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••] provide comprehensive and comparative up-to-date reviews reflecting the views of four leading labs on the current state of the polar auxin transport field.
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The first paper in a series of reports that demonstrate auxin efflux carrier activity of PGP-type proteins. Arabidopsis PGP1 is convincingly shown to confer enhanced auxin efflux from plant protoplasts as well as from yeast and human HeLa cells.
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Geisler M., Blakeslee J.J., Bouchard R., Lee O.R., Vincenzetti V., Bandyopadhyay A., Titapiwatanakun B., Peer W.A., Bailly A., Richards E.L., et al. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44 (2005) 179-194. The first paper in a series of reports that demonstrate auxin efflux carrier activity of PGP-type proteins. Arabidopsis PGP1 is convincingly shown to confer enhanced auxin efflux from plant protoplasts as well as from yeast and human HeLa cells.
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Geisler, M.1
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The authors map the tissues that mediate auxin responses and AUX1 influx carrier-dependent auxin transport during Arabidopsis root gravitropism. Tissue-specific mapping of AUX1-mediated transport in lateral root cap and epidermal cells is combined with computational modelling of the resulting auxin gradient that is proposed to drive the differential expansion of epidermal cells during root gravitropism.
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Swarup R., Kramer E.M., Perry P., Knox K., Leyser H.M., Haseloff J., Beemster G.T., Bhalerao R., and Bennett M.J. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 7 (2005) 1057-1065. The authors map the tissues that mediate auxin responses and AUX1 influx carrier-dependent auxin transport during Arabidopsis root gravitropism. Tissue-specific mapping of AUX1-mediated transport in lateral root cap and epidermal cells is combined with computational modelling of the resulting auxin gradient that is proposed to drive the differential expansion of epidermal cells during root gravitropism.
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This study characterises the AUX1 protein as a bona fide auxin influx carrier by expression in a heterologous Xenopus oocyte system. AUX1 transports IAA in a proton-driven anionic symport system with substrate and pharmacological preferences matching those previously attributed to 'the influx carrier' in plants. Different AUX1 mutant forms expressed in Xenopus reflect the differences in allele strength observed in Arabidopsis concerning their auxin uptake properties in the heterologous system.
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Yang Y., Hammes U.Z., Taylor C.G., Schachtman D.P., and Nielsen E. High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16 (2006) 1123-1127. This study characterises the AUX1 protein as a bona fide auxin influx carrier by expression in a heterologous Xenopus oocyte system. AUX1 transports IAA in a proton-driven anionic symport system with substrate and pharmacological preferences matching those previously attributed to 'the influx carrier' in plants. Different AUX1 mutant forms expressed in Xenopus reflect the differences in allele strength observed in Arabidopsis concerning their auxin uptake properties in the heterologous system.
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Yang, Y.1
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Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis
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••] this study demonstrates that PIN1 protein does not individually act as an auxin efflux facilitator but enhances PGP1 and PGP19 efflux facilitator activities in human and yeast heterologous systems. Genetic and direct interactions between PIN and PGP proteins are reported, suggesting a complex network of regulation for auxin efflux carrier complexes that open the door for further investigations. Confirms AUX1 auxin influx carrier activity in an additional heterologous system.
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••] this study demonstrates that PIN1 protein does not individually act as an auxin efflux facilitator but enhances PGP1 and PGP19 efflux facilitator activities in human and yeast heterologous systems. Genetic and direct interactions between PIN and PGP proteins are reported, suggesting a complex network of regulation for auxin efflux carrier complexes that open the door for further investigations. Confirms AUX1 auxin influx carrier activity in an additional heterologous system.
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Plant Cell
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Blakeslee, J.J.1
Bandyopadhyay, A.2
Lee, O.R.3
Mravec, J.4
Titapiwatanakun, B.5
Sauer, M.6
Makam, S.N.7
Cheng, Y.8
Bouchard, R.9
Adamec, J.10
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16
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31844449045
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PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots
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Describes the isolation and phenotypic characterisation of pgp4 mutants, expression of the PGP4 gene, localisation of the protein and auxin transport activities of PGP4. It remains open as to whether PGP4 acts as an auxin influx or efflux carrier in Arabidopsis.
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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., et al. PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17 (2005) 2922-2939. Describes the isolation and phenotypic characterisation of pgp4 mutants, expression of the PGP4 gene, localisation of the protein and auxin transport activities of PGP4. It remains open as to whether PGP4 acts as an auxin influx or efflux carrier in Arabidopsis.
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Plant Cell
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Terasaka, K.1
Blakeslee, J.J.2
Titapiwatanakun, B.3
Peer, W.A.4
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Makam, S.N.6
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Sato, F.10
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17
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33750072606
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Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins
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Reports on the auxin efflux activity of PGP19 and its modulation by the immunophilin TWISTED DWARF1.
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Bouchard R., Bailly A., Blakeslee J.J., Oehring S.C., Vincenzetti V., Lee O.R., Paponov I., Palme K., Mancuso S., Murphy A.S., et al. Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 281 (2006) 30603-30612. Reports on the auxin efflux activity of PGP19 and its modulation by the immunophilin TWISTED DWARF1.
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J Biol Chem
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Bouchard, R.1
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Lee, O.R.6
Paponov, I.7
Palme, K.8
Mancuso, S.9
Murphy, A.S.10
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18
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33646547313
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PIN proteins perform a rate-limiting function in cellular auxin efflux
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Provides the long-awaited proof that some members of the PIN protein family (PIN2 and PIN7) can directly and individually confer cellular IAA efflux activity, when expressed in heterologous human HeLa and yeast systems.
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Petrasek J., Mravec J., Bouchard R., Blakeslee J.J., Abas M., Seifertova D., Wisniewska J., Tadele Z., Kubes M., Covanova M., et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312 (2006) 914-918. Provides the long-awaited proof that some members of the PIN protein family (PIN2 and PIN7) can directly and individually confer cellular IAA efflux activity, when expressed in heterologous human HeLa and yeast systems.
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Science
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Petrasek, J.1
Mravec, J.2
Bouchard, R.3
Blakeslee, J.J.4
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Seifertova, D.6
Wisniewska, J.7
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19
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33646562869
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Polar PIN localisation directs auxin flow in plants
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Neatly demonstrates that the apical localisation of PIN2 in epidermal cells is a specific directional requirement for root gravitropism and auxin-response distribution, and that the information for polar PIN2 localisation resides in its protein sequences.
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Wisniewska J., Xu J., Seifertova D., Brewer P.B., Ruzicka K., Blilou I., Rouquie D., Benkova E., Scheres B., and Friml J. Polar PIN localisation directs auxin flow in plants. Science 312 (2006) 883. Neatly demonstrates that the apical localisation of PIN2 in epidermal cells is a specific directional requirement for root gravitropism and auxin-response distribution, and that the information for polar PIN2 localisation resides in its protein sequences.
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Science
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Wisniewska, J.1
Xu, J.2
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Brewer, P.B.4
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Blilou, I.6
Rouquie, D.7
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Friml, J.10
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Auxin inhibits endocytosis and promotes its own efflux from cells
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This is the first report demonstrating that externally applied or endogenously overproduced auxin can inhibit endocytosis of a variety of proteins including PIN1 and PIN2. Externally applied auxin is shown to promote auxin efflux from cell cultures. The distribution of an auxin-response reporter, an endocytic tracer and the PIN2 protein in root tips suggest that an intrinsic mechanism by which auxin regulates its own efflux and carrier internalisation may be operational during gravistimulation of Arabidopsis roots.
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Paciorek T., Zazimalova E., Ruthardt N., Petrasek J., Stierhof Y.D., Kleine-Vehn J., Morris D.A., Emans N., Jürgens G., Geldner N., et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435 (2005) 1251-1256. This is the first report demonstrating that externally applied or endogenously overproduced auxin can inhibit endocytosis of a variety of proteins including PIN1 and PIN2. Externally applied auxin is shown to promote auxin efflux from cell cultures. The distribution of an auxin-response reporter, an endocytic tracer and the PIN2 protein in root tips suggest that an intrinsic mechanism by which auxin regulates its own efflux and carrier internalisation may be operational during gravistimulation of Arabidopsis roots.
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Nature
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Paciorek, T.1
Zazimalova, E.2
Ruthardt, N.3
Petrasek, J.4
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Kleine-Vehn, J.6
Morris, D.A.7
Emans, N.8
Jürgens, G.9
Geldner, N.10
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21
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33947152773
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Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis
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This is the first report to link PIN auxin efflux carrier internalisation to clathrin-mediated endocytosis.
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Dhonukshe P., Aniento F., Hwang I., Robinson D.G., Mravec J., Stierhof Y.D., and Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17 (2007) 520-527. This is the first report to link PIN auxin efflux carrier internalisation to clathrin-mediated endocytosis.
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Curr Biol
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Dhonukshe, P.1
Aniento, F.2
Hwang, I.3
Robinson, D.G.4
Mravec, J.5
Stierhof, Y.D.6
Friml, J.7
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22
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34249821938
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Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response
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This is the first experimental evidence functionally linking phospholipid signalling to auxin efflux carrier internalisation. Demonstrates that phospholipase Dζ2 and phosphatidic acid stimulate PIN2 endocytosis while mutants lacking PLDζ2 reduce PIN2 endocytosis.
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Li G., and Xue H.W. Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19 (2007) 281-295. This is the first experimental evidence functionally linking phospholipid signalling to auxin efflux carrier internalisation. Demonstrates that phospholipase Dζ2 and phosphatidic acid stimulate PIN2 endocytosis while mutants lacking PLDζ2 reduce PIN2 endocytosis.
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(2007)
Plant Cell
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Li, G.1
Xue, H.W.2
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23
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33748423078
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AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis
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This study identifies SNX1-positive endosomes as wortmannin-sensitive potential pre-vacuolar compartments involved in PIN2 but not PIN1 auxin efflux carrier trafficking. Furthermore, the snx1 mutant phenotype shows that SNX1 is required for Arabidopsis root gravitropism, while it remains open whether PIN2 localisation or sorting directly depends on SNX1 function.
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Jaillais Y., Fobis-Loisy I., Miege C., Rollin C., and Gaude T. AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443 (2006) 106-109. This study identifies SNX1-positive endosomes as wortmannin-sensitive potential pre-vacuolar compartments involved in PIN2 but not PIN1 auxin efflux carrier trafficking. Furthermore, the snx1 mutant phenotype shows that SNX1 is required for Arabidopsis root gravitropism, while it remains open whether PIN2 localisation or sorting directly depends on SNX1 function.
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Nature
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Jaillais, Y.1
Fobis-Loisy, I.2
Miege, C.3
Rollin, C.4
Gaude, T.5
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24
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34250643053
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The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5
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Characterises the function of the Arabidopsis ESCRT associated AAA ATPase SKD1 by dominant-negative approaches and localises it to the cytosol as well as MVBs/PVCs. Additionally, this study provides electron microscopic evidence for the localisation of three Rab5-like GTPases to MVBs/PVCs that may serve as the foundation for analyses of trafficking of polarly localised proteins via these compartments.
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Haas T.J., Sliwinski M.K., Martinez D.E., Preuss M., Ebine K., Ueda T., Nielsen E., Odorizzi G., and Otegui M.S. The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19 (2007) 1295-1312. Characterises the function of the Arabidopsis ESCRT associated AAA ATPase SKD1 by dominant-negative approaches and localises it to the cytosol as well as MVBs/PVCs. Additionally, this study provides electron microscopic evidence for the localisation of three Rab5-like GTPases to MVBs/PVCs that may serve as the foundation for analyses of trafficking of polarly localised proteins via these compartments.
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(2007)
Plant Cell
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Haas, T.J.1
Sliwinski, M.K.2
Martinez, D.E.3
Preuss, M.4
Ebine, K.5
Ueda, T.6
Nielsen, E.7
Odorizzi, G.8
Otegui, M.S.9
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25
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33644785898
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Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism
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Demonstrates that the PIN2 protein becomes polyubiquitinated and degraded via a proteasomal pathway and suggests that the control of PIN2 stability is critical for root gravitropism, since a mis-localised and stabilised PIN2 mutant form is defective in this process.
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Abas L., Benjamins R., Malenica N., Paciorek T., Wisniewska J., Moulinier-Anzola J.C., Sieberer T., Friml J., and Luschnig C. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8 (2006) 249-256. Demonstrates that the PIN2 protein becomes polyubiquitinated and degraded via a proteasomal pathway and suggests that the control of PIN2 stability is critical for root gravitropism, since a mis-localised and stabilised PIN2 mutant form is defective in this process.
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(2006)
Nat Cell Biol
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Abas, L.1
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Friml, J.8
Luschnig, C.9
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26
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33644872913
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Exploring the ESCRTing machinery in eukaryotes
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This review provides the first and very informative survey of which ESCRT components are present in plant genomes (Arabidopsis and rice) and compares them with ESCRT components present in animal model organisms.
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Winter V., and Hauser M.T. Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci 11 (2006) 115-123. This review provides the first and very informative survey of which ESCRT components are present in plant genomes (Arabidopsis and rice) and compares them with ESCRT components present in animal model organisms.
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Trends Plant Sci
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Winter, V.1
Hauser, M.T.2
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27
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The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis
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Provides the first functional genetic, molecular and biochemical characterisation of an ESCRT component required for cytokinesis starting from analyses of an Arabidopsis trichome mutant.
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Spitzer C., Schellmann S., Sabovljevic A., Shahriari M., Keshavaiah C., Bechtold N., Herzog M., Müller S., Hanisch F.G., and Hülskamp M. The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133 (2006) 4679-4689. Provides the first functional genetic, molecular and biochemical characterisation of an ESCRT component required for cytokinesis starting from analyses of an Arabidopsis trichome mutant.
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(2006)
Development
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Spitzer, C.1
Schellmann, S.2
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Shahriari, M.4
Keshavaiah, C.5
Bechtold, N.6
Herzog, M.7
Müller, S.8
Hanisch, F.G.9
Hülskamp, M.10
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28
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33646778800
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The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins
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Employs quantitative co-localisation analysis to map a subpopulation of PIN protein(s) to the Golgi apparatus and demonstrates that the microtubule cytoskeleton contributes to polar PIN localisation.
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Boutte Y., Crosnier M.T., Carraro N., Traas J., and Satiat-Jeunemaitre B. The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J Cell Sci 119 (2006) 1255-1265. Employs quantitative co-localisation analysis to map a subpopulation of PIN protein(s) to the Golgi apparatus and demonstrates that the microtubule cytoskeleton contributes to polar PIN localisation.
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(2006)
J Cell Sci
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Boutte, Y.1
Crosnier, M.T.2
Carraro, N.3
Traas, J.4
Satiat-Jeunemaitre, B.5
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29
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33845784713
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Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1
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••]). Addresses AUX1 dynamics at the PM and reports that sterol composition modulates the intracellular accumulation of AUX1.
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••]). Addresses AUX1 dynamics at the PM and reports that sterol composition modulates the intracellular accumulation of AUX1.
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(2006)
Plant Cell
, vol.18
, pp. 3171-3181
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Kleine-Vehn, J.1
Dhonukshe, P.2
Swarup, R.3
Bennett, M.4
Friml, J.5
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33744468228
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AXR4 is required for localisation of the auxin influx facilitator AUX1
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Positional cloning of the AXR4 gene identifies the AXR4 protein that is demonstrated to localise to the ER and to be required for the PM localisation of AUX1 but not the PIN1 and PIN2 proteins. Provides the entry to study auxin influx carrier transport to the PM.
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Dharmasiri S., Swarup R., Mockaitis K., Dharmasiri N., Singh S.K., Kowalchyk M., Marchant A., Mills S., Sandberg G., Bennett M.J., et al. AXR4 is required for localisation of the auxin influx facilitator AUX1. Science 312 (2006) 1218-1220. Positional cloning of the AXR4 gene identifies the AXR4 protein that is demonstrated to localise to the ER and to be required for the PM localisation of AUX1 but not the PIN1 and PIN2 proteins. Provides the entry to study auxin influx carrier transport to the PM.
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(2006)
Science
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Dharmasiri, S.1
Swarup, R.2
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Dharmasiri, N.4
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Reports that an auxin gradient can provide directional information to coordinate the polarity of root hair positioning in the plane of the epidermal layer. The auxin gradient acts downstream of and is dependent on AUX1, EIN2 and GNOM function but acts upstream of coordinate polar localisation of ROP to the hair initiation site.
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Provides the first loss-of-function evidence that a plant Rho GDP dissociation inhibitor (RhoGDI) contributes to local execution of cell polarity. Arabidopsis RhoGDI1/SCN1 is shown to restrict the spatial polar localisation of ROP2 and root hairs to a single site along the trichoblast.
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Carol R.J., Takeda S., Linstead P., Durrant M.C., Kakesova H., Derbyshire P., Drea S., Zarsky V., and Dolan L. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438 (2005) 1013-1016. Provides the first loss-of-function evidence that a plant Rho GDP dissociation inhibitor (RhoGDI) contributes to local execution of cell polarity. Arabidopsis RhoGDI1/SCN1 is shown to restrict the spatial polar localisation of ROP2 and root hairs to a single site along the trichoblast.
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••] this study shows that overexpression of tobacco Nt-RhoGDI2 in tobacco pollen tubes interferes with polar pollen tube growth.
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••] this study shows that overexpression of tobacco Nt-RhoGDI2 in tobacco pollen tubes interferes with polar pollen tube growth.
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Demonstrates that auxin can act as a polarising factor on PIN protein polarity in Arabidopsis roots and in pea epicotyls, revisiting Sachs's [2] wounding studies in pea with molecular polarity markers. The studies on Arabidopsis roots further demonstrate that auxin-induced polar PIN protein relocation depends on ARF7 and ARF19 function. On the basis of these data a feedback regulation of PIN polarity is proposed that involves AUX/IAA-ARF function.
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Precise mapping of leaf vascular formation from the onset of leaf pre-procambium initiation using PIN1-GFP as a polarity marker reveals the earliest known events during auxin-transport-dependent initiation of vascular tissue polarity and patterning to occur in epidermal tissues. A combination of pharmacological and genetic studies demonstrates that early epidermal PIN1 expression domain dynamics and coordinate PIN1 polarisation are self-organising, auxin-transport-dependent events. These result in epidermal 'auxin drainage' to convergence points of auxin accumulation that define the initiation points of major vein formation. This mechanism is postulated to underlie major leaf-vein positioning and phyllotactic patterning in plants.
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Scarpella E., Marcos D., Friml J., and Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes Dev 20 (2006) 1015-1027. Precise mapping of leaf vascular formation from the onset of leaf pre-procambium initiation using PIN1-GFP as a polarity marker reveals the earliest known events during auxin-transport-dependent initiation of vascular tissue polarity and patterning to occur in epidermal tissues. A combination of pharmacological and genetic studies demonstrates that early epidermal PIN1 expression domain dynamics and coordinate PIN1 polarisation are self-organising, auxin-transport-dependent events. These result in epidermal 'auxin drainage' to convergence points of auxin accumulation that define the initiation points of major vein formation. This mechanism is postulated to underlie major leaf-vein positioning and phyllotactic patterning in plants.
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Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes
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Highlights a potential mechanism by which cell polarity may be locally executed in tobacco pollen tubes. Transient overexpressions studies of RhoGAP1 demonstrate its localisation at the flanks of pollen tubes, suggesting a local mechanism by which apical activity of the small GTPase RAC5 may be prevented to spread to the flanks of the pollen tube.
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Klahre U., and Kost B. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 18 (2006) 3033-3046. Highlights a potential mechanism by which cell polarity may be locally executed in tobacco pollen tubes. Transient overexpressions studies of RhoGAP1 demonstrate its localisation at the flanks of pollen tubes, suggesting a local mechanism by which apical activity of the small GTPase RAC5 may be prevented to spread to the flanks of the pollen tube.
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Elegant laser ablation experiments demonstrate the requirement of the cell type specifying and patterning genes SCARECROW and SHORTROOT for re-establishment of PIN4 protein polarity during regeneration of root tissue relative to an auxin-response gradient.
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Xu J., Hofhuis H., Heidstra R., Sauer M., Friml J., and Scheres B. A molecular framework for plant regeneration. Science 311 (2006) 385-388. Elegant laser ablation experiments demonstrate the requirement of the cell type specifying and patterning genes SCARECROW and SHORTROOT for re-establishment of PIN4 protein polarity during regeneration of root tissue relative to an auxin-response gradient.
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A plausible model of phyllotaxis
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•]. Similarly, future approaches that specifically integrate experimental data on cell polarisation with its computational modelling may increase understanding of mechanisms driving auxin-dependent cell and tissue polarity.
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•]. Similarly, future approaches that specifically integrate experimental data on cell polarisation with its computational modelling may increase understanding of mechanisms driving auxin-dependent cell and tissue polarity.
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