The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level

Development

Volumn 134, Issue 21, 2007, Pages 3849-3859

  Furutani, Masahiko ^a   Kajiwara, Takahito ^a   Kato, Takehide ^a   Treml, Birgit S ^b   Stockum, Christine ^b   Torres Ruiz, Ramón A ^b   Tasaka, Masao ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Arabidopsis thaliana; NPH3; Organ development; PID; PIN1; Polar auxin transport

Indexed keywords

AUXIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; MUTANT PROTEIN; NONPHOTOTROPIC HYPOCOTYL 3 PROTEIN; PHYTOHORMONE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; CELL MEMBRANE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; COTYLEDON; EMBRYO CELL; ENDOSOME; ENHANCER REGION; MERISTEM; MUTANT; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PHOTOTROPISM; PLANT DEVELOPMENT; PLANT GROWTH; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN FAMILY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PHOTOTROPISM; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS THALIANA;

EID: 36548999323     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.009654     Document Type: Article

References (64)

1. Abe, M., Takahashi, T. and Komeda, Y. (2001). Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. Plant J. 26, 487-494.
2. Aida, M., Ishida, T., Fukaki, H., Fujisawa, H. and Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9, 841-857.
3. Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., Stevenson, D. K., Zimmerman, J., Barajas, P., Cheuk, R. et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
4. Ballas, N., Wong, L. M. and Theologis, A. (1993). Identification of the auxin-responsive element, AuxRE, in the primary indoleacetic acid-inducible gene, PS-IAA4I5, of pea (Pisum sativum). J. Mol. Biol. 4, 580-596.
5. Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. and Offringa, R. (2001). The PINOID protein kinase regulates organ development in [i Arabidopsis by enhancing polar auxin transport. Development 128, 4057-4067.
6. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jürgens, G. and 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. and Smyth, D. R. (1995). Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J. 8, 505-520.
8. Blakeslee, J. J., Bandyopadhway, A., Peer, W. A., Makam, S. N. and Murphy, A. S. (2004). Relocalization of the PIN1 auxin efflux facilitator plays a role in phototropic response. Plant Physiol 134, 28-31.
9. Bögre, L., Ökresz, L., Henriques, R. and Anthony, R. G. (2003). Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci. 8, 424-431.
10. Briggs, W. R. and Christie, J. M. (2002). Phototropins 1 and 2, versatile plant blue-light receptors. Trends Plant Sci. 7, 204-210.
11. Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A. and Tsien, R. Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877-7882.
12. Chen, R., Hilson, R, Sedbrook, J., Rosen, E., Caspar, T. and 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.
13. Christensen, S. K., Dagenais, N., Chory, J. and Weigel, D. (2000). Regulation of auxin response by the protein kinase PINOID. Cell 100, 469-478.
14. Clough, S. J. and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
15. Friml, J., Wisniewska, J., Benková, E., Mendgen, K. and Palme, K. (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
16. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R. and Jürgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147-153.
17. Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O., Benjamins, R., Ouwerkerk, P. B., Ljung, K., Sandberg, G. et al. (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862-865.
18. Fukaki, H., Fujisawa, H. and Tasaka, M. (1996). Gravitropic response of inflorescence stems in Arabidopsis thaliana. Plant Physiol. 110, 933-943.
19. Furutani, M., Vernoux, T., Traas, J., Kato, T., Tasaka, M. and Aida, M. (2004). PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131, 5021-5030.
20. Gälweiler, L., Guan, C., Muller, A., Wisman, E., Mendgen, K., Yephremov, A. and Palme, K. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226-2230.
21. Geisler, M., Kolukisaoglu, H. U., Bouchard, R., Billion, K., Berger, J., Saal, B., Frangne, N., Koncz-Kalman, Z., Koncz, C., Dudler, R. et al. (2003) 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.
22. 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. (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., Jürgens, G. and Palme, K. (2001). Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425-428.
24. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A. and Jürgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230.
25. Gil, P., Dewey, E., Friml, J., Zhao, Y., Snowden, K. C., Putterill, J., Palme, K., Estelle, M. and Chory, J. (2001). BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15, 1985-1997.
26. Hadfi, K., Speth, V. and Neuhaus, G. (1998). Auxin-induced developmental patterns in Brassica juncea embryos. Development 125, 879-887.
27. Haga, K., Takano, M., Neumann, R. and Iino, M. (2005) The Rice COLEOPTILE PHOTOTROPISM1 gene encoding an ortholog of Arabidopsis NPH3 is required for phototropism of coleoptiles and lateral translocation of auxin. Plant Cell 17, 103-115.
28. Heisler, M. G., Ohno, C., Das, P., Sieber, P., Reddy, G. V., Long, J. A. and Meyerowitz, E. M. (2005). Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 21, 1899-1911.
29. Huala, E., Oeller, P. W., Liscum, E., Han, I. S., Larsen, E. and Briggs, W. R. (1997). Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278, 2120-2123.
30. Inada, S., Ohgishi, M., Mayama, T., Okada, K. and Sakai, T. (2004). RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell 16, 887-896.
31. Ishida, T., Aida, M., Takada, S. and Tasaka, M. (2000). Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana. Plant Cell Physiol. 41, 60-67.
32. Jürgens, G. and Mayer, U. (1994). Arabidopsis. In Embryos: Colour Atlas of Development (ed J. Bard), pp. 7-21. London: Wolfe.
33. Kimura, M. and Kagawa, T. (2006) Phototropin and light-signaling in phototropism. Curr. Opin. Plant Biol. 9, 503-508.
34. Lee, S. H. and Cho, H. T. (2006). PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. Plant Cell 18, 1604-1616.
35. Lin, R. and Wang, H. (2005). 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.
36. Liscum, E. and Briggs, W. R. (1996). Mutations of Arabidopsis in potential transduction and response components of the phototropic signaling pathway. Plant Physiol. 112, 291-296.
37. Liu, C., Xu, Z. and Chua, N. H. (1993). Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5, 621-630.
38. Lohmann, J. U., Hong, R. L., Hobe, M., Busch, M. A., Parcy, F., Simon, R. and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105, 793-803.
39. Lu, P., Porat, R., Nadeau, J. A. and O'Neill, S. D. (1996). Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8, 2155-2168.
40. Luschnig, C., Gaxiola, R. A., Grisafi, P. and 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.
41. Motchoulski, A. and Liscum, E. (1999). Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science 286, 961-964.
42. Muller, A., Guan, C., Galweiler, L., Tanzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E. and Palme, K. (1998). AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903-6911.
43. Multani, D. S., Briggs, S. P., Chamberlin, M. A., Blakeslee, J. J., Murphy, A. S. and Johal, G. S. (2003). Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302, 81-84.
44. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K. and Miyawaki, A. (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90.
45. Nemhauser, J. L., Feldman, L. J. and Zambryski, P. C. (2000). Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127, 3877-3888.
46. Noh, B., Murphy, A. S. and Spalding, E. P. (2001). Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13, 2441-2454.
47. Noh, B., Bandyopadhyay, A., Peer, W. A., Spalding, E. P. and Murphy, A. S. (2003). Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature 423, 999-1002.
48. Okada, K., Ueda, J., Komaki, M. K., Bell, C. J. and Shimura, Y. (1991). Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3, 677-684.
49. Paciorek, T., Zazímalová, E., Ruthardt, N., Petrásek, J., Stierhof, Y. D., Kleine-Vehn, J., Morris, D. A., Emans, N., Jürgens, G., Geldner, N. et al. (2005). Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251-1256.
50. Petrásek, J., Mravec, J., Bouchard, R., Blakeslee, J. J., Abas, M., Seifertová, D., Wisniewska, J., Tadele, Z., Kubes, M., Covanová, M. et al. (2006). PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914-918.
51. Reinhardt, D., Pesce, E. R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J. and Kuhlemeier, C. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426, 255-260.
52. Sakai, T., Wada, T., Ishiguro, S. and Okada, K. (2000). RPT2. A signal transducer of the phototropic response in Arabidopsis. Plant Cell 12, 225-236.
53. Sauer, M., Balla, J., Luschnig, C., Wisniewska, J., Reinöhl, V., Friml, J. and Benková, E. (2006). Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 20, 2902-2911.
54. Shevell, D. E., Leu, W. M., Gillmor, C. S., Xia, G., Feldmann, K. A. and Chua, N. H. (1994). EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77, 1051-1062.
55. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C. L., Paris, S., Gälweiler, L., Palme, K. and Jürgens, G. (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316-318.
56. Stogios, P. J., Downs, G. S., Jauhal, J. J., Nandra, S. K. and Prive, G. G. (2005). Sequence and structural analysis of BTB domain proteins. Genome Biol. 6, R82.
57. Takada, S. and Jürgens, G. (2007). Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134, 1141-1150.
58. Takada, S., Hibara, K., Ishida, T. and Tasaka, M. (2001). The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128, 1127-1135.
59. Takeuchi, M., Ueda, T., Sato, K., Abe, H., Nagata, T. and Nakano, A. (2000). A dominant negative mutant of sar1 GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 23, 517-525.
60. Treml, B. S., Winderl, S., Radykewicz, R., Herz, M., Schweizer, G., Hutzler, P., Glawischnig, E. and Torres Ruiz, R. A. (2005). The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development 132, 4063-4074.
61. Ueda, T., Uemura, T., Sato, M. H. and Nakano, A. (2004). Functional differentiation of endosomes in Arabidopsis cells. Plant J. 40, 783-789.
62. Uemura, T., Ueda, T., Ohniwa, R. L., Nakano, A., Takeyasu, K. and Sato, M. H. (2004). Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 29, 49-65.
63. Ulmasov, T., Hagen, G. and Guilfoyle, T. J. (1999). Activation and repression of transcription by auxin-response factors. Proc. Natl. Acad. Sci. USA 10, 5844-5849.
64. Wisniewska, J., Xu, J., Seifertová, D., Brewer, P. B., Ruzicka, K., Blilou, I., Rouquié, D., Benková, E., Scheres, B. and Friml, J. (2006). Polar PIN localization directs auxin flow in plants. Science 312, 883.