The ABC of Phytohormone Translocation

Abstract

ATP-driven transport across biological membranes is a key process to translocate solutes from the interior of the cell to the extracellular environment. In humans, ATP-binding cassette transporters are involved in absorption, distribution, metabolism, excretion, and toxicity, and also play a major role in anticancer drug resistance. Analogous transporters are also known to be involved in phytohormone translocation. These include, e.g., the transport of auxin by ABCB1/19 in Arabidopsis thaliana, the transport of abscisic acid by AtABCG25, and the transport of strigolactone by the Petunia hybrida ABC transporter PDR1. Within this article, we outline the current knowledge about plant ABC transporters with respect to their structure and function, and provide, for the first time, a protein homology model of the strigolactone transporter PDR1 from P. hybrida.

Key words

Petunia hybrida PDR1 - Solanaceae - Arabidopsis thaliana - Brassicaceae - ABC transporters - phytohormone transport - homology modelling

• References

• 1 Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E. Plant ABC Transporters. Arabidopsis Book 2011; 9: e0153
• 2 Robert HS, Friml J. Auxin and other signals on the move in plants. Nat Chem Biol 2009; 5: 325-332
• 3 Santner A, Estelle M. Recent advances and emerging trends in plant hormone signalling. Nature 2009; 459: 1071-1078
• 4 Kretzschmar T, Burla B, Lee Y, Martinoia E, Nagy R. Functions of ABC transporters in plants. Essays Biochem 2011; 50: 145-160
• 5 Martinoia E, Grill E, Tommasini R, Kreuz K, Amrhein N. ATP-dependent glutathione S-conjugate “export” pump in the vacuolar membrane of plants. Nature 1993; 364: 247-249
• 6 Lu YP, Li ZS, Rea PA. 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 U S A 1997; 94: 8243-8248
• 7 Lu YP, Li ZS, Drozdowicz YM, Hortensteiner S, Martinoia E, Rea PA. AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with Atmrp1. Plant Cell 1998; 10: 267-282
• 8 Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E. An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 1998; 13: 773-780
• 9 Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 2007; 50: 207-218
• 10 Lee M, Lee K, Lee J, Noh EW, Lee Y. AtPDR12 contributes to lead resistance in Arabidopsis . Plant Physiol 2005; 138: 827-836
• 11 Mackenzie B, Takanaga H, Hubert N, Rolfs A, Hediger MA. Functional properties of multiple isoforms of human divalent metal-ion transporter 1 (DMT1). Biochem J 2007; 403: 59-69
• 12 Larsen PB, Geisler MJB, Jones CA, Williams KM, Cancel JD. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis . Plant J 2005; 41: 353-363
• 13 Larsen PB, Cancel J, Rounds M, Ochoa V. Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 2007; 225: 1447-1458
• 14 Prell J, Poole P. Metabolic changes of Rhizobia in legume nodules. Trends Microbiol 2006; 14: 161-168
• 15 Sugiyama A, Shitan N, Yazaki K. Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-Rhizobium symbiosis. Plant Physiol 2007; 144: 2000-2008
• 16 Sugiyama A, Shitan N, Yazaki K. Signaling from soybean roots to Rhizobium: An ATP-binding cassette-type transporter mediates genistein secretion. Plant Signal Behav 2008; 3: 38-40
• 17 Priha O, Grayston SJ, Pennanen T, Smolander A. Microbial activities related to C and N cycling and microbial community structure in the rhizospheres of Pinus sylvestris, Picea abies and Betula pendula seedlings in an organic and mineral soil. FEMS Microbiol Ecol 1999; 30: 187-199
• 18 Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P. Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol 2006; 170: 165-175
• 19 Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 2009; 151: 2006-2017
• 20 Noctor G, Foyer CH. Ascorbate and Glutathione: Keeping Active Oxygen Under Control. Annu Rev Plant Physiol Plant Mol Biol 1998; 49: 249-279
• 21 Hinder B, Schellenberg M, Rodoni S, Ginsburg S, Vogt E, Martinoia E, Matile P, Hörtensteiner S. How plants dispose of chlorophyll catabolites. Directly energized uptake of tetrapyrrolic breakdown products into isolated vacuoles. J Biol Chem 1996; 271: 27233-27236
• 22 Nagy R, Grob H, Weder B, Green P, Klein M, Frelet-Barrand A, Schjoerring JK, Brearley C, Martinoia E. 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 2009; 284: 33614-33622
• 23 Zolman BK, Silva ID, Bartel B. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid beta-oxidation. Plant Physiol 2001; 127: 1266-1278
• 24 Yazaki K, Shitan N, Takamatsu H, Ueda K, Sato F. A novel Coptis japonica multidrug-resistant protein preferentially expressed in the alkaloid-accumulating rhizome. J Exp Bot 2001; 52: 877-879
• 25 Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K. Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica . Proc Natl Acad Sci U S A 2003; 100: 751-756
• 26 Sato F, Takeshita N, Fitchen JH, Fujiwara H, Yamada Y. S-adenosyl-l-methionine: scoulerine-9-O-methyltransferase from cultured Coptis japonica cells. Phytochemistry 1993; 32: 659-664
• 27 Badri DV, Loyola-Vargas VM, Broeckling CD, De-la-Peña C, Jasinski M, Santelia D, Martinoia E, Sumner LW, Banta LM, Stermitz F, Vivanco JM. Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 2008; 146: 762-771
• 28 Bultreys A, Trombik T, Drozak A, Boutry M. Nicotiana plumbaginifolia plants silenced for the ATP-binding cassette transporter gene NpPDR1 show increased susceptibility to a group of fungal and oomycete pathogens. Mol Plant Pathol 2009; 10: 651-663
• 29 Kobae Y, Sekino T, Yoshioka H, Nakagawa T, Martinoia E, Maeshima M. Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol 2006; 47: 309-318
• 30 Campbell EJ, Schenk PM, Kazan K, Penninckx IAMA, Anderson JP, Maclean DJ, Cammue BPA, Ebert PR, Manners JM. 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 2003; 133: 1272-1284
• 31 Bessire M, Borel S, Fabre G, Carraça L, Efremova N, Yephremov A, Cao Y, Jetter R, Jacquat AC, Métraux JP, Nawrath C. 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 2011; 23: 1958-1970
• 32 Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Höfer R, Schreiber L, Chory J, Aharoni A. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 2007; 145: 1345-1360
• 33 Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL. Plant cuticular lipid export requires an ABC transporter. Science 2004; 306: 702-704
• 34 Jasiński M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M. A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 2001; 13: 1095-1107
• 35 Cushnie TPT, Lamb AJ. Recent advances in understanding the antibacterial properties of flavonoids. Int J Antimicrob Agents 2011; 38: 99-107
• 36 Jia Z, Zou B, Wang X, Qiu J, Ma H, Gou Z, Song S, Dong H. Quercetin-induced H(2)O(2) mediates the pathogen resistance against Pseudomonas syringae pv. Tomato DC3000 in Arabidopsis thaliana . Biochem Biophys Res Commun 2010; 396: 522-527
• 37 Banasiak J, Biala W, Staszków A, Swarcewicz B, Kepczynska E, Figlerowicz M, Jasinski M. A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. J Exp Bot 2013; 64: 1005-1015
• 38 Okada K, Shimura Y. Modulation of root growth by physical stimuli. In: Meyerowitz EM, Somerville CR. Arabidopsis . Cold Spring Harbor: Laboratory Press; 1994: 665-684
• 39 Scarpella E, Marcos D, Friml J, Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes Dev 2006; 20: 1015-1027
• 40 Cosgrove DJ. Growth of the plant cell wall. Nat Rev Mol Cell Biol 2005; 6: 850-861
• 41 Bonner J, Bandurski RS. Studies of the physiology, pharmacology, and biochemistry of the auxins. Annu Rev Plant Physiol 1952; 3: 59-86
• 42 Whippo CW, Hangarter RP. Phototropism: bending towards enlightenment. Plant Cell 2006; 18: 1110-1119
• 43 Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 1999; 18: 2066-2073
• 44 Blakeslee JJ, Peer WA, Murphy AS. Auxin transport. Curr Opin Plant Biol 2005; 8: 494-500
• 45 Kramer EM, Bennett MJ. Auxin transport: a field in flux. Trends Plant Sci 2006; 11: 382-386
• 46 Morris DA, Rubery PH, Jarman J, Sabater M. Effects of inhibitors of protein synthesis on transmembrane auxin transport in Cucurbita pepo L. hypocotyl segments. J Exp Bot 1991; 42: 773-783
• 47 Petrásek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wisniewska J, Tadele Z, Kubes M, Covanová M, Dhonukshe P, Skupa P, Benková E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazímalová E, Friml J. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 2006; 312: 914-918
• 48 Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KFK, Smith AP, Baroux C, Grossniklaus U, Müller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 2005; 44: 179-194
• 49 Cho M, Lee SH, Cho HT. P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 2007; 19: 3930-3943
• 50 Kaneda M, Schuetz M, Lin BSP, Chanis C, Hamberger B, Western TL, Ehlting J, Samuels AL. ABC transporters coordinately expressed during lignification of Arabidopsis stems include a set of ABCBs associated with auxin transport. J Exp Bot 2011; 62: 2063-2077
• 51 Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M, Sakai T, Friml J, Peer WA, Murphy AS. ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis . Plant J 2009; 57: 27-44
• 52 Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, Lee OR, Paponov I, Palme K, Mancuso S, Murphy AS, Schulz B, Geisler M. Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 2006; 281: 30603-30612
• 53 Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 2008; 283: 21817-21826
• 54 Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J, Titapiwatanakun B, Ennis M, Kaiserli E, Lee OR, Adamec J, Peer WA, Murphy AS. phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 2011; 9: e1001076
• 55 Henrichs S, Wang B, Fukao Y, Zhu J, Charrier L, Bailly A, Oehring SC, Linnert M, Weiwad M, Endler A, Nanni P, Pollmann S, Mancuso S, Schulz A, Geisler M. Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J 2012; 31: 2965-2980
• 56 Katekar GF. Inhibitors of the geotropic response in plants: a correlation of molecular structures. Phytochemistry 1976; 15: 1421-1424
• 57 Katekar GF, Geissler AE. Auxin Transport Inhibitors: IV. Evidence of a common mode of action for a proposed class of auxin transport inhibitors: the phytotropins. Plant Physiol 1980; 66: 1190-1195
• 58 Nagashima A, Uehara Y, Sakai T. The ABC subfamily B auxin transporter AtABCB19 is involved in the inhibitory effects of N-1-naphthyphthalamic acid on the phototropic and gravitropic responses of Arabidopsis hypocotyls. Plant Cell Physiol 2008; 49: 1250-1255
• 59 Lewis DR, Miller ND, Splitt BL, Wu G, Spalding EP. Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 2007; 19: 1838-1850
• 60 Kim JY, Henrichs S, Bailly A, Vincenzetti V, Sovero V, Mancuso S, Pollmann S, Kim D, Geisler M, Nam HG. Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. J Biol Chem 2010; 285: 23309-23317
• 61 Surpin M, Rojas-Pierce M, Carter C, Hicks GR, Vasquez J, Raikhel NV. The power of chemical genomics to study the link between endomembrane system components and the gravitropic response. Proc Natl Acad Sci U S A 2005; 102: 4902-4907
• 62 Rojas-Pierce M, Titapiwatanakun B, Sohn EJ, Fang F, Larive CK, Blakeslee J, Cheng Y, Cutler SR, Cuttler S, Peer WA, Murphy AS, Raikhel NV. Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem Biol 2007; 14: 1366-1376
• 63 Conseil G, Baubichon-Cortay H, Dayan G, Jault JM, Barron D, Di Pietro A. Flavonoids: a class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proc Natl Acad Sci U S A 1998; 95: 9831-9836
• 64 Jacobs M, Rubery PH. Naturally occurring auxin transport regulators. Science 1988; 241: 346-349
• 65 Bailly A, Yang H, Martinoia E, Geisler M, Murphy AS. Plant lessons: exploring ABCB functionality through structural modeling. Front Plant Sci 2012; 2: 108
• 66 Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, Chang G. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009; 323: 1718-1722
• 67 Groot SP, Karssen CM. Dormancy and germination of abscisic acid-deficient tomato seeds: studies with the sitiens mutant. Plant Physiol 1992; 99: 952-958
• 68 Marshall JG, Scarratt JB, Dumbroff EB. Induction of drought resistance by abscisic acid and paclobutrazol in jack pine. Tree Physiol 1991; 8: 415-421
• 69 Saeedipour S. Salinity tolerance of rice lines related to endogenous abscisic acid (ABA) level synthesis under stress. AJPS 2011; 5: 628-633
• 70 Finkelstein RR, Gampala SSL, Rock CD. Abscisic acid signaling in seeds and seedlings. Plant Cell 2002; 14 (Suppl. 01) S15-S45
• 71 Okamoto M, Hanada A, Kamiya Y, Yamaguchi S, Nambara E. Measurement of abscisic acid and gibberellins by gas chromatography/mass spectrometry. Methods Mol Biol 2009; 495: 53-60
• 72 Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci U S A 2010; 107: 2361-2366
• 73 Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T. Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis . Plant Physiol 2004; 134: 1697-1707
• 74 Schachtman DP, Goodger JQD. Chemical root to shoot signaling under drought. Trends Plant Sci 2008; 13: 281-287
• 75 Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci U S A 2010; 107: 2355-2360
• 76 Kuromori T, Sugimoto E, Shinozaki K. Intertissue signal transfer of abscisic acid from vascular cells to guard cells. Plant Physiol 2014; 164: 1587-1592
• 77 Kuromori T, Sugimoto E, Shinozaki K. Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 2011; 67: 885-894
• 78 Gan S, Amasino RM. Inhibition of leaf senescence by autoregulated production of cytokinin. Science 1995; 270: 1986-1988
• 79 Werner T, Motyka V, Strnad M, Schmülling T. Regulation of plant growth by cytokinin. PNAS 2001; 98: 10487-10492
• 80 Samuelson ME, Larsson CM. Nitrate regulation of zeatin riboside levels in barley roots: effects of inhibitors of N assimilation and comparison with ammonium. Plant Science 1993; 93: 77-84
• 81 Sakakibara H. Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 2006; 57: 431-449
• 82 Chory J, Reinecke D, Sim S, Washburn T, Brenner M. A role for cytokinins in de-etiolation in Arabidopsis (det mutants have an altered response to cytokinins). Plant Physiol 1994; 104: 339-347
• 83 George EF, Hall MA, Klerk GJD. Plant growth regulators II: Cytokinins, their analogues and antagonists. In: George EF, Hall MA, Klerk GJD, editors Plant propagation by tissue culture. Amsterdam: Springer; 2008: 205-226
• 84 Barciszewski J, Siboska GE, Pedersen BO, Clark BFC, Rattan SIS. Evidence for the presence of kinetin in DNA and cell extracts. FEBS Letters 1996; 393: 197-200
• 85 Skoog F, Armstrong DJ. Cytokinins. Annu Rev Plant Physiol 1970; 21: 359-384
• 86 Kiba T, Takei K, Kojima M, Sakakibara H. Side-chain modification of cytokinins controls shoot growth in Arabidopsis . Dev Cell 2013; 27: 452-461
• 87 Corbesier L, Prinsen E, Jacqmard A, Lejeune P, Onckelen HV, Périlleux C, Bernier G. Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition. J Exp Bot 2003; 54: 2511-2517
• 88 Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 2008; 59: 75-83
• 89 Gillissen B, Bürkle L, André B, Kühn C, Rentsch D, Brandl B, Frommer WB. A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis . Plant Cell 2000; 12: 291-300
• 90 Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim KY, Kwon M, Endler A, Song WY, Martinoia E, Sakakibara H, Lee Y. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. PNAS 2014; 111: 7150-7155
• 91 Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S. Inhibition of shoot branching by new terpenoid plant hormones. Nature 2008; 455: 195-200
• 92 Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF. Strigolactone inhibition of shoot branching. Nature 2008; 455: 189-194
• 93 Boyer FD, de Saint Germain A, Pillot JP, Pouvreau JB, Chen VX, Ramos S, Stévenin A, Simier P, Delavault P, Beau JM, Rameau C. Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol 2012; 159: 1524-1544
• 94 Zwanenburg B, Pospíšil T. Structure and activity of strigolactones: new plant hormones with a rich future. Mol Plant 2013; 6: 38-62
• 95 Prandi C, Occhiato EG, Tabasso S, Bonfante P, Novero M, Scarpi D, Bova ME, Miletto I. New potent fluorescent analogues of strigolactones: synthesis and biological activity in parasitic weed germination and fungal branching. Eur J Org Chem 2011; 2011: 3781-3793
• 96 Akiyama K, Matsuzaki K, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005; 435: 824-827
• 97 López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 2008; 178: 863-874
• 98 Moons A. Transcriptional profiling of the PDR gene family in rice roots in response to plant growth regulators, redox perturbations and weak organic acid stresses. Planta 2008; 229: 53-71
• 99 Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E. A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 2012; 483: 341-344
• 100 Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C. Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis . Plant Physiol 2011; 155: 974-987
• 101 Yang H, Murphy AS. Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe . Plant J 2009; 59: 179-191
• 102 Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucl Acids Res 2000; 28: 235-242
• 103 Rutledge RM, Esser L, Ma J, Xia D. Toward understanding the mechanism of action of the yeast multidrug resistance transporter Pdr5 p: a molecular modeling study. J Struct Biol 2011; 173: 333-344
• 104 The UniProt Consortium. Activities at the Universal Protein Resource (UniProt), nucleic acids res. 42: D191–D198 (2014). Available at http://uniprot.org Accessed July 1, 2014
• 105 Claros MG, von Heijne G. TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 1994; 10: 685-686
• 106 Cserzö M, Wallin E, Simon I, von Heijne G, Elofsson A. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 1997; 10: 673-676
• 107 Hofman K, Stoffel W. TMbase – a database of membrane spanning proteins segments. Biol Chem Hoppe Seyler 1993; 347: 166
• 108 Hirokawa T, Boon-Chieng S, Mitaku S. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 1998; 14: 378-379
• 109 Pasquier C, Promponas VJ, Palaios GA, Hamodrakas JS, Hamodrakas SJ. A novel method for predicting transmembrane segments in proteins based on a statistical analysis of the SwissProt database: the PRED-TMR algorithm. Protein Eng 1999; 12: 381-385
• 110 Juretić D, Zoranić L, Zucić D. Basic charge clusters and predictions of membrane protein topology. J Chem Inf Comput Sci 2002; 42: 620-632
• 111 Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305: 567-580
• 112 Jones DT, Taylor WR, Thornton JM. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 1994; 33: 3038-3049
• 113 Nugent T, Jones DT. Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 2009; 10: 159
• 114 Rost B, Yachdav G, Liu J. The PredictProtein server. Nucleic Acids Res 2004; 32: W321-W326
• 115 Molecular Operating Environment (MOE), 2013.08. Montreal, Canada: Chemical Computing Group, Inc.; 2013
• 116 Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A. Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics 2006; Chapter 5: Unit5.6
• 117 Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993; 26: 283-291
• 118 Laskowski RA, Hutchinson EG, Michie AD, Wallace AC, Jones ML, Thornton JM. PDBsum: a Web-based database of summaries and analyses of all PDB structures. Trends Biochem Sci 1997; 22: 488-490
• 119 Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem 2004; 25: 1605-1612
• 120 The PyMOL Molecular Graphics System, Version 1.6. Schrödinger, LLC. Available at http://www.pymol.org Accessed January 1, 2014