How protein targeting to primary plastids via the endomembrane system could have evolved? A new hypothesis based on phylogenetic studies

Biology Direct

Volumn 8, Issue 1, 2013, Pages

  Gagat, Przemysław ^a   Bodył, Andrzej ^a   Mackiewicz, Paweł ^a  

^a UNIVERSITY OF WROC AW   (Poland)

Author keywords

Endomembrane system; Endoplasmic reticulum; Endosymbiont; Golgi apparatus; Horizontal gene transfer; Phylogeny; Plastid; Plastid transit peptide; Primary endosymbiosis; Protein trafficking; Signal peptide

Indexed keywords

ARABIDOPSIS THALIANA; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; CYANOBACTERIA; EMBRYOPHYTA; EUKARYOTA; ORYZA SATIVA; TRACHEOPHYTA;

VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CHLAMYDOMONAS REINHARDTII; CLASSIFICATION; GENETICS; METABOLISM; PHYLOGENY; PLASTID; RICE;

ARABIDOPSIS; CHLAMYDOMONAS REINHARDTII; ORYZA SATIVA; PHYLOGENY; PLANT PROTEINS; PLASTIDS;

EID: 84880006074     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/1745-6150-8-18     Document Type: Article

References (215)

1. Douzery EJ, Snell EA, Bapteste E, Delsuc F, Philippe H. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?. Proc Natl Acad Sci USA 2004, 101:15386-15391. 10.1073/pnas.0403984101, 524432, 15494441.
2. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 2004, 21:809-818. 10.1093/molbev/msh075, 14963099.
3. Palmer JD. The symbiotic birth and spread of plastids: how many times and whodunit?. J Phycol 2003, 39:4-12.
4. Gould SB, Waller RF, McFadden GI. Plastid evolution. Annu Rev Plant Biol 2008, 59:491-517. 10.1146/annurev.arplant.59.032607.092915, 18315522.
5. Archibald JM. The puzzle of plastid evolution. Curr Biol 2009, 19:R81-R88. 10.1016/j.cub.2008.11.067, 19174147.
6. Keeling PJ. The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci 2010, 365:729-748. 10.1098/rstb.2009.0103, 2817223, 20124341.
7. Cavalier-Smith T, Lee JJ. Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J Protozool 1985, 32:376-379.
8. Cavalier-Smith T. Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium. Proc Biol Sci 2006, 273:1943-1952. 10.1098/rspb.2006.3531, 1634775, 16822756.
9. Bodył A, Mackiewicz P, Stiller JW. Early steps in plastid evolution: current ideas and controversies. BioEssays 2009, 31:1219-1232. 10.1002/bies.200900073, 19847819.
10. Gross J, Bhattacharya D. Mitochondrial and plastid evolution in eukaryotes: an outsiders' perspective. Nat Rev Genet 2009, 10:495-505.
11. Richly E, Leister D. An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 2004, 329:11-16.
12. van Wijk KJ. Plastid proteomics. Plant Physiol Biochem 2004, 42:963-977. 10.1016/j.plaphy.2004.10.015, 15707834.
13. Green BR. Chloroplast genomes of photosynthetic eukaryotes. Plant J 2011, 66:34-44. 10.1111/j.1365-313X.2011.04541.x, 21443621.
14. Martin W, Herrmann RG. Gene transfer from organelles to the nucleus: how much, what happens, and why?. Plant Physiol 1998, 118:9-17. 10.1104/pp.118.1.9, 1539188, 9733521.
15. Selosse M, Albert B, Godelle B. Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol Evol 2001, 16:135-141. 10.1016/S0169-5347(00)02084-X, 11179577.
16. Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 2004, 5:123-135.
17. Kleine T, Maier UG, Leister D. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 2009, 60:115-138. 10.1146/annurev.arplant.043008.092119, 19014347.
18. Bruce BD. The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochim Biophys Acta 2001, 1541:2-21. 10.1016/S0167-4889(01)00149-5, 11750659.
19. Patron NJ, Waller RF. Transit peptide diversity and divergence: a global analysis of plastid targeting signals. BioEssays 2007, 29:1048-1058. 10.1002/bies.20638, 17876808.
20. Inaba T, Schnell DJ. Protein trafficking to plastids: one theme, many variations. Biochem J 2008, 413:15-28. 10.1042/BJ20080490, 18537794.
21. Li HM, Chiu CC. Protein transport into chloroplasts. Annu Rev Plant Biol 2010, 61:157-180. 10.1146/annurev-arplant-042809-112222, 20192748.
22. Shi LX, Theg SM. The chloroplast protein import system: from algae to trees. Biochim Biophys Acta 1833, 2013:314-331.
23. Plöscher M, Granvogl B, Reisinger V, Eichacker LA. Identification of the N-termini of NADPH: protochlorophyllide oxidoreductase A and B from barley etioplasts (Hordeum vulgare L.). FEBS J 2009, 276:1074-1081. 10.1111/j.1742-4658.2008.06850.x, 19154351.
24. Samol I, Rossig C, Buhr F, Springer A, Pollmann S, Lahroussi A, von Wettstein D, Reinbothe C, Reinbothe S. The outer chloroplast envelope protein OEP16-1 for plastid import of NADPH:protochlorophyllide oxidoreductase A in Arabidopsis thaliana. Plant Cell Physiol 2011, 52:96-111. 10.1093/pcp/pcq177, 21098556.
25. Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N, et al. Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 2005, 7:1224-1231. 10.1038/ncb1330, 16284624.
26. Nanjo Y, Oka H, Ikarashi N, Kaneko K, Kitajima A, Mitsui T, Munoz FJ, Rodriguez-Lopez M, Baroja-Fernandez E, Pozueta-Romero J. Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-Golgi to the chloroplast through the secretory pathway. Plant Cell 2006, 18:2582-2592. 10.1105/tpc.105.039891, 1626603, 17028208.
27. Kaneko K, Yamada C, Yanagida A, Koshu T, Umezawa Y, Itoh K, Hori H, Mitsui T. Differential localizations and functions of rice nucleotide pyrophosphatase/phosphodiesterase isozymes 1 and 3. Plant Biotechnol 2011, 28:69-76.
28. Chen MH, Huang LF, Li HM, Chen YR, Yu SM. Signal peptide-dependent targeting of a rice alpha-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol 2004, 135:1367-1377. 10.1104/pp.104.042184, 519054, 15235120.
29. Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, Mitsui T. Involvement of alpha-amylase I-1 in starch degradation in rice chloroplasts. Plant Cell Physiol 2005, 46:858-869. 10.1093/pcp/pci091, 15821023.
30. Kitajima A, Asatsuma S, Okada H, Hamada Y, Kaneko K, Nanjo Y, Kawagoe Y, Toyooka K, Matsuoka K, Takeuchi M, et al. The rice alpha-amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids. Plant Cell 2009, 21:2844-2858. 10.1105/tpc.109.068288, 2768910, 19767453.
31. Buren S, Ortega-Villasante C, Blanco-Rivero A, Martinez-Bernardini A, Shutova T, Shevela D, Messinger J, Bako L, Villarejo A, Samuelsson G. Importance of post-translational modifications for functionality of a chloroplast-localized carbonic anhydrase (CAH1) in Arabidopsis thaliana. PLoS One 2011, 6:e21021. 10.1371/journal.pone.0021021, 3112209, 21695217.
32. Levitan A, Trebitsh T, Kiss V, Pereg Y, Dangoor I, Danon A. Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. Proc Natl Acad Sci USA 2005, 102:6225-6230. 10.1073/pnas.0500676102, 1087927, 15837918.
33. Bhattacharya D, Archibald JM, Weber AP, Reyes-Prieto A. How do endosymbionts become organelles? understanding early events in plastid evolution. BioEssays 2007, 29:1239-1246. 10.1002/bies.20671, 18027391.
34. John CR. Conserved amino acid sequence domains in alpha-amylases from plants, mammals, and bacteria. Biochem Biophys Res Commun 1985, 128:470-476. 10.1016/0006-291X(85)91702-4, 3921026.
35. MacGregor EA, Janecek S, Svensson B. Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim Biophys Acta 2001, 1546:1-20. 10.1016/S0167-4838(00)00302-2, 11257505.
36. Gupta R, Gigras P, Mohapatra H, Goswami VK, Chauhan B. Microbial α-amylases: a biotechnological perspective. Process Biochem 2003, 38:1599-1616.
37. Terashima M, Hayashi N, Thomas BR, Rodriguez RL, Katoh S. Kinetic parameters of two rice [alpha]-amylase isozymes for oligosaccharide degradation. Plant Sci 1996, 116:9-14.
38. Terashima M, Hosono M, Katoh S. Functional roles of protein domains on rice alpha-amylase activity. Appl Microbiol Biotechnol 1997, 47:364-367. 10.1007/s002530050941, 9163949.
39. Nanjo Y, Asatsuma S, Itoh K, Hori H, Mitsui T, Fujisawa Y. Posttranscriptional regulation of alpha-amylase II-4 expression by gibberellin in germinating rice seeds. Plant Physiol Biochem 2004, 42:477-484. 10.1016/j.plaphy.2004.04.005, 15246060.
40. Ziegler P. Partial purification and characterization of the major endoamylase of mature pea leaves. Plant Physiol 1988, 86:659-666. 10.1104/pp.86.3.659, 1054548, 16665966.
41. Okita TW, Preiss J. Starch degradation in spinach leaves: isolation and characterization of the amylases and R-enzyme of spinach leaves. Plant Physiol 1980, 66:870-876. 10.1104/pp.66.5.870, 440744, 16661544.
42. Li B, Servaites JC, Geiger DR. Characterization and subcellular localization of debranching enzyme and endoamylase from leaves of sugar beet. Plant Physiol 1992, 98:1277-1284. 10.1104/pp.98.4.1277, 1080345, 16668788.
43. Echeverria E, Boyer CD. Localization of starch biosynthetic and degradative enzymes in maize leaves. Am J Bot 1986, 73:167-171.
44. Levi C, Preiss J. Amylopectin degradation in pea chloroplast extracts. Plant Physiol 1978, 61:218-220. 10.1104/pp.61.2.218, 1091835, 16660263.
45. Kakefuda G, Duke SH, Hostak MS. Chloroplast and extrachloroplastic starch-degrading enzymes in Pisum sativum L. Planta 1986, 168:175-182.
46. Lin TP, Spilatro SR, Preiss J. Subcellular localization and characterization of amylases in Arabidopsis leaf. Plant Physiol 1988, 86:251-259. 10.1104/pp.86.1.251, 1054463, 16665876.
47. Terashima M, Kubo A, Suzawa M, Itoh Y, Katoh S. The roles of the N-linked carbohydrate chain of rice alpha-amylase in thermostability and enzyme kinetics. Eur J Biochem 1994, 226:249-254. 10.1111/j.1432-1033.1994.tb20048.x, 7957256.
48. Hummel E, Osterrieder A, Robinson DG, Hawes C. Inhibition of Golgi function causes plastid starch accumulation. J Exp Bot 2010, 61:2603-2614. 10.1093/jxb/erq091, 2882258, 20423939.
49. The WallProtDB database [http://www.polebio.scsv.ups-tlse.fr/WallProtDB/searchform.php].
50. Yu T-S, Zeeman SC, Thorneycroft D, Fulton DC, Dunstan H, Lue W-L, Hegemann B, Tung S-Y, Umemoto T, Chapple A, et al. α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 2005, 280:9773-9779. 10.1074/jbc.M413638200, 15637061.
51. Deschamps P, Haferkamp I, D'Hulst C, Neuhaus HE, Ball SG. The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci 2008, 13:574-582. 10.1016/j.tplants.2008.08.009, 18824400.
52. Deschamps P, Moreau H, Worden AZ, Dauvillee D, Ball SG. Early gene duplication within chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics 2008, 178:2373-2387. 10.1534/genetics.108.087205, 2323822, 18245855.
53. Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, Buleon A, Haebel S, Ritte G, Steup M, Falcon LI, et al. Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 2008, 25:536-548. 10.1093/molbev/msm280, 18093994.
54. Ball S, Colleoni C, Cenci U, Raj JN, Tirtiaux C. The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 2011, 62:1775-1801. 10.1093/jxb/erq411, 21220783.
55. Nagashima H, Nakamura S, Nisizawa K, Hori T. Enzymic synthesis of floridean starch in a red alga, Serraticardia maxima. Plant Cell Physiol 1971, 12:243-253.
56. Borowitzka MA. Plastid development and floridean starch grain formation during carposporogenesis in the coralline red alga Lithothrix aspergillum gray. Protoplasma 1978, 95:217-228.
57. Preiss J. Regulation of the biosynthesis and degradation of starch. Annu Rev Plant Physiol 1982, 33:431-454.
58. Kombrink E, Wöber G. Identification and subcellular localization of starch-metabolizing enzymes in the green alga Dunaliella marina. Planta 1980, 149:130-137.
59. Levi C, Gibbs M. Starch degradation in synchronously grown Chlamydomonas reinhardtii and characterization of the amylase. Plant Physiol 1984, 74:459-463. 10.1104/pp.74.3.459, 1066708, 16663444.
60. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB. Molecular evidence for the early colonization of land by fungi and plants. Science 2001, 293:1129-1133. 10.1126/science.1061457, 11498589.
61. Sanderson MJ. Molecular data from 27 proteins do not support a Precambrian origin of land plants. Am J Bot 2003, 90:954-956. 10.3732/ajb.90.6.954, 21659192.
62. Martin W. Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 2010, 365:847-855. 10.1098/rstb.2009.0252, 2817231, 20124349.
63. Andrykovich G, Marx I. Isolation of a new polysaccharide digesting bacterium from a salt marsh. Appl Microbiol Biotechnol 1988, 54:1061-1062.
64. Hopkinson BM, Roe KL, Barbeau KA. Heme uptake by Microscilla marina and evidence for heme uptake systems in the genomes of diverse marine bacteria. Appl Environ Microbiol 2008, 74:6263-6270. 10.1128/AEM.00964-08, 2570271, 18757577.
65. DeBoy RT, Mongodin EF, Fouts DE, Tailford LE, Khouri H, Emerson JB, Mohamoud Y, Watkins K, Henrissat B, Gilbert HJ, Nelson KE. Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicus. J Bacteriol 2008, 190:5455-5463. 10.1128/JB.01701-07, 2493263, 18556790.
66. Reichenbach H, Dworkin M. Studies on Stigmatella aurantiaca (Myxobacterales). J Gen Microbiol 1969, 58:3-14. 10.1099/00221287-58-1-3, 5365932.
67. Olczak M, Morawiecka B, Wa{ogonek}torek W. Plant purple acid phosphatases - genes, structures and biological function. Acta Biochim Pol 2003, 50:1245-1256.
68. Liao H, Wong FL, Phang TH, Cheung MY, Li WY, Shao G, Yan X, Lam HM. GmPAP3, a novel purple acid phosphatase-like gene in soybean induced by NaCl stress but not phosphorus deficiency. Gene 2003, 318:103-111.
69. Yeung SL, Cheng C, Lui TK, Tsang JS, Chan WT, Lim BL. Purple acid phosphatase-like sequences in prokaryotic genomes and the characterization of an atypical purple alkaline phosphatase from Burkholderia cenocepacia J2315. Gene 2009, 440:1-8. 10.1016/j.gene.2009.04.002, 19376213.
70. Vincent J, Averill B. An enzyme with a double identity: purple acid phosphatase and tartrate- resistant acid phosphatase. FASEB J 1990, 4:3009-3014.
71. Schenk G, Ge Y, Carrington LE, Wynne CJ, Searle IR, Carroll BJ, Hamilton S, de Jersey J. Binuclear metal centers in plant purple acid phosphatases: Fe-Mn in sweet potato and Fe-Zn in soybean. Arch Biochem Biophys 1999, 370:183-189. 10.1006/abbi.1999.1407, 10510276.
72. Klabunde T, Strater N, Frohlich R, Witzel H, Krebs B. Mechanism of Fe(III)-Zn(II) purple acid phosphatase based on crystal structures. J Mol Biol 1996, 259:737-748. 10.1006/jmbi.1996.0354, 8683579.
73. Olczak M, Ciuraszkiewicz J, Wójtowicz H, Maszczak D, Olczak T. Diphosphonucleotide phosphatase/phosphodiesterase (PPD1) from yellow lupin (Lupinus luteus L.) contains an iron-manganese center. FEBS Lett 2009, 583:3280-3284. 10.1016/j.febslet.2009.09.024, 19755125.
74. Olczak M, Olczak T. Diphosphonucleotide phosphatase/phosphodiesterase from yellow lupin (Lupinus luteus L.) belongs to a novel group of specific metallophosphatases. FEBS Lett 2002, 519:159-163. 10.1016/S0014-5793(02)02740-0, 12023036.
75. Olczak M, Olczak T. N-glycosylation sites of plant purple acid phosphatases important for protein expression and secretion in insect cells. Arch Biochem Biophys 2007, 461:247-254. 10.1016/j.abb.2007.02.005, 17367744.
76. Oddie GW, Schenk G, Angel NZ, Walsh N, Guddat LW, de Jersey J, Cassady AI, Hamilton SE, Hume DA. Structure, function, and regulation of tartrate-resistant acid phosphatase. Bone 2000, 27:575-584. 10.1016/S8756-3282(00)00368-9, 11062342.
77. Ullah AH, Cummins BJ. Aspergillus ficuum extracellular pH 6.0 optimum acid phosphatase: purification, N-terminal amino acid sequence, and biochemical characterization. Prep Biochem 1988, 18:37-65. 10.1080/00327488808062512, 3375203.
78. Veljanovski V, Vanderbeld B, Knowles VL, Snedden WA, Plaxton WC. Biochemical and molecular characterization of AtPAP26, a vacuolar purple acid phosphatase up-regulated in phosphate-deprived Arabidopsis suspension cells and seedlings. Plant Physiol 2006, 142:1282-1293. 10.1104/pp.106.087171, 1630754, 16963519.
79. Morita N, Nakazato H, Okuyama H, Kim Y, Thompson GA. Evidence for a glycosylinositolphospholipid-anchored alkaline phosphatase in the aquatic plant Spirodela oligorrhiza. Biochim Biophys Acta 1996, 1290:53-62. 10.1016/0304-4165(95)00185-9, 8645707.
80. Flanagan JU, Cassady AI, Schenk G, Guddat LW, Hume DA. Identification and molecular modeling of a novel, plant-like, human purple acid phosphatase. Gene 2006, 377:12-20.
81. Attard A, Gourgues M, Galiana E, Panabières F, Ponchet M, Keller H. Strategies of attack and defense in plant-oomycete interactions, accentuated for Phytophthora parasitica Dastur (syn. P. Nicotianae Breda de Haan). J Plant Physiol 2008, 165:83-94. 10.1016/j.jplph.2007.06.011, 17766006.
82. Sun G, Yang Z, Ishwar A, Huang J. Algal genes in the closest relatives of animals. Mol Biol Evol 2010, 27:2879-2889. 10.1093/molbev/msq175, 20627874.
83. Borderies G, Jamet E, Lafitte C, Rossignol M, Jauneau A, Boudart G, Monsarrat B, Esquerre-Tugaye MT, Boudet A, Pont-Lezica R. Proteomics of loosely bound cell wall proteins of Arabidopsis thaliana cell suspension cultures: a critical analysis. Electrophoresis 2003, 24:3421-3432. 10.1002/elps.200305608, 14595688.
84. Jamet E, Canut H, Boudart G, Pont-Lezica RF. Cell wall proteins: a new insight through proteomics. Trends Plant Sci 2006, 11:33-39. 10.1016/j.tplants.2005.11.006, 16356755.
85. Zhang Y, Giboulot A, Zivy M, Valot B, Jamet E, Albenne C. Combining various strategies to increase the coverage of the plant cell wall glycoproteome. Phytochemistry 2011, 72:1109-1123. 10.1016/j.phytochem.2010.10.019, 21109274.
86. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjölander K, Gruissem W, Baginsky S. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 2004, 14:354-362. 10.1016/j.cub.2004.02.039, 15028209.
87. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 2008, 3:e1994. 10.1371/journal.pone.0001994, 2291561, 18431481.
88. Supuran CT. Carbonic anhydrases - an overview. Curr Pharm Des 2008, 14:603-614. 10.2174/138161208783877884, 18336305.
89. Smith KS, Jakubzick C, Whittam TS, Ferry JG. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci USA 1999, 96:15184-15189. 10.1073/pnas.96.26.15184, 24794, 10611359.
90. Smith KS, Ferry JG. Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 2000, 24:335-366. 10.1111/j.1574-6976.2000.tb00546.x, 10978542.
91. Hewett-Emmett D, Tashian RE. Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. Mol Phylogenet Evol 1996, 5:50-77. 10.1006/mpev.1996.0006, 8673298.
92. Elleuche S, Poggeler S. Evolution of carbonic anhydrases in fungi. Curr Genet 2009, 55:211-222. 10.1007/s00294-009-0238-x, 19296112.
93. Carter CJ, Thornburg RW. Tobacco Nectarin III is a bifunctional enzyme with monodehydroascorbate reductase and carbonic anhydrase activities. Plant Mol Biol 2004, 54:415-425.
94. Hou WC, Liu JS, Chen HJ, Chen TE, Chang CF, Lin YH. Dioscorin, the major tuber storage protein of yam (Dioscore batatas Decne), with carbonic anhydrase and trypsin inhibitor activities. J Agric Food Chem 1999, 47:2168-2172. 10.1021/jf980738o, 10552514.
95. Hou WC, Liu JS, Chen HJ, Chen TE, Chang CF, Lin YH. Dioscorins from different Dioscorea species all exhibit both carbonic anhydrase and trypsin inhibitor activities. Bot Bull Acad Sinica 2000, 41:191-196.
96. Shewry PR. Tuber storage proteins. Ann Bot 2003, 91:755-769. 10.1093/aob/mcg084, 12730067.
97. Fukuzawa H, Fujiwara S, Yamamoto Y, Dionisio-Sese ML, Miyachi S. cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: regulation by environmental CO2 concentration. Proc Natl Acad Sci USA 1990, 87:4383-4387. 10.1073/pnas.87.11.4383, 54114, 2112252.
98. Fujiwara S, Fukuzawa H, Tachiki A, Miyachi S. Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 1990, 87:9779-9783. 10.1073/pnas.87.24.9779, 55257, 2124702.
99. Rawat M, Moroney JV. Partial characterization of a new isoenzyme of carbonic anhydrase isolated from Chlamydomonas reinhardtii. J Biol Chem 1991, 266:9719-9723.
100. Tachiki A, Fukuzawa H, Miyachi S. Characterization of carbonic anhydrase isozyme CA2, which is the CAH2 gene product, in Chlamydomonas reinhardtii. Biosci Biotechnol Biochem 1992, 56:794-798. 10.1271/bbb.56.794, 1368343.
101. Ishida S, Muto S, Miyachi S. Structural analysis of periplasmic carbonic anhydrase 1 of Chlamydomonas reinhardtii. Eur J Biochem 1993, 214:9-16. 10.1111/j.1432-1033.1993.tb17890.x, 8508810.
102. Satoh A, Iwasaki T, Odani S, Shiraiwa Y. Purification, characterization and cDNA cloning of soluble carbonic anhydrase from Chlorella sorokiniana grown under ordinary air. Planta 1998, 206:657-665. 10.1007/s004250050444, 9821693.
103. Fisher M, Gokhman I, Pick U, Zamir A. A salt-resistant plasma membrane carbonic anhydrase is induced by salt in Dunaliella salina. J Biol Chem 1996, 271:17718-17723. 10.1074/jbc.271.30.17718, 8663366.
104. Moroney JV, Bartlett SG, Samuelsson G. Carbonic anhydrases in plants and algae. Plant Cell Environ 2001, 24:141-153.
105. Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G. A novel alpha-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 1998, 17:1208-1216. 10.1093/emboj/17.5.1208, 1170469, 9482718.
106. Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D. Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ 2007, 30:617-629. 10.1111/j.1365-3040.2007.01651.x, 17407539.
107. Rowlett RS. Structure and catalytic mechanism of the beta-carbonic anhydrases. Biochim Biophys Acta 1804, 2009:362-373.
108. Wilkinson B, Gilbert HF. Protein disulfide isomerase. Biochim Biophys Acta 2004, 1699:35-44.
109. Gruber CW, Cemazar M, Heras B, Martin JL, Craik DJ. Protein disulfide isomerase: the structure of oxidative folding. Trends Biochem Sci 2006, 31:455-464. 10.1016/j.tibs.2006.06.001, 16815710.
110. Kozlov G, Määttänen P, Thomas DY, Gehring K. A structural overview of the PDI family of proteins. FEBS J 2010, 277:3924-3936. 10.1111/j.1742-4658.2010.07793.x, 20796029.
111. Gleiter S, Bardwell JC. Disulfide bond isomerization in prokaryotes. Biochim Biophys Acta 2008, 1783:530-534. 10.1016/j.bbamcr.2008.02.009, 2391271, 18342631.
112. Pelham HR. The retention signal for soluble proteins of the endoplasmic reticulum. Trends Biochem Sci 1990, 15:483-486. 10.1016/0968-0004(90)90303-S, 2077689.
113. Turano C, Coppari S, Altieri F, Ferraro A. Proteins of the PDI family: unpredicted non-ER locations and functions. J Cell Physiol 2002, 193:154-163. 10.1002/jcp.10172, 12384992.
114. Lu DP, Christopher DA. Immunolocalization of a protein disulfide isomerase to Arabidopsis thaliana chloroplasts and its association with starch biogenesis. Int J Plant Sci 2006, 167:1-9.
115. Lu DP, Christopher D. The effect of irradiance and redox-modifying reagents on the 52 kDa protein disulfide isomerase of Arabidopsis chloroplasts. Biol Plant 2008, 52:42-48.
116. Armbruster U, Hertle A, Makarenko E, Zuhlke J, Pribil M, Dietzmann A, Schliebner I, Aseeva E, Fenino E, Scharfenberg M, et al. Chloroplast proteins without cleavable transit peptides: rare exceptions or a major constituent of the chloroplast proteome?. Mol Plant 2009, 2:1325-1335. 10.1093/mp/ssp082, 19995733.
117. Ni T, Yue J, Sun G, Zou Y, Wen J, Huang J. Ancient gene transfer from algae to animals: mechanisms and evolutionary significance. BMC Evol Biol 2012, 12:83. 10.1186/1471-2148-12-83, 3494510, 22690978.
118. Yue J, Huang J. Algal genes in aplastidic eukaryotes are not necessarily derived from historical plastids. Mob Genet Elements 2012, 2:193-196. 10.4161/mge.21745, 3469431, 23087844.
119. Gross J, Bhattacharya D. Endosymbiont or host: who drove mitochondrial and plastid evolution?. Biol Direct 2011, 6:12. 10.1186/1745-6150-6-12, 3050876, 21333023.
120. Ertel F, Mirus O, Bredemeier R, Moslavac S, Becker T, Schleiff E. The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J Biol Chem 2005, 280:28281-28289. 10.1074/jbc.M503035200, 15951438.
121. Tu SL, Chen LJ, Smith MD, Su YS, Schnell DJ, Li HM. Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. Plant Cell 2004, 16:2078-2088. 10.1105/tpc.104.023952, 519199, 15258267.
122. Hsu SC, Patel R, Bedard J, Jarvis P, Inoue K. Two distinct Omp85 paralogs in the chloroplast outer envelope membrane are essential for embryogenesis in Arabidopsis thaliana. Plant Signal Behav 2008, 3:1134-1135. 10.4161/psb.3.12.7095, 2634479, 19704458.
123. Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, Maier UG. Protein targeting into secondary plastids. J Eukaryot Microbiol 2009, 56:9-15. 10.1111/j.1550-7408.2008.00370.x, 19335770.
124. Agrawal S, Striepen B. More membranes, more proteins: complex protein import mechanisms into secondary plastids. Protist 2010, 161:672-687. 10.1016/j.protis.2010.09.002, 3005297, 21036664.
125. Patron NJ, Waller RF, Archibald JM, Keeling PJ. Complex protein targeting to dinoflagellate plastids. J Mol Biol 2005, 348:1015-1024. 10.1016/j.jmb.2005.03.030, 15843030.
126. Durnford DG, Gray MW. Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryot Cell 2006, 5:2079-2091. 10.1128/EC.00222-06, 1694827, 16998072.
127. Weeden NF. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 1981, 17:133-139. 10.1007/BF01733906, 7265265.
128. Martin W, Schnarrenberger C. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 1997, 32:1-18. 10.1007/s002940050241, 9309164.
129. Martin W. Endosymbiosis and the origins of chloroplast-cytosol isoenzymes: revising the product-specificity corollary. Horizontal Gene Transfer 1998, 363-379. London: Chapman Hall, Syvanen M, Kado C.
130. Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG, McLeod R, Roberts CW. Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot Cell 2006, 5:1517-1531. 10.1128/EC.00106-06, 1563581, 16963634.
131. Brinkmann H, Martin W. Higher-plant chloroplast and cytosolic 3-phosphoglycerate kinases: a case of endosymbiotic gene replacement. Plant Mol Biol 1996, 30:65-75. 10.1007/BF00017803, 8616244.
132. Martin W, Mustafa AZ, Henze K, Schnarrenberger C. Higher-plant chloroplast and cytosolic fructose-1,6-bisphosphatase isoenzymes: origins via duplication rather than prokaryote-eukaryote divergence. Plant Mol Biol 1996, 32:485-491. 10.1007/BF00019100, 8980497.
133. Nowitzki U, Gelius-Dietrich G, Schwieger M, Henze K, Martin W. Chloroplast phosphoglycerate kinase from Euglena gracilis: endosymbiotic gene replacement going against the tide. Eur J Biochem 2004, 271:4123-4131. 10.1111/j.1432-1033.2004.04350.x, 15479241.
134. Tyra HM, Linka M, Weber AP, Bhattacharya D. Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 2007, 8:R212. 10.1186/gb-2007-8-10-r212, 2246286, 17919328.
135. Yang Y, Glynn JM, Olson BJ, Schmitz AJ, Osteryoung KW. Plastid division: across time and space. Curr Opin Plant Biol 2008, 11:577-584. 10.1016/j.pbi.2008.10.001, 18990608.
136. Jarvis P. Organellar proteomics: chloroplasts in the spotlight. Curr Biol 2004, 14:R317-R319. 10.1016/j.cub.2004.03.054, 15084303.
137. Cavalier-Smith T. Membrane heredity and early chloroplast evolution. Trends Plant Sci 2000, 5:174-182. 10.1016/S1360-1385(00)01598-3, 10740299.
138. Clemens DL, Horwitz MA. Uptake and intracellular fate of Francisella tularensis in human macrophages. Ann N Y Acad Sci 2007, 1105:160-186. 10.1196/annals.1409.001, 17435118.
139. Welin A, Lerm M. Inside or outside the phagosome? The controversy of the intracellular localization of Mycobacterium tuberculosis. Tuberculosis 2012, 92:113-120. 10.1016/j.tube.2011.09.009, 22033468.
140. Mashburn-Warren LM, Whiteley M. Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 2006, 61:839-846. 10.1111/j.1365-2958.2006.05272.x, 16879642.
141. Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 2010, 64:163-184. 10.1146/annurev.micro.091208.073413, 3525469, 20825345.
142. Wang Z, Xu C, Benning C. TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J 2012, 70:614-623. 10.1111/j.1365-313X.2012.04900.x, 22269056.
143. Andersson MX, Goksor M, Sandelius AS. Membrane contact sites: physical attachment between chloroplasts and endoplasmic reticulum revealed by optical manipulation. Plant Signal Behav 2007, 2:185-187. 10.4161/psb.2.3.3973, 2634053, 19704692.
144. Andersson MX, Goksör M, Sandelius AS. Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 2007, 282:1170-1174.
145. Shimojima M, Ohta H, Nakamura Y. Biosynthesis and Function of Chloroplast Lipids. Photosynthesis, Essential and Regulatory Functions 2009, 35-55. Dordrecht, The Netherlands: Springer, Wada H, Murata N.
146. Brown AP, Slabas AR, Rafferty JB. Fatty acid biosynthesis in plants - metabolic pathways, structure and organization. Photosynthesis, Essential and Regulatory Functions 2009, 11-34. Dordrecht, The Netherlands: Springer, Wada H, Murata N.
147. Benning C. Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 2009, 25:71-91. 10.1146/annurev.cellbio.042308.113414, 19572810.
148. Jouhet J, Dubots E, Maréchal E, Maryse A, Block MA. Lipid trafficking in plant photosynthetic cells. Photosynthesis, Essential and Regulatory Functions 2009, 349-372. Dordrecht, The Netherlands: Springer, Wada H, Murata N.
149. Goss R, Wilhelm C. Lipids in algae, lichens and mosses. Photosynthesis, Essential and Regulatory Functions 2009, 117-135. Dordrecht, The Netherlands: Springer, Wada H, Murata N.
150. Heinz E, Roughan PG. Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 1983, 72:273-279. 10.1104/pp.72.2.273, 1066223, 16662992.
151. Giroud C, Gerber A, Eichenberger W. Lipids of Chlamydomonas reinhardtii - analysis of molecular-species and intracellular site(s) of biosynthesis. Plant Cell Physiol 1988, 29:587-595.
152. Archibald JM. Endosymbiosis: double-take on plastid origins. Curr Biol 2006, 16:R690-R692. 10.1016/j.cub.2006.08.006, 16950094.
153. Nowack EC, Melkonian M, Glockner G. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 2008, 18:410-418. 10.1016/j.cub.2008.02.051, 18356055.
154. Marin B, Nowack EC, Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis. Protist 2005, 156:425-432. 10.1016/j.protis.2005.09.001, 16310747.
155. Nowack ECM, Vogel H, Groth M, Grossman AR, Melkonian M, Glöckner G. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol Biol Evol 2011, 28:407-422. 10.1093/molbev/msq209, 20702568.
156. Mackiewicz P, Bodył A. A hypothesis for import of the nuclear-encoded PsaE protein of Paulinella chromatophora (Cercozoa, Rhizaria) into its cyanobacterial endosymbionts/plastids via the endomembrane system. J Phycol 2010, 46:847-859.
157. Mackiewicz P, Bodył A, Gagat P. Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora. Theory Biosci 2012, 131:1-18. 10.1007/s12064-011-0147-7, 3334493, 22209953.
158. Mackiewicz P, Bodył A, Gagat P. Protein import into the photosynthetic organelles of Paulinella chromatophora and its implications for primary plastid endosymbiosis. Symbiosis 2012, 58:99-107. 10.1007/s13199-012-0202-2, 3589627, 23482692.
159. Nowack EC, Grossman AR. Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci USA 2012, 109:5340-5345. 10.1073/pnas.1118800109, 3325729, 22371600.
160. Marin B, Nowack EC, Glockner G, Melkonian M. The ancestor of the Paulinella chromatophore obtained a carboxysomal operon by horizontal gene transfer from a Nitrococcus-like gamma-proteobacterium. BMC Evol Biol 2007, 7:85. 10.1186/1471-2148-7-85, 1904183, 17550603.
161. Yoon HS, Nakayama T, Reyes-Prieto A, Andersen RA, Boo SM, Ishida K, Bhattacharya D. A single origin of the photosynthetic organelle in different Paulinella lineages. BMC Evol Biol 2009, 9:98. 10.1186/1471-2148-9-98, 2685391, 19439085.
162. Bodył A, Mackiewicz P, Gagat P. Organelle evolution: Paulinella breaks a paradigm. Curr Biol 2012, 22:R304-R306. 10.1016/j.cub.2012.03.020, 22575468.
163. Schleiff E, Eichacker LA, Eckart K, Becker T, Mirus O, Stahl T, Soll J. Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope. Protein Sci 2003, 12:748-759. 10.1110/ps.0237503, 2323836, 12649433.
164. Schleiff E, Soll J. Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 2005, 6:1023-1027. 10.1038/sj.embor.7400563, 1371041, 16264426.
165. Hsu SC, Inoue K. Two evolutionarily conserved essential beta-barrel proteins in the chloroplast outer envelope membrane. Biosci Trends 2009, 3:168-178.
166. Inoue K. The chloroplast outer envelope membrane: the edge of light and excitement. J Integr Plant Biol 2007, 49:1100-1111.
167. Bodył A, Mackiewicz P, Stiller JW. Comparative genomic studies suggest that the cyanobacterial endosymbionts of the amoeba Paulinella chromatophora possess an import apparatus for nuclear-encoded proteins. Plant Biol 2010, 12:639-649.
168. GenBank database [http://www.ncbi.nlm.nih.gov/].
169. TbestDB database [http://tbestdb.bcm.umontreal.ca/searches/login.php].
170. Dragonblast database [http://dbdata.rutgers.edu/dragon/].
171. DOE Joint Genome Institute database [http://www.jgi.doe.gov].
172. Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, et al. CDD: a conserved domain database for protein classification. Nucleic Acids Res 2005, 33:D192-D196. 10.1093/nar/gni191, 540023, 15608175.
173. Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 2008, 9:286-298. 10.1093/bib/bbn013, 18372315.
174. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189-1191. 10.1093/bioinformatics/btp033, 2672624, 19151095.
175. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56:564-577. 10.1080/10635150701472164, 17654362.
176. Lartillot N, Philippe H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 2004, 21:1095-1109. 10.1093/molbev/msh112, 15014145.
177. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704. 10.1080/10635150390235520, 14530136.
178. Jobb G, von Haeseler A, Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 2004, 4:18. 10.1186/1471-2148-4-18, 459214, 15222900.
179. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263, 15647292.
180. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 2002, 18:298-305. 10.1093/bioinformatics/18.2.298, 11847077.
181. Small I, Peeters N, Legeai F, Lurin C. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 2004, 4:1581-1590. 10.1002/pmic.200300776, 15174128.
182. Petsalaki EI, Bagos PG, Litou ZI, Hamodrakas SJ. PredSL: a tool for the N-terminal sequence-based prediction of protein subcellular localization. Genomics Proteomics Bioinformatics 2006, 4:48-55. 10.1016/S1672-0229(06)60016-8, 16689702.
183. Boden M, Hawkins J. Prediction of subcellular localization using sequence-biased recurrent networks. Bioinformatics 2005, 21:2279-2286. 10.1093/bioinformatics/bti372, 15746276.
184. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300:1005-1016. 10.1006/jmbi.2000.3903, 10891285.
185. Lao DM, Shimizu T. A method for discriminating a signal peptide and a putative 1st transmembrane segment. Mathematics and Engineering Techniques in Medicine and Biological Sciences (METMBS'01); 25-28 June 2001 2001, 119-125. Las Vegas, Nevada: CSREA Press, Valafar H.
186. Gschloessl B, Guermeur Y, Cock JM. HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinforma 2008, 9:393.
187. Kall L, Krogh A, Sonnhammer EL. A combined transmembrane topology and signal peptide prediction method. J Mol Biol 2004, 338:1027-1036. 10.1016/j.jmb.2004.03.016, 15111065.
188. Hiller K, Grote A, Scheer M, Munch R, Jahn D. PrediSi: prediction of signal peptides and their cleavage positions. Nucleic Acids Res 2004, 32:W375-W379. 10.1093/nar/gkh378, 441516, 15215414.
189. ProtCompB - Prediction sub-cellular protein localization [http://linux1.softberry.com/berry.phtml?topic=protcompan&group=programs&subgroup=proloc].
190. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FS. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 2010, 26:1608-1615. 10.1093/bioinformatics/btq249, 2887053, 20472543.
191. Plewczynski D, Slabinski L, Tkacz A, Kajan L, Holm L, Ginalski K, Rychlewski L. The RPSP: web server for prediction of signal peptides. Polymer 2007, 48:5493-5496.
192. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet 2000, 16:276-277. 10.1016/S0168-9525(00)02024-2, 10827456.
193. Reczko M, Fiziev P, Staub E, Hatzigeorgiou A. Finding signal peptides in human protein sequences using recurrent neural networks. Algorithms in Bioinformatics 2002, 60-67. Berlin/Heidelberg: Springer, Guigó R, Gusfield D.
194. Shen HB, Chou KC. Signal-3L: a 3-layer approach for predicting signal peptides. Biochem Biophys Res Commun 2007, 363:297-303. 10.1016/j.bbrc.2007.08.140, 17880924.
195. Chou KC, Shen HB. Signal-CF: a subsite-coupled and window-fusing approach for predicting signal peptides. Biochem Biophys Res Commun 2007, 357:633-640. 10.1016/j.bbrc.2007.03.162, 17434148.
196. Nielsen H, Krogh A. Prediction of signal peptides and signal anchors by a hidden markov model. Proc Int Conf Intell Syst Mol Biol 1998, 6:122-130.
197. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: signalP 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028, 15223320.
198. SIG-Pred: Signal Peptide Prediction [http://bioinformatics.leeds.ac.uk/prot_analysis/Signal.html].
199. Gomi M, Sonoyama M, Mitaku S. High performance system for signal peptide prediction: SOSUIsignal. CBIJ 2004, 4:142-147.
200. The Arabidopsis Information Resource (TAIR) [http://www.arabidopsis.org/].
201. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I, Millar AH. SUBA: the Arabidopsis subcellular database. Nucleic Acids Res 2007, 35:D213-D218. 10.1093/nar/gkl863, 1635339, 17071959.
202. Nakabachi A, Shigenobu S, Sakazume N, Shiraki T, Hayashizaki Y, Carninci P, Ishikawa H, Kudo T, Fukatsu T. Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc Natl Acad Sci USA 2005, 102:5477-5482. 10.1073/pnas.0409034102, 555734, 15800043.
203. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 2000, 407:81-86.
204. Charles H, Balmand S, Lamelas A, Cottret L, Perez-Brocal V, Burdin B, Latorre A, Febvay G, Colella S, Calevro F, Rahbe Y. A genomic reappraisal of symbiotic function in the aphid/Buchnera symbiosis: reduced transporter sets and variable membrane organisations. PLoS One 2011, 6:e29096. 10.1371/journal.pone.0029096, 3246468, 22229056.
205. Jones JD, Thompson TE. Spontaneous phosphatidylcholine transfer by collision between vesicles at high lipid concentration. Biochemistry 1989, 28:129-134. 10.1021/bi00427a019, 2640559.
206. Lev S. Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat Rev Mol Cell Biol 2010, 11:739-750. 10.1038/nrm2971, 20823909.
207. Tokuda H. Biogenesis of outer membranes in Gram-negative bacteria. Biosci Biotechnol Biochem 2009, 73:465-473. 10.1271/bbb.80778, 19270402.
208. Tefsen B, Geurtsen J, Beckers F, Tommassen J, de Cock H. Lipopolysaccharide transport to the bacterial outer membrane in spheroplasts. J Biol Chem 2005, 280:4504-4509.
209. Chang G, Roth CB. Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science 2001, 293:1793-1800. 10.1126/science.293.5536.1793, 11546864.
210. Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CR. Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem 1998, 273:12466-12475. 10.1074/jbc.273.20.12466, 9575204.
211. Doerrler WT, Gibbons HS, Raetz CR. MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J Biol Chem 2004, 279:45102-45109. 10.1074/jbc.M408106200, 15304478.
212. Eckford PD, Sharom FJ. The reconstituted Escherichia coli MsbA protein displays lipid flippase activity. Biochem J 2010, 429:195-203. 10.1042/BJ20100144, 2888566, 20412049.
213. Kol MA, van Dalen A, de Kroon AI, de Kruijff B. Translocation of phospholipids is facilitated by a subset of membrane-spanning proteins of the bacterial cytoplasmic membrane. J Biol Chem 2003, 278:24586-24593. 10.1074/jbc.M301875200, 12714595.
214. Kol MA, van Laak AN, Rijkers DT, Killian JA, de Kroon AI, de Kruijff B. Phospholipid flop induced by transmembrane peptides in model membranes is modulated by lipid composition. Biochemistry 2003, 42:231-237. 10.1021/bi0268403, 12515559.
215. Malinverni JC, Silhavy TJ. An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc Natl Acad Sci USA 2009, 106:8009-8014. 10.1073/pnas.0903229106, 2683108, 19383799.