Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe

Plant Journal

Volumn 59, Issue 1, 2009, Pages 179-191

  Yang, Haibing ^a   Murphy, Angus S ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

ABCB; Auxin transporters; Expression; Functional characterization; Schizosaccharomyces pombe

Indexed keywords

ARABIDOPSIS PROTEIN; CARRIER PROTEIN; INDOLEACETIC ACID DERIVATIVE; RECOMBINANT PROTEIN;

ARABIDOPSIS; ARTICLE; CHEMICAL STRUCTURE; GENE VECTOR; GENETICS; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SCHIZOSACCHAROMYCES;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENETIC VECTORS; INDOLEACETIC ACIDS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SCHIZOSACCHAROMYCES;

ARABIDOPSIS; NICOTIANA TABACUM; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 67649460868     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03856.x     Document Type: Article

References (64)

1. Basi, G., Schmid, E. Maundrell, K. (1993) TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Genes Dev. 123, 131 136.
2. Benjamins, R. Scheres, B. (2008) Auxin: the looping star in plant development. Annu. Rev. Plant Biol. 59, 443 465. (Pubitemid 351813038)
3. Bennett, M.J., Marchant, A., Green, H.G., May, S.T. Ward, S.P. (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science, 273, 948.
4. Blakeslee, J.J., Bandyopadhyay, A., Lee, O.R. et al. (2007) Interactions among PIN-FORMED and P-Glycoprotein auxin transporters in Arabidopsis. Plant Cell, 19, 131 147. (Pubitemid 46852707)
5. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K. Scheres, B. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature, 433, 39 44. (Pubitemid 40101136)
6. Borner, G.H.H., Sherrier, D.J., Weimar, T., Michaelson, L.V., Hawkins, N.D., MacAskill, A., Napier, J.A., Beale, M.H., Lilley, K.S. Dupree, P. (2005) Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137, 104 116. (Pubitemid 43034293)
7. Bouchard, R., Bailly, A., Blakeslee, J.J. et al. (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J. Biol. Chem. 281, 30603 30612. (Pubitemid 44582116)
8. Brown, B.T. Phillips, J.N. (1982) The transport behaviour of the synthetic auxin. 2,4-dichlorophenoxyacetic acid in decapitated seedlings of sunflower (Helianthus annuus L.). Aust. J. Plant Physiol. 9, 5 13.
9. Carrier, D.J., Bakar, N.T.A., Swarup, R., Callaghan, R., Napier, R.M., Bennett, M.J. Kerr, I.D. (2008) The binding of auxin to the Arabidopsis auxin influx transporter AUX1. Plant Physiol. 148, 529 535. (Pubitemid 352847585)
10. Chang, D.T.-H., Oyang, Y.-J. Lin, J.-H. (2005) MEDock: a web server for efficient prediction of ligand binding sites based on a novel optimization algorithm. Nucleic Acids Res. 33, W233 W238.
11. Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T. Masson, P.H. (1998) The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc. Natl Acad. Sci. USA, 95, 15112 15117. (Pubitemid 29003765)
12. Cho, M., Lee, S.H. Cho, H.-T. (2007) P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell, 19, 3930 3943. (Pubitemid 351253111)
13. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881 10890.
14. Dawson, R.J.P. Locher, K.P. (2006) Structure of a bacterial multidrug ABC transporter. Nature, 443, 180 185. (Pubitemid 44387602)
15. Diana, S., Vincent, V., Elisa, A., Lucien, B., Yoichiro, F., Petra, D., Stefano, M., Enrico, M. Markus, G. (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett. 579, 5399 5406.
16. Dudler, R. Hertig, C. (1992) Structure of an mdr-like gene from Arabidopsis thaliana. Evolutionary implications. J. Biol. Chem. 267, 5882 5888.
17. Eswar, N., Marti-Renom, M.A., Webb, B., Madhusudhan, M.S., Eramian, D., Shen, M.-Y., Pieper, U. Andrej, S. (2000) Comparative protein structure modeling with MODELLER. Curr. Protoc. Bioinformatics, 15, 5.6.1 5.6.30.
18. Forsburg, S.L. (1993) Comparison of different Schizosaccharomyces pombe expression systems. Nucleic Acids Res. 21, 2955 2956.
19. Geisler, M., Blakeslee, J.J., Bouchard, R. et al. (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44, 179 194. (Pubitemid 43919880)
20. Gemmill, T.R. Trimble, R.B. (1999) Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim. Biophys. Acta, 1426, 227 237. (Pubitemid 29027941)
21. Gray, W.M., Ostin, A., Sandberg, G., Romano, C.P. Estelle, M. (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl Acad. Sci. USA, 95, 7197 7202. (Pubitemid 28278130)
22. Grossmann, G., Opekarová, M., Malinsky, J., Weig-Meckl, I. Tanner, W. (2007) Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J. 26, 1 8. (Pubitemid 46094694)
23. Grossmann, G., Malinsky, J., Stanhlschmidt, W., Loibl, M., Weig-Mekl, I., Frommer, W.B., Opekarova, M. Tanner, E. (2008) Plasma membrane microdomains regulate turnover of transport proteins in yeast. J. Cell Biol. http://www.jcb.org/cgi/doi/10.1083/jcb.200806035
24. Hayashi, K.-I., Tan, X., Zheng, N., Hatate, T., Kimura, Y., Kepinski, S. Nozaki, H. (2008) Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proc. Natl Acad. Sci. USA, 105, 5632 5637. (Pubitemid 351753914)
25. Ito, H. Gray, W.M. (2006) A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol. 142, 63 74. (Pubitemid 44412230)
26. Iwaki, T., Giga-Hama, Y. Takegawa, K. (2006) A survey of all 11 ABC transporters in fission yeast: two novel ABC transporters are required for red pigment accumulation in a Schizosaccharomyces pombe adenine biosynthetic mutant. Microbiology, 152, 2309 2321. (Pubitemid 44219640)
27. Jacobs, W.P., McCready, C.C. Osborne, D.J. (1966) Transport of the auxin 2,4-dichlorophenoxyacetic acid through absiccion zones, pulvini, and petioles of Phaseolus vulgaris. Plant Physiol. 41, 725 730.
28. Jones, A.R., Kramer, E.M., Knox, K., Swarup, R., Bennett, M.J., Lazarus, C.M., Leyser, H.M.O. Grierson, C.S. (2009) Auxin transport through non-hair cells sustains root-hair development. Nat. Cell Biol. 11, 78 84.
29. Lee, M., Choi, Y., Burla, B., Kim, Y.-Y., Jeon, B., Maeshima, M., Yoo, J.-Y., Martinoia, E. Lee, Y. (2008) The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat. Cell Biol. 10, 1217 1223.
30. Lewis, D.R., Miller, N.D., Splitt, B.L., Wu, G. Spalding, E.P. (2007) 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. (Pubitemid 47218844)
31. +-PPase AVP1 regulates auxin-mediated organ development. Science, 310, 121 125. (Pubitemid 41434551)
32. Lundstrom, K. (2007) Structural genomics and drug discovery. J. Cell Mol. Med. 11, 224 238.
33. Lupas, A., Van Dyke, M. Stock, J. (1991) Predicting coiled coils from protein sequences. Science, 252, 1162 1164. (Pubitemid 21917026)
34. Luschnig, C., Gaxiola, R.A., Grisafi, P. Fink, G.R. (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175 2187. (Pubitemid 28348041)
35. Matsuyama, A., Shirai, A., Yashiroda, Y., Kamata, A., Horinouchi, S. Yoshida, M. (2004) pDUAL., a multipurpose, multicopy vector capable of chromosomal integration in fission yeast. Yeast, 21, 1289 1305. (Pubitemid 39618520)
36. Matsuyama, A., Arai, R., Yashiroda, Y. et al. (2006) ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 24, 841 847. (Pubitemid 44086626)
37. Mongrand, S., Morel, J., Laroche, J., Claverol, S., Carde, J.-P., Hartmann, M.-A., Bonneu, M., Simon-Plas, F., Lessire, R. Bessoule, J.-J. (2004) Lipid rafts in higher plant cells: purification and characterization of triton x-100-insoluble microdomains from tobacco plasma membrane. J. Biol. Chem. 279, 36277 36286. (Pubitemid 39128964)
38. Moon, J., Zhao, Y., Dai, X., Zhang, W., Gray, W.M., Huq, E. Estelle, M. (2007) A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol. 143, 684 696. (Pubitemid 46940962)
39. Moore, B., Zhou, L., Rolland, F., Hall, Q., Cheng, W.-H., Liu, Y.-X., Hwang, I., Jones, T. Sheen, J. (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science, 300, 332 336. (Pubitemid 36433725)
40. Mravec, J., Kubes, M., Bielach, A., Gaykova, V., Petrásek, J., Skupa, P., Chand, S., Benková, E., Zazímalová, E. Friml, J. (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development, 135, 3345 3354.
41. Noh, B., Murphy, A.S. Spalding, E.P. (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell, 13, 2441 2454. (Pubitemid 33146108)
42. Peer, W. Murphy, A.S. (2007) Flavonoids and auxin transport: modulators or regulators? Trends in Plant Science, 12, 556 563. (Pubitemid 350181563)
43. Petrasek, J., Mravec, J., Bouchard, R., Blakeslee, J.J. Abas, M. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science, 312, 914 918. (Pubitemid 43727324)
44. Prusty, R., Grisafi, P. Fink, G.R. (2004) The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA, 101, 4153 4157. (Pubitemid 38405898)
45. Raven, J.A. (1975) Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol. 74, 163 172.
46. Rojas-Pierce, M., Titapiwatanakun, B., Sohn, E.J. et al. (2007) Arabidopsis P-Glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem. Biol. 14, 1366 1376. (Pubitemid 350257005)
47. Rubery, P.H. Sheldrake, A.R. (1974) Carrier-mediated auxin transport. Planta, 118, 101 121.
48. Sali, A. Blundell, T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779 815.
49. Santelia, D., Vincenzetti, V., Azzarello, E., Bovet, L., Fukao, Y., Duchtig, P., Mancuso, S., Martinoia, E. Geisler, M. (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett. 579, 5399 5406. (Pubitemid 41395162)
50. Shitan, N., Bazin, I., Dan, K., Obata, K., Kigawa, K., Ueda, K., Sato, F., Forestier, C. Yazaki, K. (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, 751 756. (Pubitemid 36126124)
51. Swarup, R., Kramer, E.M., Perry, P., Knox, K. Leyser, H.M. (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057 1065.
52. Tan, X., Calderon-Villalobos, L.I.A., Sharon, M., Zheng, C., Robinson, C.V., Estelle, M. Zheng, N. (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature, 446, 640 645. (Pubitemid 46606890)
53. Terasaka, K., Blakeslee, J.J., Titapiwatanakun, B. et al. (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell, 17, 2922 2939.
54. Titapiwatanakun, B. Murphy, A. (2008) Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J. Exp. Bot., 60, 1093 1107.
55. Titapiwatanakun, B., Blakeslee, J.J., Bandyopadhyay, A. et al. (2008) ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J. 57, 27 44.
56. Verrier, P.J., Bird, D., Burla, B. et al. (2008) Plant ABC proteins - a unified nomenclature and updated inventory. Trends Plant Sci. 13, 151 159.
57. Wachtler, V. Balasubramanian, M.K. (2006) Yeast lipid rafts? - an emerging view. Trends Cell Biol. 16, 1 4. (Pubitemid 43077088)
58. Wachtler, V., Rajagopalan, S. Balasubramanian, M.K. (2003) Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 116, 867 874. (Pubitemid 36367636)
59. Wernicke, W., Gorst, J. Milkovits, L. (1986) The ambiguous role of 2,4-dichlorophenoxyacetic acid in wheat tissue culture. Physiol. Plant. 68, 597 602.
60. Willemsen, V., Friml, J., Grebe, M., van den Toorn, A., Palme, K. Scheres, B. (2003) Cell polarity and PIN protein positioning in Arabidopsis require sterol methyltransferase1 function. Plant Cell, 15, 612 625. (Pubitemid 36339577)
61. Worrall, D., Ng, C.K.Y. Hetherington, A.M. (2003) Sphingolipids, new players in plant signaling. Trends Plant Sci. 8, 317 320. (Pubitemid 36996632)
62. Wu, G., Lewis, D.R. Spalding, E.P. (2007) 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. (Pubitemid 47218843)
63. Yang, Y., Hammes, U.Z., Taylor, C.G., Schachtman, D.P. Nielsen, E. (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123 1127. (Pubitemid 43815747)
64. Zolnerciks, J.K., Wooding, C. Linton, K.J. (2007) Evidence for a Sav1866-like architecture for the human multidrug transporter P-glycoprotein. FASEB J. 21, 3937 3948. (Pubitemid 350232351)