Abstract
Brassinosteroids (BRs) are growth-promoting natural substances required for normal plant growth and development. To understand the molecular mechanism of BR action, a cDNA microarray containing 1265 rice genes was analyzed for expression differences in rice lamina joint treated with brassinolide (BL). A novel BL-enhanced gene, designated OsBLE2, was identified and cloned. The full-length cDNA is 3243 bp long, encoding a predicted polypeptide of 761 amino acid residues and nine possible transmembrane regions. OsBLE2 expression was most responsive to BL in the lamina joint and leaf sheath in rice seedlings. Besides, auxin and gibberellins also increased its expression. OsBLE2 expressed more, as revealed by in situ hybridization, in vascular bundles and root primordia, where the cells are actively undergoing division, elongation, and differentiation. Transgenic rice expressing antisense OsBLE2 exhibits various degrees of repressed growth. BL could not enhance its expression in transgenic rice expressing antisense BRI1, a BR receptor, indicating that BR signaling to the enhanced expression of OsBLE2 is through BRI1. BL effect in the d1 mutant rice was much weaker than that in its wild-type control, indicating that heterotrimeric G protein may be a component of BRs signaling. These results suggest that OsBLE2 is involved in BL-regulated growth and development processes in rice.
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References
Aloni, R. 1995. The induction of vascular tissues by auxin and cytokinin. In: P.J. Davies (Ed.) Plant Hormone: Physiology, Biochemistry and Molecular Biology, Kluwer Academic Publisher, Dordrecht, Netherlands, pp. 531-546.
Ashikari, M., Wu, J., Yano, M., Sasaki, T. and Yoshimura, A. 1999. Rice gibberellin-insensitive dwarf gene Dwarf1 encodes the β subunit of GTP-binding protein. Proc. Natl. Acad. Sci. USA 96: 10284-10289.
Chomczynski, P. and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
Clouse, S.D. and Zurek, D.M. 1991. Molecular analysis of brassinolide action in plant growth and development. In: H.G.C. Cutlar, T. Yokota and G. Adam (Eds.) Brassinosteroid: Chemistry, Bioactivity and Application, ACS Symposium Series 474, American Chemical Society, Washington, DC, pp. 122-140.
Clouse, S.D. and Sasse, J.M. 1998. Brassinosteroids: essential regulator of plant growth and development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 427-451.
Goda, H., Shimada, Y., Asami, T., Fujioka, S. and Yoshida, S. 2002. Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 130: 1319-1334.
Fujisawa, Y., Kato, H. and Iwasaki, Y. 2001. Structure and function of hetrotrimetric G protein in plants. Plant Cell Physiol. 42: 789-794.
He, R., Wang, G. and Wang, X. 1991. Effects of brassinolide on growth and chilling resistance of maize seedling. In: H.G.C. Cutlar, T. Yokota and G. Adam (Eds.) Brassinosteroid: Chemistry, Bioactivity and Application, ACS Symposium Series 474, American Chemical Society, Washington, DC, pp. 220-230.
Hiei, Y., Ohta, S., Komari, T. and Kumashiro, Y. 1994. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis. Plant J. 6: 271-282.
Hood, E.E., Helmer, G.L., Fraley, R.T. and Chilton, M.D. 1986. The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo540 outside of T-DNA. J. Bact. 168: 1291-1301.
Hu, Y., Bao, F. and Li, J. 2000. Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant J. 24: 693-701.
Iwasaki, T. and Shibaoka, H. 1991. Brassionsteroids act as regulator of tracheary element differentiation in isolated Zinnia elegans mesophyll. Plant Cell Physiol. 32: 1007-1014.
Jiang, J. and Clouse, S.D. 2001. Expression of a plant gene with sequence similarity to animal TGF-receptor interacting protein is regulated by brassinosteroids and required for normal plant development. Plant J. 26: 35-45.
Kauschmann, A., Jessop, A., Koncz, C., Szekeres, M., Willmitzer, L. and Altmann, T. 1996. Genetic evidence for an essential role of brassinosteroids in plant development. Plant J. 9: 701-713.
Kawasaki, S., Borchert, C., Deyholos M., Wang, H., Brazilla, S., Kawai, K., Galbraith, D. and Bohnert, H. 2001. Gene expression profile during the initial phase of salt stress in rice. Plant Cell 13: 889-905.
Kawaguchi, M., Imaizumi-Anraku, H., Fukai, S. and Syono, K. 1996. Unusual branching in the seedlings of Lotus japonicus: gibberellins reveal the nitrogen-sensitive cell division within the pericycle on roots. Plant Cell Physiol. 37: 461-470.
Koka, C.V., Cerny, R.E., Gardner, R.G., Noguchi, T., Fujioka, S., Takatsuto, S. Yoshida, S. and Clouse, S.D. 2000. A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. Plant Physiol. 122: 85-98.
Kouchi, B. and Hata, S. 1993. Isolation and characterization of a novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol. Gen. Genet. 238: 106-119.
Li, J. and Chory, J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
Li, J. and Chory, J. 1999. Brassinosteroid actions in plants. J. Exp. Bot. 50: 275-282.
Li, J. and Nam, K.H. 2002. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295: 1299-301.
Li, J., Nam, K.H., Vafeados, D. and Chory, J. 2001. BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol. 127: 14-22.
Li, J., Lease, K., Tax, A.F.E. and Walker, J.C. 2001. BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 98: 5916-5921.
Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E. and Walker J.C. 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213-222.
Mandava, N.B. 1988. Plant growth-promoting brassinosteroids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39: 23-52.
Man-Ho, O., Romanow, W.G., Smith, R.C., Zamsiki, E, Sasse, J. and Clous, S.D. 1998. Soybean BRU1 encode a functional xyloglucan endotransglycosylase that is highly expressed in inner epicotyl tissues during brassinosteroid-promoted elongation. Plant Cell Physiol. 39: 124-130.
Marinissen, M.J. and Gutkind, J.S. 2001. G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol. Sci. 22: 368-376.
Müssig, C., Fischer, S. and Altmann, T. 2002. Brassinosteroidregulated gene expression. Plant Physiol. 129: 1241-1251.
Nam, K.H. and Li, J. 2002. BRI1/BAK1, a receptor pair mediating brassinosteroid signaling. Cell 110: 203-212.
Ohta, S., Mita, Hattori, T. and Nakamura, K. 1990. Construction and expression in tobacco of a β-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol. 31: 805-813.
Ruan, Y., Gilmore, J. and Conner, T. 1998. Towards Arabidopsis genome analysis: monitoring expression profiles of 1400 genes using cDNA microarrays. Plant J. 15: 821-833.
Sasse, J.M. 1997. Recent progress in brassinosteroid research. Physiol. Plant. 100: 696-701.
Schumacher, K. and Chory, J. 2000. Brassinosteroid signal transduction: still casting the actors. Curr. Opin. Plant Biol. 3: 79-84.
Seki, M., Narusaki, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y. and Shinozaki K. 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13: 61-72.
Uozu, S., Tanaka-Ueguchi, M., Kitano, H., Hattori, K. and Matsuoka, M. 2000. Characterization of XET-related genes of rice. Plant Physiol. 122: 853-859.
Ullah, H., Chen, J., Wang, S. and Jones, A. 2002. Role of a heterotrimeric g protein in regulation of Arabidopsis seed germination. Plant Physiol. 129: 897-907.
Wada, K., Marumo, S., Ikekawa, N., Morisaki, M. and Mori, K. 1981. Brassinolide and homobrassinolide promotion of lamina inclination of rice seedlings. Plant Cell Physiol. 22: 323-325.
Xu, W., Purugganan, M.M., Polisensky, D.H., Antosiewicz, D.M., Fry, S.C. and Braam, J. 1995. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7: 1555-1567.
Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., Ashikari, M., Kitano, H. and Matsuoka, M. 2000. Loss of function of a rice brassinosteroid insensitive1 homology prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591-1606.
Yang, G. and Komatsu, S. 2000. Involvement of calcium-dependent protein kinase in rice lamina inclination caused by brassinolide. Plant Cell Physiol. 41: 1243-1250.
Yazaki, J., Kishimoto, N., Nakamura, K., Fuji, F., J. Wu, J., Yamamoto, K., Sakata, K., Sasaki, K. and Kikuchi, S. 2000. Embarking on rice functional genomics via cDNA microarray with 1265 genes: use of 3′UTR probes for specific gene expression analysis. DNA Res. 7: 367-370.
Yin, Y., Wang, Z.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.
Yokota, T. and Takahashi, N. 1986. Chemistry, physiology and agricultural application of brassinolide and related steroids. In: M. Bopp (Ed.) Plant Growth Substances, Springer-Verlag, Berlin, pp. 129-138.
Zurek, D.M., and Clouse, S.D. 1994. molecular cloning and characterization of a brassinosteroid-regulated gene from elongating soybean epicotyls. Plant Physiol. 104: 161-170.
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Yang, G., Matsuoka, M., Iwasaki, Y. et al. A novel brassinolide-enhanced gene identified by cDNA microarray is involved in the growth of rice. Plant Mol Biol 52, 843–854 (2003). https://doi.org/10.1023/A:1025001304994
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DOI: https://doi.org/10.1023/A:1025001304994