Abstract
Members of the plant-specific GRAS family of putative transcription factors are involved in various aspects of plant development. SCARECROW (SCR) is a member of this protein family and plays a significant role in the radial patterning of both roots and shoots. However, little is known about the regulation of SCR expression and its mode of action in plants. Here, we report on the isolation and characterization of a Brassica napus SCARECROW-like protein, BnSCL1, isolated by selecting for proteins that interact with the Arabidopsis histone deacetylase AtHDA19 in a yeast two-hybrid screen. BnSCL1 contains domains conserved in the GRAS family of proteins, interacts with AtHDA19 through a VHIID domain, and exerts transcription activation of reporter genes. BnSCL1 is expressed predominantly in the roots, where its expression is regulated by auxin, as it also is in shoots and mature leaves. These results indicate that BnSCL1 is a member of the GRAS family, and suggest that its mode of action in plant auxin response may involve interaction with HDA19.
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Abel, S., Nguyen, M. D. and Theologis, A. 1995. The PS-IAA4/ 5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol. 251: 533–549.
Aranda, A. and Pascual, A. 2001. Nuclear hormone receptors and gene expression. Physiol. Rev. 81: 1269–1304.
Aufsatz, W., Mette, M. F., van der Winden, J., Matzke, M., Matzke, A. J. 2002. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by doublestranded RNA. EMBO J. 21: 6832–6841.
Canettieri, G., Morantte, I., Guzman, E., Asahara, H., Herzig, S., Anderson, S. D., Yates, J. R. and Montminy, M. 2003. Attenuation of a phosphorylation-dependent activator by an HDAC-PP1 complex. Nat. Struct. Biol. 10: 175–181.
Costa, S. and Dolan, L. 2000. Development of the root pole and cell patterning in Arabidopsis roots. Curr. Opin. Genet. Dev. 10: 405–409.
Di Laurenzio, L., Wysocka-Diller, J., Malamy, J. E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M. G., Feldmann, K. A. and Benfey, P. N. 1996. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86: 423–433.
Friml, J., Benkova, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jurgens, G. and Palme, K. 2002. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108: 661–673.
Fu, X. and Harberd, N. P. 2003. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421: 740–743.
Gao, M.-J., Allard, G., Byass, L., Flanagan, A. M. and Singh, J. 2002. Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol. Biol. 49: 459–471.
Gao, M.-J. Schäfer, U. A., Parkin, I. A. P., Hegedus, D. D., Lydiate, D. J. and Hannoufa, A. 2003. A novel protein from Brassica napus has a putative KID domain and responds to low temperature. Plant J. 33: 1073–1086.
Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.-T. and Benfey, P. N. 2000. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101: 555–567.
Kaya, H., Shibahara, K., Taoka, K., Iwabuchi, M., Stillman, B. and Araki, T. 2001. FASCIATA genes for chromatin assembly factor-1 in Arabidopsis matain the cellular organization of apical meristem. Cell 104: 131–142.
Kurdistani, S. K. and Grunstein, M. 2003. Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell Biol. 4: 276–284.
Leyser, O. 2002. Molecular genetics of auxin signaling. Annu. Rev. Plant Biol. 53: 377–398.
Llave, C., Xie, Z., Kasschau, K. D. and Carrington, J. C. 2002a. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297: 2053–2056.
Llave, C., Kasschau, K. D., Rector, M. A. and Carrington, J. C. 2002b. Endogenous and silencing-associated small RNAs in plants. Plant Cell 14: 1605–1619.
Lusser, A., Kölle, D. and Loidl, P. 2001. Histone acetylation: lessons from the plant kingdom. Trends Plant Sci. 6: 59–65.
Mello, J. A. and Almouzni, G. 2001. The ins and outs of nucleosome assembly.Curr. Opin. Genet. Dev. 11: 136–141.
Morohashi, K., Minami, M., Takase, H., Hotta, Y. and Hiratsuka, K. 2003. Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J. Biol. Chem. 278: 20865–20873.
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.
Nakajima, K. and Benfey, P. N. 2002. Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14: S265–S276.
Pandey, R., Muller, A., Napoli, C. A., Selinger, D. A., Pikaard, C. S., Richards, E. J., Bender, J., Mount, D. W. and Jorgensen, R. A. 2002. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic. Acids Res. 30: 5036–5055.
Parkin, I. A. P., Lydiate, D. J. and Trick, M. 2002. Assessing the level of collinearity between Arabidopsis thaliana and Brassica napus for A. thaliana chromosome 5. Genome 45: 356–366.
Paterson, A. H., Lan, T. H., Amasino, R., Osborn, T. C. and Quiros, C. 2001. Brassica genomics: a complement to, and early beneficiary of, the Arabidopsis sequence. Genome Biol. 2: 1011.1–1011.4.
Probst, A. V., Fagard, M., Proux, F., Mourrain, P., Boutet, S., Earley, K., Lawrence, R. J., Pikaard, C. S., Murfett, J., Furner, I., Vaucheret, H. and Scheid, O. M. 2004. Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell. 16: 1021–1034.
Pysh, L. D., Wysocka–Diller, J. W., Camilleri, C., Bouchez, D. and Benfey, P. N. 1999. The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18: 111–119.
Raikhel, N. 1992. Nuclear targeting in plants. Plant Physiol. 100: 1627–1632.
Reyes, J. C., Hennig, L. and Gruissem, W. 2002. Chromatinremodeling and memory factors. New regulators of plant development. Plant Physiol. 130: 1090–1101.
Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P. N., Leyser, O., Bechtold, N., Weisbeek, P. and Scheres, B. 1999. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463–472.
Sabatini, S., Heidstra, R., Wildwater, M. and Scheres, B. 2003. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17: 354–358.
Schumacher, K., Schmitt, T., Rossberg, M., Schmitz, G. and Theres, K. 1999. The lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc. Natl. Acad. Sci. USA 96: 290–295.
Silverstone, A. L., Ciampaglio, C. N. and Sun, T. P. 1998. The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10: 155–169.
Tian, L. and Chen, Z. J. 2001. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc. Natl. Acad. Sci. USA 98: 200–205.
Torchia, J., Rose, D. W., Inostroza, J., Kamei, Y., Westin, S., Glass, C. K. and Rosenfeld, M. G. 1997. The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 387: 677–684.
Tussiè-Luna, M. I., Bayarsaihan, D., Seto, E., Ruddle, F. H. and Roy, A. L. 2002. Physical and functional interactions of histone deacetylase 3 with TFII–I family proteins and PIASxß. Proc. Natl. Acad. Sci. USA 99: 12807–12812.
Verbsky, M. L. and Richards, E. J. 2001. Chromatin remodeling in plants. Curr. Opin. Plant Biol. 4: 494–500.
Wagner, D. 2003. Chromatin regulation of plant development. Curr. Opin. Plant Biol. 6: 20–28.
Wen, C. K. and Chang, C. 2002. Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14: 87–100.
Wu, K., Malik, K., Tian, L., Brown, D. and Miki, B. 2000. Functional analysis of a RPD3 histone deacetylase homologue in Arabidopsis thaliana. Plant Mol. Biol. 44: 167–176.
Wu, K., Tian, L., Zhou, C., Brown, D. and Miki, B. 2003. Repression of gene expression by Arabidopsis HD2 histone deacetylases. Plant J. 34: 241–247.
Wysocka-Diller, J. W., Helariutta, Y., Fukaki, H., Malamy, J. E. and Benfey, P. N. 2000. Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127: 595–603.
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.
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Gao, Mj., Parkin, I., Lydiate, D. et al. An auxin-responsive SCARECROW-like transcriptional activator interacts with histone deacetylase. Plant Mol Biol 55, 417–431 (2004). https://doi.org/10.1007/s11103-004-0892-9
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DOI: https://doi.org/10.1007/s11103-004-0892-9