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The B subfamily of plant ATP binding cassette transporters and their roles in auxin transport

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  • Published:
Biologia Plantarum

Abstract

The ATP binding cassette B/multidrug-resistance/P-glycoprotein (ABCB/MDR/PGP) subfamily is a member of the ABC protein family. Significant progress has been made in the functional characterization of ABCB genes, particularly in Arabidopsis thaliana. This review evaluates recent advances concerning the plant ABCB subfamilies including their evolution and structure, the involvement and regulation of ABCB-mediated auxin transport, and the roles of ABCBs in plant growth and development. Insights into specific functions of members of the ABCB subfamily and their mediation of various regulatory pathways are also presented.

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Abbreviations

ABC:

ATP binding cassette

ABCB:

ATP binding cassette B

AUX1/LAX:

AUXIN RESISTANT1/LIKE AUX1

MDR:

multidrug-resistance

NBDs:

nucleotide-binding domains

NPA:

1-naphthylphthalamic acid

PGP:

P-glycoprotein

phot1:

PHOTOTROPIN 1

PID:

PINOID

PIN1:

PINFORMED1

TMDs:

transmembrane domains

TWD1:

immunophilin-like FKBP42 TWISTED DWARF1

References

  • Abel, S., Theologis, A.: The odyssey of auxin. — Cold Spring Harbour Perspect Biol. 2: a004572, 2010.

    CAS  Google Scholar 

  • Ambudkar, S., Dey, S., Hrycyna, C., Ramachandra, M., Pastan, I., Gottesman, M.: Biochemical, cellular, and pharmacological aspects of the multidrug transporter. — Annu. Rev. Pharmacol. Toxicol. 39: 361–398, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Bailly, A., Sovero, V., Vincenzetti, V., Santelia, D., Bartnik, D., Koenig, B.W., Mancuso, S., Martinoia, E., Geisler, M.: Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. — J. biol. Chem. 28: 21817–21826, 2008.

    Article  Google Scholar 

  • Baluska, F., Samaj, J., Menzel, D.: Polar transport of auxin: carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? — Trends Cell Biol. 13: 282–285, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Bandyopadhyay, A., Blakeslee, J.J., Lee, O.R., Mravec, J., Sauer, M., Titapiwatanakun, B., Makam, S.N., Bouchard, R., Geisler, M., Martinoia, E., Friml, J., Peer, W.A., Murphy, A.S.: Interactions of PIN and PGP auxin transport mechanisms. — Biochem. Soc. Trans. 35: 137–141, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Blakeslee, J.J., Bandyopadhyay, A., Lee, O.R., Mravec, J., Titapiwatanakun, B., Sauer, M., Makam, S.N., Cheng, Y., Bouchard, R., Adamec, J., Geisler, M., Nagashima, A., Sakai, T., Martinoia, E., Friml, J., Peer, W.A., Murphy, A.S.: Interactions among PINFORMED and P-glycoprotein auxin transporters in Arabidopsis thaliana. — Plant Cell 19: 131–147, 2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blakeslee, J.J., Peer, W.A., Murphy, A.S.: MDR/PGP auxin transport proteins and endocytic cycling. — In: In: Samaj, J., Baluska, F., Menze, D. (ed.): Plant Endocytosis. Pp. 159–176. Springer-Verlag, Berlin — Heidelberg 2005.

    Chapter  Google Scholar 

  • Bouchard, R., Bailly, A., Blakeslee, J.J., Oehring, S.C., Vincenzetti, V., Lee, O.R., Paponov, I., Palme, K., Mancuso, S., Murphy, A.S., Schulz, B., Geisler, M.: Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. — J. biol. Chem. 281: 30603–30612, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Brown, D.E., Rashotte, A.M., Murphy, A.S., Normanly, J., Tague, B.W., Peer, W.A., Taiz, L., Muday, G.K.: Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. — Plant Physiol. 126: 524–535, 2001.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cho, M., Lee, S.H., Cho, H.T.: P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. — Plant Cell 19: 3930–3943, 2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Christie, J.M., Yang, H., Richter, G.L., Sullivan, S., Thomson, C.E., Lin, J., Titapiwatanakun, B., Ennis, M., Kaiserli, E., Lee, O.R., Adamec, J., Peer, W.A., Murphy, A.S.: phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. — PLoS Biol. 9: e1001076, 2011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crouzet, J., Roland, J., Peeters, E., Trombik, T., Ducos, E., Nader, J., Boutry, M.: NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum, is involved in diterpene transport. — Plant mol. Biol. 82: 181–192, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Davies, T.G.E., Theodoulou, F.L., Hallahan, D.L., Forde, B.G.: Cloning and characterisation of a novel p-glycoprotein homologue from barley. — Gene 199: 195–202, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Ferte, J., Kuhnel, J.M., Chapuis, G., Rolland, Y., Lewin, G., Schwaller, M.A.: Flavonoid-related modulators of multidrug resistance: synthesis, pharmacological activity, and structureactivity relationships. — J. med. Chem. 42: 478–489, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Geisler, M., Blakeslee, J.J., Bouchard, R., Lee, O.R., Vincenzetti, V., Bandyopadhyay, A., Titapiwatanakun, B., Peer, W.A., Bailly, A., Richards, E.L., Ejendal, K.F., Smith, A.P., Baroux, C., Grossniklaus, U., Müller, A., Hrycyna, C.A., Dudler, R., Murphy, A.S., Martinoia, E.: Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. — Plant J. 44: 179–194, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Geisler, M., Girin, M., Brandt, S., Vincenzetti, V., Plaza, S., Paris, N., Kobae, Y., Maeshima, M., Billion, K., Kolukisaoglu, U.H., Schulz, B., Martinoia, E.: Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. — Mol. Biol. Cell 15: 3393–3405, 2004.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Geisler, M., Kolukisaoglu, H.U., Bouchard, R., Billion, K., Berger, J., Saal, B., Frangne, N., Koncz-Kalman, Z., Koncz, C., Dudler, R., Blakeslee, J.J., Murphy, A.S., Martinoia, E., Schulz, B.: TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. — Mol. Biol. Cell 14: 4238–4249, 2003.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goto, N., Starke, M., Kranr, A.R.: Effect of gibberellins on flower development of the pin-formed mutant of Arabidopsis thaliana. — Arabidopsis Inf. Serv. 23: 66–71, 1987.

    Google Scholar 

  • Henrichs, S., Wang, B., Fukao, Y., Zhu, J., Charrier, L., Bailly, A., Oehring, S.C., 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. 31: 2965–2980, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jasinski, M., Ducos, E., Martinoia, E., Boutry, M.: The ATPbinding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis. — Plant Physiol. 131: 1169–1177, 2003.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kamimoto, Y., Terasaka, K., Hamamoto, M., Takanashi, K., Fukuda, S., Shitan, N., Sugiyama, A., Suzuki, H., Shibata, D., Wang, B., Pollmann, S., Geisler, M., Yazaki, K.: Arabidopsis ABCB21 is a facultative auxin importer/ exporter regulated by cytoplasmic auxin concentration. — Plant Cell Physiol. 53: 2090–2100, 2012.

    CAS  PubMed  Google Scholar 

  • Klein, M., Geisler, M., Suh, S.J., Kolukisaoglu, H.U., Azevedo, L., Plaza, S., Curtis, M.D., Richter, A., Weder, B., Schulz, B., Martinoia, E.: 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: 219–236, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Knöller, A.S., Blakeslee, J.J., Richards, E.L., Peer, W.A., Murphy, A.S.: Brachytic2/ZmABCB1 functions in IAA export from intercalary meristems. — J. exp. Bot. 61: 3689–3696, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  • Krouk, G., Lacombe, B., Bielach, A., Perrine-Walker, F., Malinska, K., Mounier, E., Hoyerova, K., Tillard, P., Leon, S., Ljung, K., Zazimalova, E., Benkova, E., Nacry, P., Gojon, A.: Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. — Dev. Cell 18: 927–937, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Kubeš, M., Yang, H., Richter, G.L., Cheng, Y., Młodzińska, E., Wang, X., Blakeslee, J.J., Carraro, N., Petrášek, J., Zažímalová, E., Hoyerová, K., Peer, W.A., Murphy, A.S.: The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. — Plant J. 69: 640–654, 2012.

    Article  PubMed  Google Scholar 

  • Lee, M., Choi, Y., Burla, B., Kim, Y.Y., Jeon, B., Maeshima, M., Yoo, J.Y., Martinoia, E., Lee, Y.: The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. — Nat. Cell Biol. 10: 1217–1223, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Lee, M., Lee, K., Lee, J., Noh, E.W., Lee, Y.: AtPDR12 contributes to lead resistance in Arabidopsis. — Plant Physiol. 138: 827–836, 2005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Le Hir, R., Sorin, C., Chakraborti, D., Moritz, T., Schaller, H., Tellier, F., Robert, S., Morin, H., Bako, L., Bellini, C.: ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis. — Plant J. 76: 811–824, 2013.

    Article  PubMed  Google Scholar 

  • Lewis, D.R., Miller, N.D., Splitt, B.L., Wu, G., Spalding, E.P.: Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. — Plant Cell 19: 1838–1850, 2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lewis, D.R., Wu, G., Ljung, K., Spalding, E.P.: Auxin transport into cotyledons and cotyledon growth depend similarly on the ABCB19 multidrug resistance-like transporter. — Plant J. 60: 91–101, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Lin, R., Wang, H.: Two homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. — Plant Physiol. 138: 949–964, 2005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu, Q., Zhou, G.Q., Xu, F., Yan, X.L., Liao, H., Wang, J.X.: The involvement of auxin in root architecture plasticity in Arabidopsis induced by heterogeneous phosphorus availability. — Biol. Plant. 57: 739–748, 2013.

    Article  CAS  Google Scholar 

  • Ljung, K., Hull, A.K., Celenza, J., Yamada, M., Estelle, M., Normanly, J., Sandberg, G.: Sites and regulation of auxin biosynthesis in Arabidopsis roots. — Plant Cell 17: 1090–1104, 2005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martinoia, E., Klein, M., Geisler, M., Bovet, L., Forestier, C., Kolukisaoglu, U., Müller-Röber, B., Schulz, B.: Multifunctionality of plant ABC transporters-more than just detoxifiers. — Planta 214: 345–355, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Mravec, J., Kubes, M., Bielach, A., Gaykova, V., Petrásek, J., Skůpa, P., Chand, S., Benková, E., Zazímalová, E., Friml, J.: Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. — Development 135: 3345–3354, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Multani, D.S., Briggs, S.P., Chamberlin, M.A., Blakeslee, J.J., Murphy, A.S., Johal, G.S.: Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. — Science 302: 81–84, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Murphy, A., Peer, W., Blakeslee, J.J., Lee, O.R., Bandyopadhyay, A., Titapiwatanakun, B., Richards, E., Smith, A., Geisler, M., Martinoia, E., Ejendal, K.F.K., Hrycyna, C.A.: Transport. — Biol. Plant. 49 (Suppl): S9, 2005.

  • Murphy, A.S., Hoogner, K.R., Peer, W.A., Taiz, L.: Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. — Plant Physiol. 128: 935–950, 2002.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murphy, A.S., Peer, W.A., Taiz, L.: Regulation of auxin transport by aminopeptidases and endogenous flavonoids. — Planta 211: 315–324, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Noh, B., Bandyopadhyay, A., Peer, W.A., Spalding, E.P., Murphy, A.S. Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. — Nature 423: 999–1002, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Noh, B., Murphy, A.S., Spalding, E.P.: Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxinmediated development. — Plant Cell 13: 2441–2454, 2001.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nuhse, T.S., Stensballe, A., Jensen, O.N., Peck, S.C.: Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. — Plant Cell 16: 2394–2405, 2004.

    Article  PubMed Central  PubMed  Google Scholar 

  • Okada, K., Shimura, Y.: Modulation of Root Growth by Physical Stimuli in Arabidopsis. — Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1994.

    Google Scholar 

  • Okada, K., Ueda, J., Komaki, M.K., Bell, C.J., Shimura, Y.: Requirement of the auxin polar transport-system in early stages of Arabidopsis floral bud formation. — Plant Cell 3: 677–684, 1991.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park, B.S., Sang, W.G., Song, J.T., Lee, B.H., Kim, J.H., Se, H.S.: Auxin is involved in the regulation of leaf and root development by LAF1 under short day conditions. — Biol. Plant. 55: 647–652, 2011.

    Article  CAS  Google Scholar 

  • Peer, W.A., Bandyopadhyay, A., Blakeslee, J.J., Makam, S.N., Chen, R.J., Mason, P.H., Murphy, A.S.: Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. — Plant Cell 16: 1898–1911, 2004.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peer, W.A., Blakeslee, J.J., Yang, H., Murphy, A.S.: Seven things we think we know about auxin transport. — Mol. Plant 4: 487–504, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Peer, W.A., Brown, D.E., Tague, B.W., Muday, G.K., Taiz, L., Murphy, A.S.: Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. — Plant Physiol. 126: 536–548, 2001.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Petrášek, J., Friml, J.: Auxin transport routes in plant development. — Development 136: 2675–2688, 2009.

    Article  PubMed  Google Scholar 

  • Petrásek, J., Mravec, J., Bouchard, R., Blakeslee, J.J., Abas, M., Seifertová, D., Wisniewska, J., Tadele, Z., Kubes, M., Covanová, M., Dhonukshe, P., Skupa, P., Benková, E., Perry, L., Krecek, P., Lee, O.R., Fink, G.R., Geisler, M., Murphy, A.S., Luschnig, C., Zazímalová, E., Friml, J.: PIN proteins perform a rate-limiting function in cellular auxin efflux. — Science 312: 914–918, 2006.

    Article  PubMed  Google Scholar 

  • Sandberg, G., Tarkowski, P., Petersson, S.V., Tarkowska, D., Benfey, P., Dolezal, K., Ljung, K.: Auxin-cytokinin crosstalk and interaction with other hormones. — Biol. Plant. 49(Suppl): S26, 2005.

    Google Scholar 

  • Rea, P.A.: Plant ATP-binding cassette transporters. — Annu. Rev. Plant Biol. 58: 347–375, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Richter, S., Geldner, N., Schrader, J., Wolters, H., Stierhof, Y.D., Rios, G., Koncz, C., Robinson, D.G., Jurgens, G.: Functional diversification of closely related ARF-GEFs in protein secretion and recycling. — Nature 448: 488–492, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Rojas-Pierce, M., Titapiwatanakun, B., Sohn, E.J., Fang, F., Larive, C.K., Blakeslee, J., Cheng, Y., Cutler, S.R., Peer, W.A., Murphy, A.S., Raikhel, N.V.: Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. — Chem. Biol. 14: 1366–1376, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Santelia, D., Vincenzetti, V., Azzarello, E., Bovet, L., Fukao, Y., Düchtig, P., Mancuso, S., Martinoia, E., Geisler, M.: MDRlike ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. — FEBS Lett. 579: 5399–5406, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Sasaki, T., Ezaki, B., Matsumoto, H.: A gene encoding multidrug resistance (MDR) -like protein is induced by aluminum and inhibitors of calcium flux in wheat. — Plant Cell Physiol. 43: 177–185, 2002.

    CAS  PubMed  Google Scholar 

  • Schiefelbein, J.W.: Constructing a plant cell. The genetic control of root hair development. — Plant Physiol. 124: 1525–1531, 2000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen, C., Bai, Y., Wang, S., Zhang, S., Wu, Y., Chen, M., Jiang, D., Qi, Y.: Expression profile of PIN, AUX/LAX and PGP auxin transporter gene families in Sorghum bicolor under phytohormone and abiotic stress. — FEBS J. 277: 2954–2969, 2010.

    Article  CAS  PubMed  Google Scholar 

  • 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. nat. Acad. Sci. USA 100: 751–756, 2003.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shitan, N., Dalmas, F., Dan, K., Kato, N., Ueda, K., Sato, F., Forestier, C., Yazaki, K.: Characterization of Coptis japonica CjABCB2, an ATP-binding cassette protein involved in alkaloid transport. — Phytochemistry 9: 109–116, 2013.

    Article  Google Scholar 

  • Sidler, M., Hassa, P., Hasan, S., Ringli, C., Dudler, R.: Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. — Plant Cell 10: 1623–1636, 1998.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Swarup, R., Bennett, M.: Auxin transport: the fountain of life in plants? — Dev. Cell 5: 824–826, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Takanashi, K., Sugiyama, A., Sato, S., Tabata, S., Yazaki.: LjABCB1, an ATP-binding cassette protein specifically induced in uninfected cells of Lotus japonicus nodules. — J. Plant Physiol. 169: 322–326, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Takanashi, K., Sugiyama, A., Yazaki, K.: Involvement of auxin distribution in root nodule development of Lotus japonicus. — Planta 234:73–81, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Tanaka, H., Dhonukshe, P., Brewer, P.B., Friml, J.: Spatiotemporal asymmetric auxin distribution: a mean to coordinate plant development. — Cell Mol. Life Sci. 63: 2738–2754, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Teale, W.D., Paponov, I., Palme, K.: Auxin in action: signalling, transport and the control of plant growth and development. — Nat. Rev. mol. cell. Biol. 7: 847–859, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Terasaka, K., Blakeslee, J.J., Titapiwatanakun, B., Peer, W.A., Bandyopadhyay, A., Makam, S.N., Lee, O.R., Richards, E.L., Murphy, A.S., Sato, F., Yazaki, K.: PGP4, an ATP binding cassette P glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. — Plant Cell 17: 2922–2939, 2005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • The, O.K., Moore, I.: An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. — Nature 448: 493–496, 2007.

    Article  Google Scholar 

  • Titapiwatanakun, B., Blakeslee, J.J., Bandyopadhyay, A., Yang, H., Mravec, J., Sauer, M., Cheng, Y., Adamec, J., Nagashima, A., Geisler, M., Sakai, T., Friml, J., Peer, W.A., Murphy, A.S.: ABCB19/PGP19 stabilizes PIN1 on membrane microdomains in Arabidopsis. — Plant J. 57: 27–44, 2008.

    Article  PubMed  Google Scholar 

  • Titapiwatanakun, B., Murphy, A.S.: Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. — J. exp. Bot. 60: 1093–1107, 2008.

    Article  PubMed  Google Scholar 

  • Verrier, P.J., Bird, D., Burla, B., Dassa, E., Forestier, C., Geisler, M., Klein, M., Kolukisaoglu, U., Lee, Y., Martinoia, E., Murphy, A., Rea, P.A., Samuels, L., Schulz, B., Spalding, E.J., Yazaki, K., Theodoulou, F.L.: Plant ABC proteins — a unified nomenclature and updated inventory. — Trends Plant Sci. 13: 151–159, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Vieten, A., Sauer, M., Brewer, P.B., Friml, J.: Molecular and cellular aspects of auxin-transport-mediated development. — Trends Plant Sci. 12: 160–168, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Wang, B., Bailly, A., Zwiewka, M., Henrichs, S., Azzarello, E., Mancuso, S., Maeshima, M., Friml, J., Schulz, A., Geisler, M.: Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. — Plant Cell 25: 202–214, 2013.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang, W., Takezawa, D., Poovaiah, B.W.: A potato cDNA encoding a homologue of mammalian multidrug resistant Pglycoprotein. — Plant mol. Biol. 31: 683–687, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Wisniewska, J., Xu, J., Seifertová, D., Brewer, P.B., Ruzicka, K., Blilou, I., Rouquié, D., Benková, E., Scheres, B., Friml, J.: Polar PIN localization directs auxin flow in plants. — Science 312: 883, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Wu, G., Lewis, D.R., Spalding, E.P.: Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. — Plant Cell 19: 1826–1837, 2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu, G., Otegui, M.S., Spalding, E.P.: The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. — Plant Cell 22: 3295–3304, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang, H., Murphy, A.S.: Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. — Plant J. 59: 179–191, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Zazímalová, E., Murphy, A.S., Yang, H., Hoyerová, K., Hosek, P.: Auxin transporters — why so many? — Cold Spring Harbour Perspect Biol. 2: a001552, 2010.

    Google Scholar 

  • Zhang, L., Lu, X., Shen, Q., Chen, Y.F., Wang, T., Zhang, F.Y., Wu, S.Y., Jiang, W.M., Liu, P., Zhang, L.D., Wang, Y.Y., Tang, K.X.: Identification of putative artemisia annua ABCG transporter unigenes related to artemisinin yield following expression analysis in different plant tissues and in response to methyl jasmonate and abscisic acid treatments. — Plant mol. Biol. Rep. 30: 838–847, 2012.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, 310058, P.R. China

    Y. X. Xu, Y. Liu, S. T. Chen, L. G. Xu, Y. H. Qi & D. A. Jiang

  2. Tianmu College, Zhejiang A & F University, Zhuji, 311800, P.R. China

    X. Q. Li & S. H. Jin

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  1. Y. X. Xu
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  6. Y. H. Qi
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  7. D. A. Jiang
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  8. S. H. Jin
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Corresponding authors

Correspondence to D. A. Jiang or S. H. Jin.

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Acknowledgement: This work was financially supported by the National Science and Technology Support Plan (2012BAC09B01) and the National Natural Science Foundation of China (Nos. 31170584, 31171462, 31200525 and 31271692).

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Xu, Y.X., Liu, Y., Chen, S.T. et al. The B subfamily of plant ATP binding cassette transporters and their roles in auxin transport. Biol Plant 58, 401–410 (2014). https://doi.org/10.1007/s10535-014-0423-8

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  • DOI: https://doi.org/10.1007/s10535-014-0423-8

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