MODULATOR of PIN genes control steady-state levels of Arabidopsis PIN proteins

Plant Journal

Volumn 51, Issue 4, 2007, Pages 537-550

  Malenica, Nenad ^a,c   Abas, Lindy ^c   Benjamins, René ^b,c   Kitakura, Saeko ^d   Sigmund, Harald F ^c   Jun, Kim S ^c   Hauser, Marie Theres ^c   Friml, Jiří ^d   Luschnig, Christian ^c  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Auxin; Membrane protein; PIN proteins; PIN FORMED; Polar auxin transport; Post transcriptional regulation

Indexed keywords

MEMBRANE PROTEIN; PIN PROTEINS; POLAR AUXIN TRANSPORT; POST-TRANSCRIPTIONAL REGULATION;

GENES; GROWTH KINETICS; PLANTS (BOTANY); PROTEINS;

GENETIC ENGINEERING;

ARABIDOPSIS PROTEIN; CARRIER PROTEIN; HYBRID PROTEIN; INDOLEACETIC ACID DERIVATIVE; PIN1 PROTEIN, ARABIDOPSIS; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; GENE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; MUTATION; NORTHERN BLOTTING; PLANT; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; BLOTTING, NORTHERN; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; IMMUNOHISTOCHEMISTRY; INDOLEACETIC ACIDS; MEMBRANE TRANSPORT PROTEINS; MUTATION; PLANT ROOTS; PLANT SHOOTS; RECOMBINANT FUSION PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 34547820875     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03158.x     Document Type: Article

References (68)

1. Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wisniewska, J., Moulinier-Anzola, J. C., Sieberer, T., Friml, J. Luschnig, C. (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nature Cell Biol. 8, 249 256.
2. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y. S., Amasino, R. Scheres, B. (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell, 119, 109 120.
3. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. Struhl, K. (1987) Current Protocols in Molecular Biology. New York : John Wiley/Greene.
4. Bell, C. J. Ecker, J. R. (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics, 19, 137 144.
5. Benjamins, R., Malenica, N. Luschnig, C. (2005) Regulating the regulator: the control of auxin transport. Bioessays, 27, 1246 1255.
6. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jürgens, G. Friml, J. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591 602.
7. Bennett, S. R. M., Alvarez, J., Bossinger, G. Smyth, D. R. (1995) Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J. 8, 505 520.
8. Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., Walker, A.R., Schulz, B. Feldmann, K.A. (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science, 273, 948 950.
9. Bennett, T., Sieberer, T., Willett, B., Booker, J., Luschnig, C. Leyser, O. (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol. 16, 553 563.
10. Blakeslee, J.J., Peer, W.A. Murphy, A.S. (2005) Auxin transport. Curr. Opin. Plant Biol. 8, 494 500.
11. 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.
12. 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.
13. Bonifacino, J. S. Traub, L. M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395 447.
14. Casimiro, I., Marchant, A., Bhalerao, R.P. et al. (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell, 13, 843 852.
15. 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.
16. Connolly, E.L., Fett, J.P. Guerinot, M.L. (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell, 14, 1347 1357.
17. Davies, P.J. (ed 2004) Plant hormones : Biosynthesis, Signal Transduction, Action! Dordrecht, Kluwer Academic Publishers : The Netherlands.
18. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D., Mravec, J., Stierhof, Y.-D. Friml, J. (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol., 17, 520 527.
19. Friml, J., Benkova, E., Mayer, U., Palme, K. Muster, G. (2003a) Automated whole mount localisation techniques for plant seedlings. Plant J. 34, 115 124.
20. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R. Jürgens, G. (2003b) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature, 426, 147 153.
21. Friml, J., Yang, X., Michniewicz, M. et al. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science, 306, 862 865.
22. 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.
23. Geldner, N., Friml, J., Stierhof, Y.D., Jurgens, G. Palme, K. (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature, 413, 425 428.
24. Gil, P., Dewey, E., Friml, J., Zhao, Y., Snowden, K.C., Putterill, J., Palme, K., Estelle, M. Chory, J. (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15, 1985 1997.
25. Haughn, G.W. Somerville, C.R. (1986) Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204, 430 434.
26. Hein, C., Springael, J.Y., Volland, C., Haguenauer-Tsapis, R. Andre, B. (1995) NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18, 77 87.
27. Hicke, L. Dunn, R. (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141 172.
28. Hicke, L. Riezman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell, 84, 277 287.
29. Horak, J. Wolf, D.H. (1997) Catabolite inactivation of the galactose transporter in the yeast Saccharomyces cerevisiae: ubiquitination, endocytosis, and degradation in the vacuole. J. Bacteriol. 179, 1541 1549.
30. Jaillais, Y., Fobis-Loisy, I., Miege, C., Rollin, C. Gaude, T. (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature, 443, 106 109.
31. Kimbrough, J.M., Salinas-Mondragon, R., Boss, W.F., Brown, C.S. Sederoff, H.W. (2004) The fast and transient transcriptional network of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiol. 136, 2790 2805.
32. Li, L., Xu, J., Xu, Z.H. Xue, H.W. (2005) Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell, 17, 2738 2753.
33. Ljung, K., Hull, A.K., Celenza, J., Yamada, M., Estelle, M., Normanly, J. Sandberg, G. (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell, 17, 1090 1104.
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.
35. Meijer, H.A., Dictus, W.J., Keuning, E.D. Thomas, A.A. (2000) Translational control of the Xenopus laevis connexin-41 5'-untranslated region by three upstream open reading frames. J. Biol. Chem. 275, 30787 30793.
36. Meusser, B., Hirsch, C., Jarosch, E. Sommer, T. (2005) ERAD: the long road to destruction. Nature Cell Biol. 7, 766 772.
37. Morris, D.A., Friml, J. Zazimalova, E. (2004) Auxin transport. In Plant Hormones: Biosynthesis, Signal Transduction, Action! (Davies, P.J., ed). Dordrecht, The Netherlands : Kluwer Academic Publishers, pp. 437 470.
38. Müller, A., Guan, C., Gälweiler, L., Tanzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E. Palme, K. (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903 6911.
39. Müller, J., Piffanelli, P., Devoto, A., Miklis, M., Elliott, C., Ortmann, B., Schulze-Lefert, P. Panstruga, R. (2005) Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell, 17, 149 163.
40. Murphy, A.S., Bandyopadhyay, A., Holstein, S.E. Peer, W.A. (2005) Endocytotic cycling of PM proteins. Annu. Rev. Plant Biol. 56, 221 251.
41. Myers, S.J., Dingledine, R. Borges, K. (1999) Genetic regulation of glutamate receptor ion channels. Annu. Rev. Pharmacol. Toxicol. 39, 221 241.
42. Myers, S.J., Huang, Y., Genetta, T. Dingledine, R. (2004) Inhibition of glutamate receptor 2 translation by a polymorphic repeat sequence in the 5'-untranslated leaders. J. Neurosci. 24, 3489 3499.
43. Okada, K., Ueda, J., Komaki, M.K., Bell, C.J. Shimura, Y. (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell, 3, 677 684.
44. Paciorek, T., Zazimalova, E., Ruthardt, N. et al. (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature, 435, 1251 1256.
45. Paponov, I.A., Teale, W.D., Trebar, M., Blilou, I. Palme, K. (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci. 10, 170 177.
46. Peer, W.A., Bandyopadhyay, A., Blakeslee, J.J., Makam, S.N., Chen, R.J., Masson, P.H. Murphy, A.S. (2004) 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.
47. Petrasek, J., Cerna, A., Schwarzerova, K., Elckner, M., Morris, D.A. Zazimalova, E. (2003) Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiol. 131, 254 263.
48. Petrasek, J., Mravec, J., Bouchard, R. et al. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science, 312, 914 918.
49. Raiborg, C., Rusten, T.E. Stenmark, H. (2003) Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15, 446 455.
50. Robatzek, S., Chinchilla, D. Boller, T. (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537 542.
51. Roman, G., Lubarsky, B., Kieber, J.J., Rothenberg, M. Ecker, J.R. (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics, 139, 1393 1409.
52. Roth, A.F., Sullivan, D.M. Davis, N.G. (1998) A large PEST-like sequence directs the ubiquitination, endocytosis, and vacuolar degradation of the yeast a-factor receptor. J. Cell Biol. 142, 949 961.
53. Sabatini, S., Beis, D., Wolkenfelt, H. et al. (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell, 99, 463 472.
54. Sauer, M., Balla, J., Luschnig, C., Wisniewska, J., Reinohl, V., Friml, J. Benkova, E. (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 20, 2902 2911.
55. Sieberer, T., Seifert, G.J., Hauser, M.T., Grisafi, P., Fink, G.R. Luschnig, C. (2000) Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr. Biol. 10, 1595 1598.
56. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S., Gälweiler, L., Palme, K. Jürgens, G. (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science, 286, 316 318.
57. Takano, J., Miwa, K., Yuan, L., von Wiren, N. Fujiwara, T. (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl Acad. Sci. USA, 102, 12276 12281.
58. Talbert, P.B., Adler, H.T., Parks, D.W. Comai, L. (1995) The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development, 121, 2723 2735.
59. Tanaka, H., Dhonukshe, P. Friml, J. (2006) Spatio-temporal asymmetric auxin distribution: means to coordinate plant development. Cell. Mol. Life Sci. 63, 2738 2754.
60. Terasaka, K., Blakeslee, J.J. Titapiwatanakun, et al. (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell, 17, 2922 2939.
61. Utsuno, K., Shikanai, T., Yamada, Y. Hashimoto, T. (1998) Agr, an agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol. 39, 1111 1118.
62. Vieten, A., Vanneste, S., Wisniewska, J., Benkova, E., Benjamins, R., Beeckman, T., Luschnig, C. Friml, J. (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development, 132, 4521 4531.
63. Weigel, D., Ahn, J.H., Blazquez, M.A. et al. (2000) Activation tagging in Arabidopsis. Plant Physiol. 122, 1003 1013.
64. Wisniewska, J., Xu, J., Seifertova, D., Brewer, P.B., Ruzicka, K., Blilou, I., Rouquie, D., Benkova, E., Scheres, B. Friml, J. (2006) Polar PIN localization directs auxin flow in plants. Science, 312, 883.
65. Wood, M.W., VanDongen, H.M. VanDongen, A.M. (1996) The 5'-untranslated region of the N-methyl-d-aspartate receptor NR2A subunit controls efficiency of translation. J. Biol. Chem. 271, 8115 8120.
66. Xu, J., Hofhuis, H., Heidstra, R., Sauer, M., Friml, J. Scheres, B. (2006) A molecular framework for plant regeneration. Science, 311, 385 388.
67. 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.
68. Zhong, R. Ye, Z.H. (2001) Alteration of auxin polar transport in the Arabidopsis ifl1 mutants. Plant Physiol. 126, 549 563.