The β-subunit of the arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes

Plant Cell

Volumn 15, Issue 2, 2003, Pages 393-409

  Ullah, Hemayet ^a   Chen, Jin Gui ^a   Temple, Brenda ^b   Boyes, Douglas C ^c   Alonso, José M ^d,e   Davis, Keith R ^c   Ecker, Joseph R ^d   Jones, Alan M ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c Clinical Data Inc   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; GENES; PROTEINS;

NULL MUTANTS;

PLANT CELL CULTURE;

ARABIDOPSIS; EMBRYOPHYTA;

EID: 0037327627     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.006148     Document Type: Article

References (71)

1. 2+ channel by TGa1, a heterotrimeric G protein α-subunit homologue. FEBS Lett. 424, 17-21.
2. Aoyama, T., and Chua, N.H. (1997). A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605-612.
3. Assmann, S.M. (2002). Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell 14 (suppl.), S355-S373.
4. Bairoch, A., and Apweiler, R. (2000). The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 28, 45-48.
5. Beeckman, T., Burssens, S., and Inze, D. (2001). The peri-cell-cycle in Arabidopsis. J. Exp. Bot. 52, 403-411.
6. Beffa, R., Szell, M., Meuwly, P., Pay, A., Vogeli-Lange, R., Metraux, J.-P., Neuhaus, G., Meins, F., and Nagy, F. (1995). Cholera toxin elevates pathogen resistance and induces pathogenesis-related gene expression in tobacco. EMBO J. 14, 5753-5761.
7. Blakely, L.M., Blakely, R.M., Colowit, P.M., and Elliot, D.S. (1988). Experimental studies on lateral root formation in radish seedling roots: Analysis of the dose-response to exogenous auxin. Plant Physiol. 87, 414-419.
8. + inward-rectifier evoked by auxin. Plant J. 5, 55-68.
9. Boerjan, W., Cervera, M.T., Delarue, M., Beeckman, T., Dewitte, W., Bellini, C., Caboche, M., Van Onckelen, H., Van Montagu, M., and Inze, D. (1995). Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7, 1405-1419.
10. Bogre, L., Meskiene, I., Herberle-Bors, E., and Hirt, H. (2000). Stressing the role of MAP kinases in mitogenic stimulation. Plant Mol. Biol. 43, 705-718.
11. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K., and Gorlach, J. (2001). Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13, 1499-1510.
12. Casimiro, I., Marchant, A., Bhalerao, R.P., Beeckman, T., Dhooge, S., Swarup, R., Graham, N., Inze, D., Sandberg, G., Casero, P.J., and Bennett, M. (2001). Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13, 843-852.
13. Celenza, J.L., Grisafi, P.L., and Fink, G.R. (1995). A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev. 9, 2131-2142.
14. Chen, J.-G., Ullah, H., Young, J.C., Sussman, M.R., and Jones, A.M. (2001). ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev. 15, 902-911.
15. Christopher, J.A. (1998). The Structural Properties Observation and Calculation Kit. (College Station, TX: The Center for Macromolecular Design, Texas A&M University).
16. Clapham, D.E., and Neer, E.J. (1997). G protein βγ subunits. Annu. Rev. Pharmacol. Toxicol. 37, 167-203.
17. Clouse, S.D. (1998). Brassinosteroid affects the rate of cell division in isolated leaf protoplasts from Petunia hybrida. Plant Cell Rep. 17, 921-924.
18. + channels (GIRKs). J. Biol. Chem. 276, 11409-11413.
19. Dubrovsky, J.G., Rost, T.L., Colon-Carmona, A., and Doener, P. (2001). Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214, 30-36.
20. Ephritikhine, G., Fellner, M., Vannini, C., Lapous, D., and Barbier-Brygoo, H. (1999). The sax1 dwarf mutant of Arabidopsis thaliana shows altered sensitivity of growth responses to abscisic acid, auxin, gibberellins and ethylene and is partially rescued by exogenous brassinosteroid. Plant J. 18, 303-314.
21. + channel current in guard cells of fava bean. Plant Cell 3, 1037-1044.
22. Fischer, D. (2000). Hybrid fold recognition: Combining sequence derived properties with evolutionary information. Pac. Symp. Biocomput. 2000, 119-130.
23. Friml, J., Benkova, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jurgens, G., and Palme, K. (2002a). AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661-673.
24. Friml, J., Wisniewska, J., Benkova, E., Mendgens, K., and Palme, K. (2002b). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
25. Gray, W.M., Ostin, A., Sandberg, G., Romano, C.P., and Estelle, M. (1998). High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl. Acad. Sci. USA 95, 7197-7202.
26. Himanen, K., Boucheron, E., Vanneste, S., de Almeida Engler, J., Inzé, D., and Beeckman, T. (2002). Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14, 2339-2351.
27. Hobbie, L., and Estelle, M. (1995). The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J. 7, 211-220.
28. Hoffmann, W.K., deVos, S., Tsukaski, K., Wachsman, W., Pinkus, G.S., Said, J.W., and Koeffler, H.P. (2001). Altered apoptosis pathways in mantle cell lymphoma detected by oligonucleotide microarray. Blood 98, 787-794.
29. Jones, A.M. (2002). G protein-coupled signaling in Arabidopsis. Curr. Opin. Plant Biol. 5, 402-407.
30. Jones, A.M., Ecker, J.R., and Chen, J.-G. (2003). A re-evaluation of the role of the heterotrimeric G protein in coupling light responses in Arabidopsis. Plant Physiol., in press.
31. Jones, D.T. (1999). GenTHREADER: An efficient and reliable protein fold recognition method for genomic sequences. J. Mol. Biol. 287, 797-815.
32. Jones, H.D., Smith, S.J., Desikan, R., Plakidou-Dymock, S., Lovegrove, A., and Hooley, R. (1998). Heterotrimeric G proteins are implicated in gibberellin induction of amylase gene expression in wild oat aleurone. Plant Cell 10, 245-254.
33. Kelley, L.A., MacCallum, R.M., and Sternberg, M.J.E. (2000). Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299, 499-520.
34. Klee, H.J. (1987). The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthesis gene products in transgenic petunia plants. Genes Dev. 1, 86-96.
35. Kovtun, Y., Chiu, W.-L., Zeng, W., and Sheen, J. (1998). Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395, 716-720.
36. Kroll, S.D., Chen, J., De Vivo, M., Carty, D.J., Buku, A., Premont, R.T., and Iyengar, R. (1992). The Q205L Go-alpha subunit expressed in NIH-3T3 cells induces transformation. J. Biol. Chem. 267, 23183-23188.
37. Kubo, M., and Kakimoto, T. (2000). The cytokinin-hypersensitive genes of Arabidopsis negatively regulate the cytokinin-signaling pathway for cell division and chloroplast development. Plant J. 23, 385-394.
38. Lambright, D.G., Sondek, J., Bohm, A., Skiba, N.P., Hamm, H.E., and Sigler, P.B. (1996). The 2.0 A crystal structure of a heterotrimeric G protein. Nature 379, 311-319.
39. Laskowski, M.J., Williams, M.E., Nusbaum, H.C., and Sussex, I.M. (1995). Formation of lateral root meristems is a two-stage process. Development 121, 3303-3310.
40. Lease, K.A., Wen, J., Li, J., Doke, J.T., Liscum, E., and Walker, J.C. (2001). A mutant Arabidopsis heterotrimeric G protein β subunit affects leaf, flower, and fruit development. Plant Cell 13, 2631-2641.
41. Malamy, J., and Benfey, P. (1997). Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Genes Dev. 124, 33-44.
42. Mason, M.G., and Botella, J.R. (2000). Completing the heterodimer: Isolation and characterization of an Arabidopsis thaliana G protein γ-subunit cDNA. Proc. Natl. Acad. Sci. USA 97, 14784-14788.
43. Mockaitis, K., and Howell, S.H. (2000). Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J. 24, 785-796.
44. Muday, G.K., and Haworth, P. (1994). Tomato root growth, gravitropism, and lateral development: Correlation with auxin transport. Plant Physiol. Biochem. 32, 193-203.
45. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473-497.
46. Neuhaus, G., Bowler, C., Kern, R., and Chua, N.-H. (1993). Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73, 937-952.
47. + expression represents an essential step in coleoptile growth and gravitropism. Proc. Natl. Acad. Sci. USA 96, 12186-12191.
48. Pryciak, P.M., and Huntress, F.A. (1998). Membrane recruitment of the kinase cascade scaffold Ste5p by the G beta gamma complex underlies activation of the yeast pheromone response pathway. Genes Dev. 12, 2684-2697.
49. Schaefer, M., Petroncki, M., Dorner, D., Forte, M., and Knoblich, J.A. (2001). Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 107, 183-194.
50. Schwechheimer, C., and Deng, X.W. (2000). The COP/DET/FUS proteins: Regulators of eukaryotic growth and development. Semin. Cell Dev. Biol. 11, 495-503.
51. Shi, J., Blundell, T.L., and Mizuguchi, K. (2001). FUGUE: Sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243-257.
52. Smith, D., and Fedoroff, N.V. (1995). LRP1, a gene expressed in lateral and adventitious root primordia of Arabidopsis. Plant Cell 7, 735-745.
53. + channels in Vicia stomatal guard cells by peptide homologs to the auxin-binding protein C terminus. Proc. Natl. Acad. Sci. USA 90, 11493-11497.
54. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The ClustalX Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876-4882.
55. Timpte, C., Lincoln, C., Pickett, F.B., Turner, J., and Estelle, M. (1995). The AXR1 and AUX1 genes of Arabidopsis function in separate auxin-response pathways. Plant J. 8, 561-569.
56. Ueguchi-Tanaka, M., Fujisawa, Y., Kobayashi, M., Ashikari, M., Iwasaki, Y., Kitano, H., and Matsuoka, M. (2000). Rice dwarf mutant d1, which is defective in the α subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc. Natl. Acad. Sci. USA 97, 11638-11643.
57. Ullah, H., Chen, J.-G., Wang, S., and Jones, A.M. (2002). Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol. 129, 897-907.
58. Ullah, H., Chen, J.-G., Young, J.C., Im, K.-H., Sussman, M.R., and Jones, A.M. (2001). Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292, 2066-2069.
59. Vanderbeld, B., and Kelly, G.M. (2000). New thoughts on the role of beta-gamma subunit in G protein signal transduction. Biochem. Cell Biol. 78, 537-550.
60. van Drogen, F., Stuke, V.M., Jorritsma, G., and Peter, M. (2001). MAP kinase dynamics in response to pheromones in budding yeast. Nat. Cell Biol. 3, 1051-1061.
61. a1b1g1. Cell 83, 1047-1058.
62. Wall, M.A., Posner, B.A., and Sprang, S.R. (1998). Structural basis of activity and subunit recognition in G protein heterotrimers. Structure 6, 1169-1183.
63. Wang, X.-Q., Ullah, H., Jones, A.M., and Assmann, S.M. (2001). G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292, 2070-2072.
64. Warpeha, K.M.F., Hamm, H.E., Rasenick, M.M., and Kaufman, L.S. (1991). A blue-light activated GTP-binding protein in the plasma membrane of etiolated peas. Proc. Natl. Acad. Sci. USA 88, 8925-8929.
65. Wise, A., Thomas, P.G., Carr, T.H., Murphy, G.A., and Millner, P.A. (1997). Expression of the Arabidopsis G protein GPa1: Purification and characterization of the recombinant protein. Plant Mol. Biol. 33, 723-728.
66. Xie, Q., Frugis, G., Colgan, D., and Chua, N.-H. (2000). Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14, 3024-3036.
67. Xie, Q., Guo, H.-S., Dallman, G., Fang, S., Weismann, A.M., and Chua, H.-H. (2002). SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167-170.
68. Yin, Y., Wang, A.-Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181-191.
69. Zaina, S., Brevaiaro, D., Mappelli, S., Bertani, A., and Reggiani, R. (1994). Two putative G protein a subunits dissociate from rice coleoptile membranes after GTP stimulation. J. Plant Physiol. 143, 293-297.
70. Zaina, S., Mappelli, S., Reggiani, R., and Bretani, A. (1991). Auxin and GTPase activity in membranes from aerobic and anaerobic rice coleoptiles. J. Plant Physiol. 138, 760-762.
71. Zaina, S., Reggiani, R., and Bertani, A. (1990). Preliminary evidence for involvement of GTP-binding protein(s) in auxin signal transduction in rice (Oryza sativa L.) coleoptile. J. Plant Physiol. 136, 653-658.