Abstract
ATP-binding cassette (ABC) proteins belong to a large family of proteins which mostly catalyze ATP-driven membrane translocation. They are found throughout the tree of life, from Archaea to Eukarya. In plants, they are known to perform essential functions in multiple subcellular compartments, though the locations of each ABC protein in a given species have not yet been defined. Here, we mine available proteomic, targeting, and fluorescence localization data to identify the subcellular location of each predicted ABC protein of Arabidopsis. Then we examine the functions of plastidic ABC proteins in detail. Transport functions are particularly important to the plastid, where a diverse group of substrates must be transported to allow specialized plastid metabolic functions to occur. Plastidic transporters that remain unidentified have been hypothesized based on known substrate translocation events. We attempt to narrow this gap by compiling available information about each plastidic ABC protein, including the primary literature, Chloroplast 2010 database information, transcriptomic data, coexpression analyses, and phylogenic data. This process ultimately allows us to make new hypotheses about the function of several plastidic ABC proteins and to identify a new family member of the AtABCI subfamily.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ajjawi I, Lu Y, Savage LJ, Bell SM, Last RL (2010) Large-scale reverse genetics in Arabidopsis: case studies from the Chloroplast 2010 Project. Plant Physiol 152(2):529–540. doi:10.1104/pp. 109.148494
Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216(5):841–853. doi:10.1007/s00425-002-0937-8
Andersson M (2013) Chloroplast contact to the endoplasmic reticulum and lipid trafficking. In: Biswal B, Krupinska K, Biswal UC (eds) Plastid development in leaves during growth and senescence, vol 36, Advances in photosynthesis and respiration. Springer, Netherlands, pp 155–167. doi:10.1007/978-94-007-5724-0_8
Arabidopsis Genome I (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815. doi:10.1038/35048692
Awai K, Xu C, Tamot B, Benning C (2006) A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc Natl Acad Sci U S A 103:10817–10822
Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151(4):2006–2017. doi:10.1104/pp. 109.147462
Badri DV, Chaparro JM, Manter DK, Martinoia E, Vivanco JM (2012) Influence of ATP-binding cassette transporters in root exudation of phytoalexins, signals, and in disease resistance. Front Plant Sci 3:149. doi:10.3389/fpls.2012.00149
Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL (2006) Chewing the fat: beta-oxidation in signalling and development. Trends Plant Sci 11(3):124–132. doi:10.1016/j.tplants.2006.01.005
Balk J, Pilon M (2011) Ancient and essential: the assembly of iron-sulfur clusters in plants. Trends Plant Sci 16(4):218–226. doi:10.1016/j.tplants.2010.12.006
Bayer RG, Stael S, Csaszar E, Teige M (2011) Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11(7):1287–1299. doi:10.1002/pmic.201000495
Bernard DG, Cheng Y, Zhao Y, Balk J (2009) An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis. Plant Physiol 151(2):590–602. doi:10.1104/pp. 109.143651
Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu XW, Yephremov A, Samuels L (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52(3):485–498. doi:10.1111/j.1365-313X.2007.03252.x
Block M, Dubots E, Maréchal E (2013) Glycerolipid biosynthesis and chloroplast biogenesis. In: Biswal B, Krupinska K, Biswal UC (eds) Plastid development in leaves during growth and senescence, vol 36, Advances in photosynthesis and respiration. Springer, Netherlands, pp 131–154. doi:10.1007/978-94-007-5724-0_7
Bouige P, Laurent D, Piloyan L, Dassa E (2002) Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr Protein Pept Sci 3(5):541–559. doi:10.2174/1389203023380486
Brautigam A, Weber APM (2009) Proteomic analysis of the proplastid envelope membrane provides novel insights into small molecule and protein transport across proplastid membranes. Mol Plant 2(6):1247–1261. doi:10.1093/Mp/Ssp070
Breckels LM, Gatto L, Christoforou A, Groen AJ, Lilley KS, Trotter MWB (2013) The effect of organelle discovery upon sub-cellular protein localisation. J Proteom 88:129–140. doi:10.1016/j.jprot.2013.02.019
Chahal HK, Outten FW (2012) Separate FeS scaffold and carrier functions for SufB(2)C(2) and SufA during in vitro maturation of [2Fe2S] Fdx. J Inorgan Biochem 116:126–134. doi:10.1016/j.jinorgbio.2012.06.008
Chen S, Sanchez-Fernandez R, Lyver ER, Dancis A, Rea PA (2007) Functional characterization of AtATM1, AtATM2, and AtATM3, a subfamily of Arabidopsis half-molecule ATP-binding cassette transporters implicated in iron homeostasis. J Biol Chem 282(29):21561–21571. doi:10.1074/jbc.M702383200
Coleman JA, Quazi F, Molday RS (2013) Mammalian P4-ATPases and ABC transporters and their role in phospholipid transport. Biochimica et biophysica acta 1831(3):555–574. doi:10.1016/j.bbalip.2012.10.006
Couturier J, Touraine B, Briat JF, Gaymard F, Rouhier N (2013) The iron-sulfur cluster assembly machineries in plants: current knowledge and open questions. Front Plant Sci 4:259. doi:10.3389/fpls.2013.00259
Crouzet J, Trombik T, Fraysse AS, Boutry M (2006) Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett 580(4):1123–1130. doi:10.1016/j.febslet.2005.12.043
Davies P (2010) Regulatory factors in hormone action: level, location and signal transduction. In: Davies P (ed) Plant hormones. Springer, Netherlands, pp 16–35. doi:10.1007/978-1-4020-2686-7_2
Dean M, Annilo T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genom Hum G 6:123–142. doi:10.1146/annurev.genom.6.080604.162122
Dubots E, Botte C, Boudiere L, Yamaryo-Botte Y, Jouhet J, Marechal E, Block MA (2012) Role of phosphatidic acid in plant galactolipid synthesis. Biochimie 94(1):86–93. doi:10.1016/j.biochi.2011.03.012
Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, Garin J, Joyard J, Masselon C, Rolland N (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteom 9(6):1063–1084. doi:10.1074/mcp.M900325-MCP200
Garcia O, Bouige P, Forestier C, Dassa E (2004) Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343(1):249–265. doi:10.1016/j.jmb.2004.07.093
Giroud C, Gerber A, Eichenberger W (1988) Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol 29:587–595
Gray MW (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4(9):a011403. doi:10.1101/cshperspect.a011403
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-angstrom resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16(3):334–342. doi:10.1038/Nsmb.1559
Heinz E, Roughan G (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72:273–279
Higgins CF (1992) ABC transporters - from microorganisms to man. Annu Rev Cell Biol 8:67–113. doi:10.1146/annurev.cb.08.110192.000435
Higgins CF, Linton KJ (2003) ABC transporters: An introduction and overview. In: Holland IB, Susan PCC, Karl K, Christopher F. HigginsA2 - I. Barry Holland SPCCKK, Christopher FH (eds) ABC Proteins. Academic, London, pp xvii–xxiii. 10.1016/B978-012352551-2/50001-9
Hinnebusch AG (1997) Translational regulation of yeast GCN4 - a window on factors that control initiator-tRNA binding to the ribosome. J Biol Chem 272(35):21661–21664. doi:10.1074/jbc.272.35.21661
Hjorth E, Hadfi K, Zauner S, Maier UG (2005) Unique genetic compartmentalization of the SUF system in cryptophytes and characterization of a SufD mutant in Arabidopsis thaliana. FEBS Lett 579(5):1129–1135. doi:10.1016/j.febslet.2004.12.084
Holland IB (2011) ABC transporters, mechanisms and biology: an overview. Essays Biochem 50:1–17. doi:10.1042/Bse0500001
Hollenstein K, Dawson RJ, Locher KP (2007) Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17(4):412–418. doi:10.1016/j.sbi.2007.07.003
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747. doi:10.1155/2008/420747
Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21(2):655–667. doi:10.1105/tpc.108.064543
Huang CF, Yamaji N, Ma JF (2010) Knockout of a bacterial-type ATP-binding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis. Plant Physiol 153(4):1669–1677. doi:10.1104/pp. 110.155028
Ito H, Gray WM (2006) A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol 142(1):63–74. doi:10.1104/pp. 106.084533
Jaquinod M, Villiers F, Kieffer-Jaquinod S, Hugouvieux V, Bruley C, Garin J, Bourguignon J (2007) A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. MolCell Proteom 6(3):394–412
Joo SH, Chung HS, Raetz CR, Garrett TA (2012) Activity and crystal structure of Arabidopsis thaliana UDP-N-acetylglucosamine acyltransferase. Biochemistry 51(21):4322–4330. doi:10.1021/bi3002242
Joshi HJ, Hirsch-Hoffmann M, Baerenfaller K, Gruissem W, Baginsky S, Schmidt R, Schulze WX, Sun Q, van Wijk KJ, Egelhofer V, Wienkoop S, Weckwerth W, Bruley C, Rolland N, Toyoda T, Nakagami H, Jones AM, Briggs SP, Castleden I, Tanz SK, Millar AH, Heazlewood JL (2011) MASCP Gator: an aggregation portal for the visualization of Arabidopsis proteomics data. Plant Physiol 155(1):259–270. doi:10.1104/pp. 110.168195
Jouhet J, Marechal E, Block MA (2007) Glycerolipid transfer for the building of membranes in plant cells. Progr Lipid Res 46(1):37–55. doi:10.1016/j.plipres.2006.06.002
Kamimoto Y, Hamamoto M, Shitan N, Yazaki K (2009) Unusual expression of an Arabidopsis ATP-binding cassette transporter ABCC11. Plant Biotechnol 26 (2):261-265. doi:DOI 10.5511/plantbiotechnology.26.261
Kaneda M, Schuetz M, Lin BSP, Chanis C, Hamberger B, Western TL, Ehlting J, Samuels AL (2011) ABC transporters coordinately expressed during lignification of Arabidopsis stems include a set of ABCBs associated with auxin transport. J Exp Bot 62(6):2063–2077. doi:10.1093/Jxb/Erq416
Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. The Arabidopsis Book 9:e0153. doi:10.1199/tab.0153
Kato T, Tabata S, Sato S (2009) Analyses of expression and phenotypes of knockout lines for Arabidopsis ABCF subfamily members. Plant Biotechnol 26(4):409–414. doi:10.5511/plantbiotechnology.26.409
Katoh H, Hagino N, Grossman AR, Ogawa T (2001) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183(9):2779–2784. doi:10.1128/JB.183.9.2779-2784.2001
Kaundal R, Saini R, Zhao PX (2010) Combining machine learning and homology-based approaches to accurately predict subcellular localization in Arabidopsis. Plant Physiol 154(1):36–54. doi:10.1104/pp. 110.156851
Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc B 365(1541):729–748. doi:10.1098/rstb.2009.0103
Klein M, Geisler M, Suh SJ, Kolukisaoglu HU, Azevedo L, Plaza S, Curtis MD, Richter A, Weder B, Schulz B, Martinoia E (2004) Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility. Plant J 39(2):219–236. doi:10.1111/j.1365-313X.2004.02125.x
Kobae Y, Sekino T, Yoshioka H, Nakagawa T, Martinoia E, Maeshima M (2006) Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant and Cell Physiol 47(3):309–318. doi:10.1093/Pcp/Pcj001
Kougioumoutzi E, Cartolano M, Canales C, Dupre M, Bramsiepe J, Vlad D, Rast M, Dello Ioio R, Tattersall A, Schnittger A, Hay A, Tsiantis M (2013) SIMPLE LEAF3 encodes a ribosome-associated protein required for leaflet development in Cardamine hirsuta. Plant J 73(4):533–545. doi:10.1111/Tpj.12072
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948
Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225(6):1447–1458. doi:10.1007/s00425-006-0452-4
Layer G, Gaddam SA, Ayala-Castro CN, Choudens SO, Lascoux D, Fontecave M, Outten FW (2007) SufE transfers sulfur from SufS to SufB for iron-sulfur cluster assembly. J Biol Chem 282(18):13342–13350. doi:10.1074/jbc.M608555200
Li C, Guan Z, Liu D, Raetz CR (2011) Pathway for lipid A biosynthesis in Arabidopsis thaliana resembling that of Escherichia coli. Proc Natl Acad Sci U S A 108(28):11387–11392. doi:10.1073/pnas.1108840108
Liang X, Qin L, Liu P, Wang M, Ye H (2013) Genes for iron-sulfur cluster assembly are targets of abiotic stress in rice, Oryza sativa. Plant Cell Environ. doi:10.1111/pce.12198
Linton KJ, Higgins CF (1998) The Escherichia coli ATP-binding cassette (ABC) proteins. Mol Microbiol 28(1):5–13
Locher KP (2009) Review. Structure and mechanism of ATP-binding cassette transporters. Philos Trans R Soc Lond B, Biol Sci 364(1514):239–245. doi:10.1098/rstb.2008.0125
Lu B, Benning C (2009) A 25-amino acid sequence of the Arabidopsis TGD2 protein is sufficient for specific binding of phosphatidic acid. J Biol Chem 284(26):17420–17427
Lu YP, Li ZS, Drozdowicz YM, Hortensteiner S, Martinoia E, Rea PA (1998) AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell 10(2):267–282. doi:10.1105/Tpc.10.2.267
Lu B, Xu C, Awai K, Jones AD, Benning C (2007) A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J Biol Chem 282:35945–35953
Malinverni JC, Silhavy TJ (2009) An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. Proc Natl Acad Sci USA 106(19):8009–8014. doi:10.1073/pnas.0903229106
Marin E, Divol F, Bechtold N, Vavasseur A, Nussaurne L, Forestier C (2006) Molecular characterization of three Arabidopsis soluble ABC proteins which expression is induced by sugars. Plant Sci 171(1):84–90. doi:10.1016/j.plantsci.2006.02.014
Marton MJ, deAldana CRV, Qiu HF, Chakraburtty K, Hinnebusch AG (1997) Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2 alpha kinase GCN2. Mol Cell Biol 17(8):4474–4489
Mentewab A, Stewart CN Jr (2005) Overexpression of an Arabidopsis thaliana ABC transporter confers kanamycin resistance to transgenic plants. Nat Biotechnol 23(9):1177–1180. doi:10.1038/nbt1134
Moller SG, Kunkel T, Chua NH (2001) A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes Dev 15(1):90–103
Nachin L, Loiseau L, Expert D, Barras F (2003) SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress. EMBO J 22(3):427–437. doi:10.1093/emboj/cdg061
Nagane T, Tanaka A, Tanaka R (2010) Involvement of AtNAP1 in the regulation of chlorophyll degradation in Arabidopsis thaliana. Planta 231(4):939–949. doi:10.1007/s00425-010-1099-8
Neubauer O, Alfandega A, Schoknecht J, Sternberg U, Pohlmann A, Eitinger T (2009) Two essential arginine residues in the T components of energy-coupling factor transporters. J Bacteriol 191(21):6482–6488. doi:10.1128/JB.00965-09
Obayashi T, Kinoshita K (2009) Rank of correlation coefficient as a comparable measure for biological significance of gene coexpression. DNA Res 16(5):249–260. doi:10.1093/dnares/dsp016
Pang KY, Li YJ, Liu MH, Meng ZD, Yu YL (2013) Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 526(2):411–428. doi:10.1016/j.gene.2013.05.051
Pighin JA, Zheng HQ, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306(5696):702–704. doi:10.1126/science.1102331
Puig S, Penarrubia L (2009) Placing metal micronutrients in context: transport and distribution in plants. Curr Opin Plant Biol 12(3):299–306. doi:10.1016/j.pbi.2009.04.008
Rayapuram N, Hagenmuller J, Grienenberger JM, Giege P, Bonnard G (2007) AtCCMA interacts with AtCcmB to form a novel mitochondrial ABC transporter involved in cytochrome c maturation in Arabidopsis. J Biol Chem 282(29):21015–21023. doi:10.1074/jbc.M704091200
Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10(3):218–227. doi:10.1038/nrm2646
Reyes-Prieto A, Weber AP, Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41:147–168. doi:10.1146/annurev.genet.41.110306.130134
Rodionov DA, Hebbeln P, Eudes A, ter Beek J, Rodionova IA, Erkens GB, Slotboom DJ, Gelfand MS, Osterman AL, Hanson AD, Eitinger T (2009) A novel class of modular transporters for vitamins in prokaryotes. J Bacteriol 191(1):42–51. doi:10.1128/JB.01208-08
Rolland N, Curien G, Finazzi G, Kuntz M, Marechal E, Matringe M, Ravanel S, Seigneurin-Berny D (2012) The biosynthetic capacities of the plastids and integration between cytoplasmic and chloroplast processes. Annu Rev Genet 46:233–264. doi:10.1146/annurev-genet-110410-132544
Roston R, Gao J, Xu C, Benning C (2011) Arabidopsis chloroplast lipid transport protein TGD2 disrupts membranes and is part of a large complex. Plant J 66(5):759–769. doi:10.1111/j.1365-313X.2011.04536.x
Roston RL, Gao JP, Murcha MW, Whelan J, Benning C (2012) TGD1,-2, and-3 proteins involved in lipid trafficking form ATP-binding cassette (ABC) transporter with multiple substrate-binding proteins. J Biol Chem 287(25):21406–21415. doi:10.1074/jbc.M112.370213
Saini A, Mapolelo DT, Chahal HK, Johnson MK, Outten FW (2010) SufD and SufC ATPase activity are required for iron acquisition during in vivo Fe-S cluster formation on SufB. Biochemistry 49(43):9402–9412. doi:10.1021/bi1011546
Sanchez-Fernandez R, Davies TGE, Coleman JOD, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276(32):30231–30244. doi:10.1074/jbc.M103104200
Sandberg G, Gardestrom P, Sitbon F, Olsson O (1990) Presence of indole-3-acetic-acid in chloroplasts of Nicotiana-Tabacum and Pinus-Sylvestris. Planta 180(4):562–568. doi:10.1007/Bf02411455
Saurin W, Hofnung M, Dassa E (1999) Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J Mol Evol 48(1):22–41. doi:10.1007/Pl00006442
Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281(5):2882–2892. doi:10.1074/jbc.M508333200
Shimoni-Shor E, Hassidim M, Yuval-Naeh N, Keren N (2010) Disruption of Nap14, a plastid-localized non-intrinsic ABC protein in Arabidopsis thaliana results in the over-accumulation of transition metals and in aberrant chloroplast structures. Plant Cell Environ 33(6):1029–1038. doi:10.1111/j.1365-3040.2010.02124.x
Shingles R, North M, McCarty RE (2002) Ferrous ion transport across chloroplast inner envelope membranes. Plant Physiol 128(3):1022–1030. doi:10.1104/pp. 010858
Simm S, Papasotiriou DG, Ibrahim M, Leisegang MS, Muller B, Schorge T, Karas M, Mirus O, Sommer MS, Schleiff E (2013) Defining the core proteome of the chloroplast envelope membranes. Front Plant Sci 4:11. doi:10.3389/fpls.2013.00011
Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18(3):731–746. doi:10.1105/tpc.105.038372
Stevanovic M, Hahn A, Nicolaisen K, Mirus O, Schleiff E (2012) The components of the putative iron transport system in the cyanobacterium Anabaena sp. PCC 7120. Environ Microbiol 14(7):1655–1670. doi:10.1111/j.1462-2920.2011.02619.x
Sudre D (2009) Identification of membrane proteins involved in heavy metal detoxification and transport in Arabidopsis thaliana. Diss Univ Zèurich, 2009 - Ref Enrico Martinoia, Zèurich
Sun Q, Zybailov B, Majeran W, Friso G, Olinares PDB, van Wijk KJ (2009) PPDB, the plant proteomics database at Cornell. Nucl Acids Res 37:D969–D974. doi:10.1093/Nar/Gkn654
Tameshige T, Fujita H, Watanabe K, Toyokura K, Kondo M, Tatematsu K, Matsumoto N, Tsugeki R, Kawaguchi M, Nishimura M, Okada K (2013) Pattern dynamics in adaxial-abaxial specific gene expression are modulated by a plastid retrograde signal during Arabidopsis thaliana leaf development. Plos Genet 9(7):e1003655. doi:10.1371/journal.pgen.1003655
Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, Millar HA (2013) SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res 41(Database issue):D1185–D1191. doi:10.1093/nar/gks1151
Tyra HM, Linka M, Weber AP, Bhattacharya D (2007) Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8(10):R212. doi:10.1186/Gb-2007-8-10-R212
Tyzack JK, Wang XM, Belsham GJ, Proud CG (2000) ABC50 interacts with eukaryotic initiation factor 2 and associates with the ribosome in an ATP-dependent manner. J Biol Chem 275(44):34131–34139. doi:10.1074/jbc.M002868200
van den Brule S, Smart CC (2002) The plant PDR family of ABC transporters. Planta 216(1):95–106. doi:10.1007/s00425-002-0889-z
van der Heide T, Poolman B (2002) ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep 3(10):938–943. doi:10.1093/embo-reports/kvt201
van Wijk KJ, Baginsky S (2011) Plastid proteomics in higher plants: current state and future goals. Plant Physiol 155(4):1578–1588. doi:10.1104/pp. 111.172932
Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins–a unified nomenclature and updated inventory. Trends Plant Sci 13(4):151–159. doi:10.1016/j.tplants.2008.02.001
Wang Z, Benning C (2012) Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochem Soc Trans 40:457–463. doi:10.1042/Bst20110752
Wanke D, Kolukisaoglu HU (2010) An update on the ABCC transporter family in plants: many genes, many proteins, but how many functions? Plant Biol 12:15–25. doi:10.1111/j.1438-8677.2010.00380.x
Weber APM, Linka N (2011) Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62:53–77. doi:10.1146/annurev-arplant-042110-103903
Wohlbach DJ, Quirino BF, Sussman MR (2008) Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20(4):1101–1117. doi:10.1105/tpc.107.055871
Wojas S, Hennig J, Plaza S, Geisler M, Siemianowski O, Sklodowska A, Ruszczynska A, Bulska E, Antosiewicz DM (2009) Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ Pollut 157(10):2781–2789. doi:10.1016/j.envpol.2009.04.024
Wollers S, Layer G, Garcia-Serres R, Signor L, Clemancey M, Latour JM, Fontecave M, Ollagnier de Choudens S (2010) Iron-sulfur (Fe-S) cluster assembly: the SufBCD complex is a new type of Fe-S scaffold with a flavin redox cofactor. J Biol Chem 285(30):23331–23341. doi:10.1074/jbc.M110.127449
Xin XF, Nomura K, Underwood W, He SY (2013) Induction and suppression of PEN3 focal accumulation during Pseudomonas syringae pv. tomato DC3000 infection of Arabidopsis. Mol Plant Microbe Interact 26(8):861–867. doi:10.1094/Mpmi-11-12-0262-R
Xing U, Jie QIU, Yang XU, Chen-wu XU (2012) Molecular evolution and expression analysis of subfamily ABCB transporter genes in rice. Chn J Rice Sci 26(2):127–136. doi:10.3969/j.issn.1001ª27216.2012.02.001
Xu XM, Moller SG (2004) AtNAP7 is a plastidic SufC-like ATP-binding cassette/ATPase essential for Arabidopsis embryogenesis. Proc Natl Acad Sci USA 101(24):9143–9148. doi:10.1073/pnas.0400799101
Xu C, Fan J, Riekhof W, Froehlich JE, Benning C (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J 22(10):2370–2379
Xu C, Fan J, Froehlich J, Awai K, Benning C (2005a) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17:3094–3110
Xu XM, Adams S, Chua NH, Moller SG (2005b) AtNAP1 represents an atypical SufB protein in Arabidopsis plastids. J Biol Chem 280(8):6648–6654. doi:10.1074/jbc.M413082200
Yang H, Murphy AS (2009) Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J 59(1):179–191. doi:10.1111/j.1365-313X.2009.03856.x
Yu HS, Hu SY, Zhu C (1989) Ultrastructure of sperm cells and the male germ unit in pollen tubes of Nicotiana-Tabacum. Protoplasma 152(1):29–36. doi:10.1007/Bf01354237
Zeng WQ, Brutus A, Kremer JM, Withers JC, Gao XL, Jones AD, He SY (2011) A genetic screen reveals Arabidopsis stomatal and/or apoplastic defenses against Pseudomonas syringae pv. tomato DC3000. Plos Pathog 7(10):e1002291
Acknowledgments
We apologize to any authors we did not cite, and we thank Que Kong for her expert translation of a relevant article. Funding on the TGD ABC transporters in the Benning lab is supported by a grant from the National Science Foundation, MCB1157231.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Roston, R.L., Hurlock, A.K., Benning, C. (2014). Plastidic ABC Proteins. In: Geisler, M. (eds) Plant ABC Transporters. Signaling and Communication in Plants, vol 22. Springer, Cham. https://doi.org/10.1007/978-3-319-06511-3_7
Download citation
DOI: https://doi.org/10.1007/978-3-319-06511-3_7
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-06510-6
Online ISBN: 978-3-319-06511-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)