pech JC, Latché A, Li ZG, Chervin C (2011) Chloroplast to chromoplast transition in tomato fruit: spectral confocal microscopy analyses of carotenoids and chlorophylls in isolated plastids and time-lapse recording on intact live tissue. Ann Bot (Lond) 108: 291-297.
36. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
37. Emes MJ, Neuhaus HE (1997) Metabolism and transport in nonphotosynthetic plastids. J Exp Bot 48: 1995-2005.
38. Fan X, Mattheis JP, Fellman JK (1998) A role for jasmonates in climacteric fruit ripening. Planta 204: 444-449.
39. Faurobert M, Mihr C, Bertin N, Pawlowski T, Negroni L, Sommerer N, Causse M (2007) Major proteome variations associated with cherry tomato pericarp development and ripening. Plant Physiol 143: 1327-1346.
40. Ferro M, Brugière S, Salvi D, Seigneurin-Berny D, Court M, Moyet L,. Ramus C, Miras S, Mellal M, Le Gall S, et al (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9: 1063-1084.
41. Fischer K, Kammerer B, Gutensohn M, Arbinger B, Weber A, Häusler RE, Flügge UI (1997) A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 9: 453-462.
42. Harris WM, Spurr AR (1969) Chromoplasts of tomato fruit. II. The red tomato. Am J Bot 56: 380-389.
43. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16: 241-256.
44. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I, Millar AH (2007) SUBA: the Arabidopsis subcellular database. Nucleic Acids Res (Database issue) 35: D213-D218.
45. Hetherington SE, Smillie RM, Davies WJ (1998) Photosynthetic activities of vegetative and fruiting tissues of tomato. J Exp Bot 49: 1173-1181.
46. Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM (2006) The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugarsignaling mechanism in Arabidopsis. Plant Cell 18: 1226-1238.
47. Issaq HJ, Van QN, Waybright TJ, Muschik GM, Veenstra TD (2009) Analytical and statistical approaches to metabolomics research. J Sep Sci 32: 2183-2199.
48. Jebanathirajah JA, Coleman JR (1998) Association of carbonic anhydrase with a Calvin cycle enzyme complex in Nicotiana tabacum. Planta 204: 177-182.
49. Jeong SY, Rose A, Meier I (2003) MFP1 is a thylakoid-associated, nucleoidbinding protein with a coiled-coil structure. Nucleic Acids Res 31: 5175-5185.
50. Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002) Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214: 751-758.
51. Kahlau S, Bock R (2008) Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20: 856-874.
52. Kato BS, Nicholson G, Neiman M, Rantalainen M, Holmes CC, Barrett A, Uhlén M, Nilsson P, Spector TD, Schwenk JM (2011) Variance decomposition of protein profiles from antibody arrays using a longitudinal twin model. Proteome Sci 9: 73.
53. Kato Y, Kouso T, Sakamoto W (2012) Variegated tobacco leaves generated by chloroplast FtsH suppression: implication of FtsH function in the maintenance of thylakoid membranes. Plant Cell Physiol 53: 391-404.
54. Kleffmann T, Hirsch-Hoffmann M, Gruissem W, Baginsky S (2006) plprot: a comprehensive proteome database for different plastid types. Plant Cell Physiol 47: 432-436.
55. Krech K, Ruf S, Masduki FF, Thiele W, Bednarczyk D, Albus CA, Tiller N, Hasse C, Schöttler MA, Bock R (2012) The plastid genome-encoded Ycf4 protein functions as a nonessential assembly factor for photosystem I in higher plants. Plant Physiol 159: 579-591.
56. Lee U, Rioflorido I, Hong SW, Larkindale J, Waters ER, Vierling E (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J 49: 115-127.
57. Li L, Van Eck J (2007) Metabolic engineering of carotenoid accumulation by creating a metabolic sink. Transgenic Res 16: 581-585.
58. Li X, Henry R, Yuan J, Cline K, Hoffman NE (1995) A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc Natl Acad Sci USA 92: 3789-3793.
59. Liu D, Gong Q, Ma Y, Li P, Li J, Yang S, Yuan L, Yu Y, Pan D, Xu F, et al (2010a) cpSecA, a thylakoid protein translocase subunit, is essential for photosynthetic development in Arabidopsis. J Exp Bot 61: 1655-1669.
60. Liu H, Sadygov RG, Yates JR III (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76: 4193-4201.
61. Liu X, Yu F, Rodermel S (2010b) Arabidopsis chloroplast FtsH, var2 and suppressors of var2 leaf variegation: a review. J Integr Plant Biol 52: 750-761.
62. Ljubesić N, Wrischer M, Devidé Z (1991) Chromoplasts-the last stages in plastid development. Int J Dev Biol 35: 251-258.
63. Lopez-Juez E (2007) Plastid biogenesis, between shadow and light. J Exp Biol 58: 11-26.
64. Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ (2012) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol 158: 1172-1192.
65. Lytovchenko A, Eickmeier I, Pons C, Osorio S, Szecowka M, Lehmberg K, Arrivault S, Tohge T, Pineda B, Anton MT, et al (2011) Tomato fruit photosynthesis is seemingly unimportant in primary metabolism and ripening but plays a considerable role in seed development. Plant Physiol 157: 1650-1663.
66. Maple J, Chua NH, Møller SG (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J 31: 269-277.
67. Maple J, Møller SG (2007) Interdependency of formation and localisation of the Min complex controls symmetric plastid division. J Cell Sci 120: 3446-3456.
68. Marano MR, Serra EC, Orellano G, Carrillo N (1993) The path of homoplast development in fruits and flowers. Plant Sci 94: 1-17.
69. McAndrew RS, Olson BJ, Kadirjan-Kalbach DK, Chi-Ham CL, Vitha S, Froehlich JE, Osteryoung KW (2008) In vivo quantitative relationship between plastid division proteins FtsZ1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochem J 412: 367-378.
70. Millar AH, Whelan J, Small I (2006) Recent surprises in protein targeting to mitochondria and plastids. Curr Opin Plant Biol 9: 610-615.
71. Moing A, Aharoni A, Biais B, Rogachev I, Meir S, Brodsky L, Allwood JW, Erban A, Dunn WB, Kay L, et al (2011) Extensive metabolic crosstalk in melon fruit revealed by spatial and developmental combinatorial metabolomics. New Phytol 190: 683-696.
72. Neta-Sharir I, Isaacson T, Lurie S, Weiss D (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17: 1829-1838.
73. Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, Rosso MG, Ache P, Flügge UI, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17: 760-775.
74. Onishi T, Takahashi Y (2009) Effects of site-directed mutations in the chloroplast-encoded Ycf4 gene on PSI complex assembly in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol 50: 1750-1760.
75. Osorio S, Alba R, Damasceno CMB, Lopez-Casado G, Lohse M, Zanor MI, Tohge T, Usadel B, Rose JKC, Fei Z, et al (2011) Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157: 405-425.
76. Palma JM, Corpas FJ, del Río LA (2011) Proteomics as an approach to the understanding of the molecular physiology of fruit development and ripening. J Proteomics 74: 1230-1243.
77. Paoletti AC, Parmely TJ, Tomomori-Sato C, Sato S, Zhu D, Conaway RC, Conaway JW, Florens L, Washburn MP (2006) Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors. Proc Natl Acad Sci USA 103: 18928-18933.
78. Pech JC, Purgatto E, Bouzayen M, Latché A (2012) Ethylene and fruit ripening. In MT McManus, ed, Annual Plant Reviews, Vol 44. The Plant Hormone Ethylene. Wiley-Blackwell, Oxford, UK, pp 275-304.
79. Peng L, Ma J, Chi W, Guo J, Zhu S, Lu Q, Lu C, Zhang L (2006) LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 18: 955-969.
80. Pierleoni A, Martelli PL, Fariselli P, Casadio R (2007) eSLDB: eukaryotic subcellular localization database. Nucleic Acids Res (Database issue) 35: D208-D212.
81. Pirrello J, Regad F, Latché A, Pech JC, Bouzayen M (2009) Regulation of tomato fruit ripening. CAB Reviews 4: 1-14.
82. Plücken H, Müller B, Grohmann D, Westhoff P, Eichacker LA (2002) The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Lett 532: 85-90.
83. Ren G, An K, Liao Y, Zhou X, Cao Y, Zhao H, Ge X, Kuai B (2007) Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol 144: 1429-1441.
84. Richly E, 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.
85. Rocco M, D'Ambrosio C, Arena S, Faurobert M, Scaloni A, Marra M (2006) Proteomic analysis of tomato fruits from two ecotypes during ripening. Proteomics 6: 3781-3791.
86. Rutschow H, Ytterberg AJ, Friso G, Nilsson R, van Wijk KJ (2008) Quantitative proteomics of a chloroplast SRP54 sorting mutant and its genetic interactions with CLPC1 in Arabidopsis. Plant Physiol 148: 156-175.
87. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, et al (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24: 447-454.
88. Seigneurin-Berny D, Rolland N, Garin J, Joyard J (1999) Technical advance: differential extraction of hydrophobic proteins from chloroplast envelope membranes: a subcellular-specific proteomic approach to identify rare intrinsic membrane proteins. Plant J 19: 217-228.
89. Shipman-Roston RL, Ruppel NJ, Damoc C, Phinney BS, Inoue K (2010) The significance of protein maturation by plastidic type I signal peptidase 1 for thylakoid development in Arabidopsis chloroplasts. Plant Physiol 152: 1297-1308.
90. Siddique MA, Grossmann J, Gruissem W, Baginsky S (2006) Proteome analysis of bell pepper (Capsicum annuum L.) chromoplasts. Plant Cell Physiol 47: 1663-1673.
91. Simkin AJ, Gaffé J, Alcaraz JP, Carde JP, Bramley PM, Fraser PD, Kuntz M (2007) Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochemistry 68: 1545-1556.
92. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4: 1581-1590.
93. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
94. Spurr AR, Harris WM (1968) Ultrastructure of chloroplasts and chromoplasts in Capsicum annuum. I. Thylakoid membrane changes during fruit ripening. Am J Bot 55: 1210-1224.
95. Su PH, Li HM (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146: 1231-1241.
96. Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ (2009) PPDB, the Plant Proteomics Database at Cornell. Nucleic Acids Res (Database issue) 37: D969-D974.
97. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35: 259-270.
98. The Uniprot Consortium (2010) The universal protein resource (UniProt) in 2010. Nucleic Acids Res (Web Server issue) 38: D142-D148.
99. Thelen JJ, Peck SC (2007) Quantitative proteomics in plants: choices in abundance. Plant Cell 19: 3339-3346.
100. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939.
101. Thomson WW, Whatley JM (1980) Development of non-green plastids. Annu Rev Plant Physiol 31: 375-394.
102. Tiwari K, Paliyath G (2011) Microarray analysis of ripening-regulated gene expression and its modulation by 1-MCP and hexanal. Plant Physiol Biochem 49: 329-340.
103. Torgrip RJO, Aberg KM, Alm E, Schuppe-Koistinen I, Lindberg J (2008) A note on normalization of biofluid 1D 1H-NMR data. Metabolomics 4: 114-121.
104. van Wijk KJ, Baginsky S (2011) Plastid proteomics in higher plants: current state and future goals. Plant Physiol 155: 1578-1588.
105. Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15: 1918-1933.
106. von Zychlinski A, Kleffmann T, Krishnamurthy N, Sjölander K, Baginsky S, Gruissem W (2005) Proteome analysis of the rice etioplast: metabolic and regulatory networks and novel protein functions. Mol Cell Proteomics 4: 1072-1084.
107. Waters MT, Pyke KA (2004) Plastid development and differentiation. In SG Møller, ed, Plastids. Blackwell, Oxford, pp 30-59.
108. Yakir-Tamang L, Gerst JE (2009) A phosphatidylinositol-transfer protein and phosphatidylinositol-4-phosphate 5-kinase control Cdc42 to regulate the actin cytoskeleton and secretory pathway in yeast. Mol Biol Cell 20: 3583-3597.
109. Zeng Y, Pan Z, Ding Y, Zhu A, Cao H, Xu Q, Deng X (2011) A proteomic analysis of the chromoplasts isolated from sweet orange fruits [Citrus sinensis (L.) Osbeck]. J Exp Bot 62: 5297-5309.
110. Zhang M, Yuan B, Leng P (2009) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60: 1579-1588.
111. Zhu W, Smith JW, Huang CM (November 10, 2009) Mass-spectrometrybased label-free quantitative proteomics. J Biomed Biotech http://dx.doi.org/10.1155/2010/840518.
112. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3: e1994.