NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation

Plant Journal

Volumn 43, Issue 1, 2005, Pages 118-130

  Wilmoth, Jill C ^a   Wang, Shucai ^b   Tiwari, Shiv B ^b   Joshi, Atul D ^a   Hagen, Gretchen ^b   Guilfoyle, Thomas J ^b   Alonso, Jose M ^c,d   Ecker, Joseph R ^c   Reed, Jason W ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b University of Missouri   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

ARF19; ARF7; Auxin; Auxin response factor; Lateral root; NPH4

Indexed keywords

GENES; GENETIC ENGINEERING;

AUXIN; AUXIN RESPONSE FACTORS (ARF); GLUTAMINE-RICH MIDDLE DOMAINS; LEAF EXPANSION;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; ARF19 PROTEIN, ARABIDOPSIS; ARF7 PROTEIN, ARABIDOPSIS; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; DOSE RESPONSE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PHYSIOLOGY; PLANT LEAF; PLANT ROOT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; PHENOTYPE; PLANT LEAVES; PLANT ROOTS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ALLELES; AUXINS; CELLS; GENES; GLUTAMINE; LEAVES; ROOTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 22044436100     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02432.x     Document Type: Article

References (68)

1. Aida, M., Vernoux, T., Furutani, M., Traas, J. and Tasaka, M. (2002) Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development, 129, 3965-3974.
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
3. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G. and Friml, J. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591-602.
4. Berleth, T. and Jürgens, G. (1993) The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development, 118, 575-587.
5. Bhalerao, R., Eklof, J., Ljung, K., Marchant, A., Bennet, M. and Sandberg, G. (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J. 29, 325-332.
6. Casimiro, I., Beeckman, T., Graham, N., Bhalerao, R., Zhang, H., Casero, P., Sandberg, G. and Bennett, M.J. (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci. 8, 165-171.
7. Dharmasiri, N. and Estelle, M. (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci. 9, 302-308.
8. Dharmasiri, N., Dharmasiri, S., Jones, A.M. and Estelle, M. (2003) Auxin action in a cell-free system. Curr. Biol. 13, 1418-1422.
9. Dubrovsky, J.G., Doerner, P.W., Colon-Carmona, A. and Rost, T.L. (2000) Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol. 124, 1648-1657.
10. Elumalai, R.P., Nagpal, P. and Reed, J.W. (2002) A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell, 14, 119-131.
11. Estelle, M.A. and Somerville, C. (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206, 200-206.
12. Fukaki, H., Tameda, S., Masuda, H. and Tasaka, M. (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29, 153-168.
13. TIR1-dependent degradation of AUX/IAA proteins. Nature, 414, 271-276.
14. Hagen, G. and Guilfoyle, T. (2002) Auxin-responsive gene expression: genes, promoters, and regulatory factors. Plant Mol. Biol. 49, 373-385.
15. Hagen, G., Martin, G., Li, Y. and Guilfoyle, T.J. (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol. Biol. 17, 567-579.
16. Hardtke, C.S. and Berleth, T. (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405-1411.
17. Hardtke, C.S., Ckurshumova, W., Vidaurre, D.P., Singh, S.A., Stamatiou, G., Tiwari, S.B., Hagen, G., Guilfoyle, T.J. and Berleth, T. (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development, 131, 1089-1100.
18. Harper, R.M., Stowe-Evans, E.L., Luesse, D.R., Muto, H., Tatematsu, K., Watahiki, M.K., Yamamoto, K. and Liscum, E. (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell, 757-770.
19. Jones, A.M., Im, K.-H., Savka, M.A., Wu, M.-J., DeWitt, G., Shillito, R. and Binns, A.N. (1998) Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science, 282, 1114-1117.
20. Kepinski, S. and Leyser, O. (2004) Auxin-induced SCFTIR1-Aux/IAA interaction involves stable modification of the SCFTIR1 complex. Proc. Natl Acad. Sci. USA, 101, 12381-12386.
21. Kim, J., Harter, K. and Theologis, A. (1997) Protein-protein interactions among the Aux/IAA proteins. Proc. Natl Acad. Sci. USA, 94, 11786-11791.
22. Knee, E.M. and Hangarter, R.P. (1996) Differential IAA dose response relations of the axr1 and axr2 mutants of Arabidopsis. Physiologia Plantarum, 98, 320-324.
23. Kovtun, Y., Chiu, W.-L., Tena, G. and Sheen, J. (2000) Functional analysis of oxidative stress-activated mitagen-activated protein kinase cascade in plants. Proc. Natl Acad. Sci. USA, 97, 2940-2945.
24. Leyser, H.M.O., Pickett, F.B., Dharmasiri, S. and Estelle, M. (1996) Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J. 10, 403-413.
25. Li, H., Johnson, P., Stepanova, A., Alonso, J.M. and Ecker, J.R. (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev. Cell, 7, 193-204.
26. 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.
27. Liscum, E. and Reed, J.W. (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49, 387-400.
28. Liu, Z.-B., Ulmasov, T., Shi, X., Hagen, G. and Guilfoyle, T.J. (1994) The soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell, 6, 645-657.
29. Lopez-Bucio, J., Cruz-Ramirez, A. and Herrera-Estrella, L. (2003) The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6, 280-287.
30. Malamy, J.E. and Ryan, K.S. (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol. 127, 899-909.
31. Marchant, A., Bhalerao, R., Casimiro, I., Eklof, J., Casero, P.J., Bennett, M. and Sandberg, G. (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell, 14, 589-597.
32. Mattsson, J., Sung, Z.R. and Berleth, T. (1999) Responses of plant vascular systems to auxin transport inhibition. Development, 126, 2979-2991.
33. Morgan, K.E., Zarembinski, T.I., Theologis, A. and Abel, S. (1999) Biochemical characterization of recombinant polypeptides corresponding to the predicted beta-alpha-alpha fold in Aux/IAA proteins. FEBS Lett. 454, 283-287.
34. Murfett, J., Wang, X.J., Hagen, G. and Guilfoyle, T.J. (2001) Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell, 13, 1047-1061.
35. Nodzon, L.A., Xu, W.-H., Wang, Y., Pi, L.-Y., Chakrabarty, P.K. and Song, W.-Y. (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J. 40, 996-1006.
36. Okushima, Y., Overvoorde, P.J., Arima, K. et al. (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell, 17, 444-463.
37. Ouellet, F., Overvoorde, P.J. and Theologis, A. (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell, 13, 829-841.
38. Przemeck, G.K.H., Mattsson, J., Hardtke, C.S., Sung, Z.R. and Berleth, T. (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta, 200, 229-237.
39. Ramos, J., Zenser, N., Leyser, O. and Callis, J. (2001) Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell, 13, 2349-2360.
40. Reed, J.W. (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420-425.
41. Reed, J.W., Elumalai, R.P. and Chory, J. (1998a) Suppressors of an Arabidopsis thaliana phyB mutation identify genes that control light signalling and hypocotyl elongation. Genetics, 148, 1295-1310.
42. Reed, R.C., Brady, S.R. and Muday, G.K. (1998b) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis thaliana. Plant Physiol. 118, 1369-1378.
43. Remington, D.L., Vision, T.J., Guilfoyle, T.J. and Reed, J.W. (2004) Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol. 135, 1738-1752.
44. Rogg, L.E., Lasswell, J. and Bartel, B. (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell, 13, 465-480.
45. Sieburth, L. (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol. 121, 1179-1190.
46. Stowe-Evans, E.L., Harper, R.M., Motchoulski, A.V. and Liscum, E. (1998) NPH4, a conditional modulator of auxin-dependent differential growth responses in Arabidopsis. Plant Physiol. 118, 1265-1275.
47. Stowe-Evans, E.L., Luesse, D.R. and Liscum, E. (2001) The enhancement of phototropin-induced phototropic curvature in Arabidopsis occurs via a photoreversible phytochrome A-dependent modulation of auxin responsiveness. Plant Physiol. 126, 826-834.
48. Tatematsu, K., Kumagai, S., Muto, H., Sato, A., Watahiki, M.K., Harper, R.M., Liscum, E. and Yamamoto, K.T. (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell, 16, 379-393.
49. Tian, Q. and Reed, J. (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development, 126, 711-721.
50. Tian, Q., Uhlir, N.J. and Reed, J.W. (2002) Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell, 14, 301-319.
51. Tian, Q., Nagpal, P. and Reed, J.W. (2003) Regulation of Arabidopsis SHY2/IAA3 protein turnover. Plant J. 36, 643-651.
52. Tian, C., Muto, H., Higuchi, K., Matamura, T., Tatematsu, K., Koshiba, T. and Yamamoto, K.T. (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J. 40, 333-343.
53. Tiwari, S.B., Wang, X.J., Hagen, G. and Guilfoyle, T.J. (2001) AUX/ IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell, 13, 2809-2822.
54. Tiwari, S.B., Hagen, G. and Guilfoyle, T.J. (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell, 15, 533-543.
55. Tiwari, S.B., Hagen, G. and Guilfoyle, T.J. (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell, 16, 533-543.
56. Tiwari, S.B., Wang, S., Hagen, G. and Guilfoyle, T.J. (2005) Transfection assays with Arabidopsis protoplasts containing integrated reporter genes. In Arabidopsis Protocols (Salinas, J. and Sanchez-Serrano, J.J., eds). Totowa, NJ: The Humana Press Inc., in press.
57. Turnbull, C.G., Booker, J.P. and Leyser, H.M. (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255-262.
58. Ulmasov, T., Liu, Z.-B., Hagen, G. and Guilfoyle, T.J. (1995) Composite structure of auxin response elements. Plant Cell, 7, 1611-1623.
59. Ulmasov, T., Hagen, G. and Guilfoyle, T.J. (1997a) ARF1, a transcription factor that binds to auxin response elements. Science, 276, 1865-1868.
60. Ulmasov, T., Murfett, J., Hagen, G. and Guilfoyle, T.J. (1997b) Aux/ IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell, 9, 1963-1971.
61. Ulmasov, T., Hagen, G. and Guilfoyle, T.J. (1999a) Activation and repression of transcription by auxin-response factors. Proc. Natl Acad. Sci. USA, 96, 5844-5849.
62. Ulmasov, T., Hagen, G. and Guilfoyle, T.J. (1999b) Dimerization and DNA binding of auxin response factors. Plant J. 19, 309-319.
63. Vandenbussche, F., Vriezen, W.H., Smalle, J., Laarhoven, L.J., Harren, F.J. and Van Der Straeten, D. (2003) Ethylene and auxin control the Arabidopsis response to decreased light intensity. Plant Physiol. 133, 517-527.
64. Watahiki, M.K. and Yamamoto, K. (1997) The massagu1 mutation of Arabidopsis identified with failure of auxin-induced growth curvature of hypocotyl confers auxin insensitivity to hypocotyl and leaf. Plant Physiol. 115, 419-426.
65. Weijers, D. and Jurgens, G. (2004) Funneling auxin action: specificity in signal transduction. Curr. Opin. Plant Biol. 7, 687-693.
66. Weijers, D., Benkova, E., Jäger, K., Schlereth, A., Hamann, T., Kientz, M., Wilmoth, J.C., Reed, J.W. and Jürgens, G. (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J. doi: 10.1038/sj. emboj.7600659 (online publication).
67. 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.
68. Zenser, N., Ellsmore, A., Leasure, C. and Callis, J. (2001) Auxin modulates the degradation rate of Aux/IAA proteins. Proc. Natl Acad. Sci. USA, 98, 11795-11800.