Plant ABC Transporters Enable Many Unique Aspects of a Terrestrial Plant's Lifestyle

Molecular Plant - Tập 9 Số 3 - Trang 338-355 - 2016
Jae‐Ung Hwang1, Won‐Yong Song2, Daewoong Hong1, Donghwi Ko1, Yasuyo Yamaoka1, Sunghoon Jang1, Sojeong Yim1, Eunjung Lee1, Deepa Khare1, Kyung Yoon Kim1, Michael Palmgren3, Hwan Su Yoon4, Enrico Martinoia5, Youngsook Lee1,2
1Department of Life Science, Pohang University of Science and Technology (POSTECH), Pohang, 37673, Korea
2Division of Integrative Bioscience and Biotechnology, POSTECH, Pohang, 37673, Korea
3Center for Membrane Pumps in Cells and Disease - PUMPKIN, Danish National Research Foundation, Department of Plant and Environmental Science, University of Copenhagen, 1871 Frederiksberg, Denmark
4Department of Biological Sciences, Sungkyunkwan University, Suwon 16419, Korea
5Department of Plant and Microbial Biology, University Zurich, Zurich, 8008 Zurich, Switzerland

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Akiyama, 2005, Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi, Nature, 435, 824, 10.1038/nature03608

Almen, 2009, Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin, BMC Biol., 7, 50, 10.1186/1741-7007-7-50

Awai, 2006, Lipid trafficking between the endoplasmic reticulum and the chloroplast, Biochem. Soc. Trans., 34, 395, 10.1042/BST0340395

Banasiak, 2013, A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids, J. Exp. Bot., 64, 1005, 10.1093/jxb/ers380

Banks, 2011, The Selaginella genome identifies genetic changes associated with the evolution of vascular plants, Science, 332, 960, 10.1126/science.1203810

Barthlott, 1997, Purity of the sacred lotus, or escape from contamination in biological surfaces, Planta, 202, 1, 10.1007/s004250050096

Baxter, 2003, Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice, Plant Physiol., 132, 618, 10.1104/pp.103.021923

Bessire, 2011, A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis, Plant Cell, 23, 1958, 10.1105/tpc.111.083121

Bienert, 2012, A pleiotropic drug resistance transporter in Nicotiana tabacum is involved in defense against the herbivore Manduca sexta, Plant J., 72, 745, 10.1111/j.1365-313X.2012.05108.x

Bird, 2007, Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion, Plant J., 52, 485, 10.1111/j.1365-313X.2007.03252.x

Bishopp, 2011, Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem, Curr. Biol., 21, 927, 10.1016/j.cub.2011.04.049

Blaby, 2014, The Chlamydomonas genome project: a decade on, Trends Plant Sci., 19, 672, 10.1016/j.tplants.2014.05.008

Blakeslee, 2007, Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis, Plant Cell, 19, 131, 10.1105/tpc.106.040782

Bonaventure, 2004, Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: occurrence of octadeca-cis-6, cis-9-diene-1,18-dioate as the major component, Plant J., 40, 920, 10.1111/j.1365-313X.2004.02258.x

Brohee, 2010, YTPdb: a wiki database of yeast membrane transporters, Biochim. Biophys. Acta, 1798, 1908, 10.1016/j.bbamem.2010.06.008

Brunetti, 2015, Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis, J. Exp. Bot., 66, 3815, 10.1093/jxb/erv185

Buda, 2013, An ATP binding cassette transporter is required for cuticular wax deposition and desiccation tolerance in the moss Physcomitrella patens, Plant Cell, 25, 4000, 10.1105/tpc.113.117648

Bult, 2016, Mouse genome database 2016, Nucleic Acids Res., 44, D840, 10.1093/nar/gkv1211

Burghardt, 2008, Cuticular transpiration, Annu. Plant Rev. Biol. Plant Cuticle, 23, 10

Campbell, 2003, Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis, Plant Physiol., 133, 1272, 10.1104/pp.103.024182

Cecchetti, 2015, ABCB1 and ABCB19 auxin transporters have synergistic effects on early and late Arabidopsis anther development, J. Integr. Plant Biol., 57, 1089, 10.1111/jipb.12332

Champagne, 2013, Proteomic snapshot of spearmint (Mentha spicata L.) leaf trichomes: a genuine terpenoid factory, Proteomics, 13, 3327, 10.1002/pmic.201300280

Cho, 2013, The function of ABCB transporters in auxin transport, Plant Signal. Behav., 8, 642, 10.4161/psb.22990

Cho, 2007, P-Glycoprotein4 displays auxin efflux transporter–like action in Arabidopsis root hair cells and tobacco cells, Plant Cell, 19, 3930, 10.1105/tpc.107.054288

Choi, 2014, The role of Arabidopsis ABCG9 and ABCG31 ATP binding cassette transporters in pollen fitness and the deposition of steryl glycosides on the pollen coat, Plant Cell, 26, 310, 10.1105/tpc.113.118935

Christie, 2009, Functional annotations for the Saccharomyces cerevisiae genome: the knowns and the known unknowns, Trends Microbiol., 17, 286, 10.1016/j.tim.2009.04.005

Clark, 2007, Evolution of genes and genomes on the Drosophila phylogeny, Nature, 450, 203, 10.1038/nature06341

Clay, 2009, Glucosinolate metabolites required for an Arabidopsis innate immune response, Science, 323, 95, 10.1126/science.1164627

Crouzet, 2013, NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum, is involved in diterpene transport, Plant Mol. Biol., 82, 181, 10.1007/s11103-013-0053-0

De Hertogh, 2002, Phylogenetic classification of transporters and other membrane proteins from Saccharomyces cerevisiae, Funct. Integr. Genomics, 2, 154, 10.1007/s10142-002-0060-8

De Michele, 2012, Ammonium and urea transporter inventory of the Selaginella and Physcomitrella genomes, Front. Plant Sci., 3, 62, 10.3389/fpls.2012.00062

Dean, 2004, Uptake of salicylic acid 2-O-beta-D-glucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism, Physiol. Plant, 120, 603, 10.1111/j.0031-9317.2004.0263.x

Dean, 2005, Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates, Annu. Rev. Genomics Hum. Genet., 6, 123, 10.1146/annurev.genom.6.080604.162122

Endo, 2008, Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells, Plant Physiol., 147, 1984, 10.1104/pp.108.116632

Everant-Bourbouloux, 1982, Transport and metabolism of labelled abscisic acid in broad-bean plants (Vicia faba L.), Physiol. Plant, 54, 431, 10.1111/j.1399-3054.1982.tb00704.x

Ezkurdia, 2014, Multiple evidence strands suggest that there may be as few as 19 000 human protein-coding genes, Hum. Mol. Genet., 23, 5866, 10.1093/hmg/ddu309

Fan, 2015, Arabidopsis TRIGALACTOSYLDIACYLGLYCEROL5 interacts with TGD1, TGD2, and TGD4 to facilitate lipid transfer from the endoplasmic reticulum to plastids, Plant Cell, 27, 2941

Footitt, 2002, Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP, EMBO J., 21, 2912, 10.1093/emboj/cdf300

Fourcroy, 2014, Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency, New Phytol., 201, 155, 10.1111/nph.12471

Francisco, 2013, ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-O-glucosides, Plant Cell, 25, 1840, 10.1105/tpc.112.102152

Frangne, 2002, Flavone glucoside uptake into barley mesophyll and Arabidopsis cell culture vacuoles. Energization occurs by H(+)-antiport and ATP-binding cassette-type mechanisms, Plant Physiol., 128, 726, 10.1104/pp.010590

Freeman, 2008, An overview of plant defenses against pathogens and herbivores, Plant Health Instructor, 10.1094/PHI-I-2008-0226-01

Fulda, 2004, Peroxisomal Acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana, Plant Cell, 16, 394, 10.1105/tpc.019646

Gaedeke, 2001, The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement, EMBO J., 20, 1875, 10.1093/emboj/20.8.1875

Gaillard, 1994, A herbicide antidote (safener) induces the activity of both the herbicide detoxifying enzyme and of a vacuolar transporter for the detoxified herbicide, FEBS Lett., 352, 219, 10.1016/0014-5793(94)00961-9

Geisler, 2005, Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1, Plant J., 44, 179, 10.1111/j.1365-313X.2005.02519.x

Gomez-Roldan, 2008, Strigolactone inhibition of shoot branching, Nature, 455, 189, 10.1038/nature07271

Goodman, 2004, A multidrug resistance–associated protein involved in anthocyanin transport in Zea mays, Plant Cell, 16, 1812, 10.1105/tpc.022574

Hayashi, 2002, Ped3p is a peroxisomal ATP-binding cassette transporter that might supply substrates for fatty acid β-oxidation, Plant Cell Physiol., 43, 1, 10.1093/pcp/pcf023

Heredia, 2003, Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer, Biochim. Biophys. Acta, 1620, 1, 10.1016/S0304-4165(02)00510-X

Hillier, 2005, Genomics in C. elegans: so many genes, such a little worm, Genome Res., 15, 1651, 10.1101/gr.3729105

Huang, 2009, A bacterial-type ABC transporter is involved in aluminum tolerance in rice, Plant Cell, 21, 655, 10.1105/tpc.108.064543

Ikegami, 2009, Activation of abscisic acid biosynthesis in the leaves of Arabidopsis thaliana in response to water deficit, J. Plant Res., 122, 235, 10.1007/s10265-008-0201-9

Ito, 2006, A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides, Plant Physiol., 142, 63, 10.1104/pp.106.084533

James, 2010, Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants, Proc. Natl. Acad. Sci. USA, 107, 17833, 10.1073/pnas.0911359107

Jasiñski, 2001, A plant plasma membrane ATP binding cassette–type transporter is involved in antifungal terpenoid secretion, Plant Cell, 13, 1095

Jetter, 2008, 4 Composition of plant cuticular waxes, Annu. Plant Rev. Biol. Plant Cuticle, 23, 145

Ji, 2014, ATP-dependent binding cassette transporter G family member 16 increases plant tolerance to abscisic acid and assists in basal resistance against pseudomonas syringae DC3000, Plant Physiol., 166, 879, 10.1104/pp.114.248153

Kamimoto, 2012, Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration, Plant Cell Physiol., 53, 2090, 10.1093/pcp/pcs149

Kaneda, 2011, ABC transporters coordinately expressed during lignification of Arabidopsis stems include a set of ABCBs associated with auxin transport, J. Exp. Bot., 62, 2063, 10.1093/jxb/erq416

Kang, 2010, PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid, Proc. Natl. Acad. Sci. USA, 107, 2355, 10.1073/pnas.0909222107

Kang, 2011, Plant ABC transporters, Arabidopsis Book, 9, e0153, 10.1199/tab.0153

Kang, 2015, Abscisic acid transporters cooperate to control seed germination, Nat. Commun., 6, 8113, 10.1038/ncomms9113

Kanno, 2010, Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions, Plant Cell Physiol., 51, 1988, 10.1093/pcp/pcq158

Kanno, 2012, Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor, Proc. Natl. Acad. Sci. USA, 109, 9653, 10.1073/pnas.1203567109

Kiba, 2013, Side-chain modification of cytokinins control shoot growth in Arabidopsis, Dev. Cell, 27, 452, 10.1016/j.devcel.2013.10.004

Kim, 2007, The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance, Plant J., 50, 207, 10.1111/j.1365-313X.2007.03044.x

Kim, 2010, Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis, Physiol. Plant, 139, 170, 10.1111/j.1399-3054.2010.01353.x

Kim, 2013, AtABCA9 transporter supplies fatty acids for lipid synthesis to the endoplasmic reticulum, Proc. Natl. Acad. Sci. USA, 110, 773, 10.1073/pnas.1214159110

Klein, 1998, Directly energized uptake of beta-estradiol 17-(beta-D-glucuronide) in plant vacuoles is strongly stimulated by glutathione conjugates, J. Biol. Chem., 273, 262, 10.1074/jbc.273.1.262

Klein, 2003, The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use, Plant J., 33, 119, 10.1046/j.1365-313X.2003.016012.x

Ko, 2014, Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin, Proc. Natl. Acad. Sci. USA, 111, 7150, 10.1073/pnas.1321519111

Krattinger, 2009, A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat, Science, 323, 1360, 10.1126/science.1166453

Krauss, 1997, Attenuation of UV radiation by plant cuticles from woody species, Plant Cell Environ., 20, 1079, 10.1111/j.1365-3040.1997.tb00684.x

Kretzschmar, 2012, A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching, Nature, 483, 341, 10.1038/nature10873

Kreuz, 1996, Old enzymes for a new job (herbicide detoxification in plants), Plant Physiol., 111, 349, 10.1104/pp.111.2.349

Kunst, 2003, Biosynthesis and secretion of plant cuticular wax, Prog. Lipid Res., 42, 51, 10.1016/S0163-7827(02)00045-0

Kuromori, 2010, ABC transporter AtABCG25 is involved in abscisic acid transport and responses, Proc. Natl. Acad. Sci. USA, 107, 2361, 10.1073/pnas.0912516107

Kuromori, 2014, Intertissue signal transfer of abscisic acid from vascular cells to guard cells, Plant Physiol., 164, 1587, 10.1104/pp.114.235556

Lamesch, 2012, The Arabidopsis information resource (TAIR): improved gene annotation and new tools, Nucleic Acids Res., 40, D1202, 10.1093/nar/gkr1090

Lang, 2008, Exploring plant biodiversity: the Physcomitrella genome and beyond, Trends Plant Sci., 13, 542, 10.1016/j.tplants.2008.07.002

Larsen, 1997, Al inhibits both shoot development and root growth in als3, an Al-sensitive Arabidopsis mutant, Plant Physiol., 114, 1207, 10.1104/pp.114.4.1207

Larsen, 2005, ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis, Plant J., 41, 353

Lee, 2012, ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant, Cell Environ., 35, 53, 10.1111/j.1365-3040.2011.02426.x

Lee, 2008, The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2, Nat. Cell Biol., 10, 1217, 10.1038/ncb1782

Lewis, 2009, Auxin transport into cotyledons and cotyledon growth depend similarly on the ABCB19 Multidrug Resistance-like transporter, Plant J., 60, 91, 10.1111/j.1365-313X.2009.03941.x

Lousa, 2013, Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporter is required for transport and metabolism of fatty acids, Proc. Natl. Acad. Sci. USA, 110, 1279, 10.1073/pnas.1218034110

Lu, 2009, A 25-amino acid sequence of the Arabidopsis TGD2 protein is sufficient for specific binding of phosphatidic acid, J. Biol. Chem., 284, 17420, 10.1074/jbc.M109.016014

Lu, 1997, AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene, Proc. Natl. Acad. Sci. USA, 94, 8243, 10.1073/pnas.94.15.8243

Lu, 2007, A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import, J. Biol. Chem., 282, 35945, 10.1074/jbc.M704063200

Lu, 2015, Mutant allele-specific uncoupling of PEN3 functions reveals engagement of the ABC transporter in distinct tryptophan metabolic pathways, Plant Physiol., 168, 814, 10.1104/pp.15.00182

Luo, 2007, An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion, Plant Cell Physiol., 48, 1790, 10.1093/pcp/pcm152

McFarlane, 2010, Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations, Plant Cell, 22, 3066, 10.1105/tpc.110.077974

Merchant, 2007, The Chlamydomonas genome reveals the evolution of key animal and plant functions, Science, 318, 245, 10.1126/science.1143609

Merilo, 2015, Abscisic acid transport and homeostasis in the context of stomatal regulation, Mol. Plant, 8, 1321, 10.1016/j.molp.2015.06.006

Müller, 2008, 13 Plant–Insect interactions on cuticular surfaces, Annu. Plant Rev. Biol. Plant Cuticle, 23, 398

Mutch, 2004, Regional variations in ABC transporter expression along the mouse intestinal tract, Physiol. Genomics, 17, 11, 10.1152/physiolgenomics.00150.2003

Nagy, 2009, The Arabidopsis ATP-binding Cassette Protein AtMRP5/AtABCC5 is a high affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage, J. Biol. Chem., 284, 33614, 10.1074/jbc.M109.030247

Nambara, 2005, Abscisic acid biosynthesis and catabolism, Annu. Rev. Plant Biol., 56, 165, 10.1146/annurev.arplant.56.032604.144046

Nawrath, 2002, The biopolymers cutin and suberin, Arabidopsis Book, 1, e0021, 10.1199/tab.0021

Nguyen, 2014, Genome-wide expression analysis of rice ABC transporter family across spatio-temporal samples and in response to abiotic stresses, J. Plant Physiol., 171, 1276, 10.1016/j.jplph.2014.05.006

Niu, 2013, The ATP-binding cassette transporter OsABCG15 is required for anther development and pollen fertility in rice, J. Integr. Plant Biol., 55, 710, 10.1111/jipb.12053

Nyathi, 2010, The Arabidopsis peroxisomal ABC transporter, comatose, complements the Saccharomyces cerevisiae pxa1 pxa2Δ mutant for metabolism of long-chain fatty acids and exhibits fatty acyl-CoA-stimulated ATPase activity, J. Biol. Chem., 285, 29892, 10.1074/jbc.M110.151225

Ouyang, 2007, The TIGR rice genome annotation resource: improvements and new features, Nucleic Acids Res., 35, D883, 10.1093/nar/gkl976

Panikashvili, 2007, The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion, Plant Physiol., 145, 1345, 10.1104/pp.107.105676

Panikashvili, 2010, The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots, Mol. Plant, 3, 563, 10.1093/mp/ssp103

Panikashvili, 2011, The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis, New Phytol., 190, 113, 10.1111/j.1469-8137.2010.03608.x

Park, 2012, The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury, Plant J., 69, 278, 10.1111/j.1365-313X.2011.04789.x

Park, 2013, The alpha/beta hydrolase CGI-58 and peroxisomal transport protein PXA1 coregulate lipid homeostasis and signaling in Arabidopsis, Plant Cell, 25, 1726, 10.1105/tpc.113.111898

Paumi, 2009, ABC transporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily, Microbiol. Mol. Biol. Rev., 73, 577, 10.1128/MMBR.00020-09

Piecuch, 2014, Yeast ABC proteins involved in multidrug resistance, Cell Mol. Biol. Lett., 19, 1, 10.2478/s11658-013-0111-2

Pighin, 2004, Plant cuticular lipid export requires an ABC transporter, Science, 306, 702, 10.1126/science.1102331

Prasad, 2012, Yeast ATP-binding cassette transporters conferring multidrug resistance, Annu. Rev. Microbiol., 66, 39, 10.1146/annurev-micro-092611-150111

Procko, 2009, The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter, FASEB J., 23, 1287, 10.1096/fj.08-121855

Quilichini, 2014, New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana, Ann. Bot., 114, 1189, 10.1093/aob/mcu042

Ren, 2007, TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels, Nucleic Acids Res., 35, D274, 10.1093/nar/gkl925

Roston, 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, 21406, 10.1074/jbc.M112.370213

Ruocco, 2011, Four potato (Solanum tuberosum) ABCG transporters and their expression in response to abiotic factors and Phytophthora infestans infection, J. Plant Physiol., 168, 2225, 10.1016/j.jplph.2011.07.008

Russell, 2000, The Arabidopsis COMATOSE locus regulates germination potential, Development, 127, 3759, 10.1242/dev.127.17.3759

Ruzicka, 2010, Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid, Proc. Natl. Acad. Sci. USA, 107, 10749, 10.1073/pnas.1005878107

Sanchez-Fernandez, 2001, The Arabidopsis thaliana ABC protein superfamily, a complete inventory, J. Biol. Chem., 276, 30231, 10.1074/jbc.M103104200

Sasse, 2015, Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport, Curr. Biol., 25, 647, 10.1016/j.cub.2015.01.015

Seo, 2011, Transport of ABA from the site of biosynthesis to the site of action, J. Plant Res., 124, 501, 10.1007/s10265-011-0411-4

Seto, 2014, Strigolactone biosynthesis and perception, Curr. Opin. Plant Biol., 21, 1, 10.1016/j.pbi.2014.06.001

Sheps, 2004, The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes, Genome Biol., 5, R15, 10.1186/gb-2004-5-3-r15

Shi, 2007, Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds, Nat. Biotechnol., 25, 930, 10.1038/nbt1322

Shim, 2013, Transgenic poplar trees expressing yeast cadmium factor 1 exhibit the characteristics necessary for the phytoremediation of mine tailing soil, Chemosphere, 90, 1478, 10.1016/j.chemosphere.2012.09.044

Shitan, 2003, Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica, Proc. Natl. Acad. Sci. USA, 100, 751, 10.1073/pnas.0134257100

Song, 2003, Engineering tolerance and accumulation of lead and cadmium in transgenic plants, Nat. Biotechnol., 21, 914, 10.1038/nbt850

Song, 2010, Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters, Proc. Natl. Acad. Sci. USA, 107, 21187, 10.1073/pnas.1013964107

Song, 2014, A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain, Proc. Natl. Acad. Sci. USA, 111, 15699, 10.1073/pnas.1414968111

Stein, 2006, Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration, Plant Cell, 18, 731, 10.1105/tpc.105.038372

Strader, 2009, The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid, Plant Cell, 21, 1992, 10.1105/tpc.109.065821

Strader, 2011, Transport and metabolism of the endogenous auxin precursor indole-3-butyric acid, Mol. Plant, 4, 477, 10.1093/mp/ssr006

Stukkens, 2005, NpPDR1, a pleiotropic drug resistance-type ATP-binding cassette transporter from Nicotiana plumbaginifolia, plays a major role in plant pathogen defense, Plant Physiol., 139, 341, 10.1104/pp.105.062372

Suh, 2005, Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis, Plant Physiol., 139, 1649, 10.1104/pp.105.070805

Tamura, 2013, MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 30, 2725, 10.1093/molbev/mst197

Terasaka, 2005, PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots, Plant Cell, 17, 2922, 10.1105/tpc.105.035816

Treutter, 2006, Significance of flavonoids in plant resistance: a review, Environ. Chem. Lett., 4, 147, 10.1007/s10311-006-0068-8

Ukitsu, 2007, Cytological and biochemical analysis of COF1, an Arabidopsis mutant of an ABC transporter gene, Plant Cell Physiol., 48, 1524, 10.1093/pcp/pcm139

Umehara, 2008, Inhibition of shoot branching by new terpenoid plant hormones, Nature, 455, 195, 10.1038/nature07272

Underwood, 2013, Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter, Proc. Natl. Acad. Sci. USA, 110, 12492, 10.1073/pnas.1218701110

Van Belle, 2001, A genomic view of yeast membrane transporters, Curr. Opin. Cell Biol., 13, 389, 10.1016/S0955-0674(00)00226-X

Van Den Brûle, 2002, The ABC transporter SpTUR2 confers resistance to the antifungal diterpene sclareol, Plant J., 30, 649, 10.1046/j.1365-313X.2002.01321.x

Vasiliou, 2009, Human ATP-binding cassette (ABC) transporter family, Hum. Genomics, 3, 281, 10.1186/1479-7364-3-3-281

Verrier, 2008, Plant ABC proteins–a unified nomenclature and updated inventory, Trends Plant Sci., 13, 151, 10.1016/j.tplants.2008.02.001

Von Uexküll, 1995, Global extent, development and economic impact of acid soils, Plant Soil, 171, 1, 10.1007/BF00009558

Waldie, 2014, Strigolactones and the control of plant development: lessons from shoot branching, Plant J., 79, 607, 10.1111/tpj.12488

Wallace, 2011, Evolutionary development of the plant spore and pollen wall, AoB Plants, 2011, plr027, 10.1093/aobpla/plr027

Wang, 2015, Insights into the origin and evolution of the plant hormone signaling machinery, Plant Physiol., 167, 872, 10.1104/pp.114.247403

Wellman, 2004, Origin, function and development of the spore wall in early land plants, 43

Wilkens, 2015, Structure and mechanism of ABC transporters, F1000Prime Rep., 7, 14, 10.12703/P7-14

Wilkinson, 1997, Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast, Plant Physiol., 113, 559, 10.1104/pp.113.2.559

Wu, 2014, OsABCG15 encodes a membrane protein that plays an important role in anther cuticle and pollen exine formation in rice, Plant Cell Rep., 33, 1881, 10.1007/s00299-014-1666-8

Xie, 2015, Cloning and characterization of a novel Nicotiana tabacum ABC transporter involved in shoot branching, Physiol. Plant, 153, 299, 10.1111/ppl.12267

Xu, 2003, A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis, EMBO J., 22, 2370, 10.1093/emboj/cdg234

Xu, 2008, Lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis requires the extraplastidic TGD4 protein, Plant Cell, 20, 2190, 10.1105/tpc.108.061176

Yadav, 2014, ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis, Plant Cell, 26, 3569, 10.1105/tpc.114.129049

Yang, 2009, Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe, Plant J., 59, 179, 10.1111/j.1365-313X.2009.03856.x

Yazaki, 2001, A novel Coptis japonica multidrug-resistant protein preferentially expressed in the alkaloid-accumulating rhizome, J. Exp. Bot., 52, 877, 10.1093/jexbot/52.357.877

Ye, 2014, Human transporter database: comprehensive knowledge and discovery tools in the human transporter genes, PLoS One, 9, e88883, 10.1371/journal.pone.0088883

Yu, 2013, ATP-binding cassette transporter controls leaf surface secretion of anticancer drug components in Catharanthus roseus, Proc. Natl. Acad. Sci. USA, 110, 15830, 10.1073/pnas.1307504110

Zhang, 2014, A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis, Mol. Plant, 7, 1522, 10.1093/mp/ssu063

Zhang, 2014, Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins, Nat. Commun., 5, 3274, 10.1038/ncomms4274

Zhao, 2015, Flavonoid transport mechanisms: how to go, and with whom, Trends Plant Sci., 20, 576, 10.1016/j.tplants.2015.06.007

Zimmer, 2013, Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions, BMC Genomics, 14, 498, 10.1186/1471-2164-14-498

Zolman, 2001, The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation, Plant Physiol., 127, 1266, 10.1104/pp.010550