PLANT PHYSIOLOGY , Vol 111, Issue 3 671-678, Copyright © 1996 by American Society of Plant Biologists

DEVELOPMENT AND GROWTH REGULATION

A Brassinosteroid-Insensitive Mutant in Arabidopsis thaliana Exhibits Multiple Defects in Growth and Development

S. D. Clouse, M. Langford and T. C. McMorris
Department of Horticultural Science, North Carolina State University, Raleigh, North Carolina 27695 (S.D.C.)

Brassinosteroids are widely distributed plant compounds that modulate cell elongation and division, but little is known about the mechanism of action of these plant growth regulators. To investigate brassinosteroids as signals influencing plant growth and development, we identified a brassinosteroid-insensitive mutant in Arabidopsis thaliana (L.) Henyh. ecotype Columbia. The mutant, termed bri1, did not respond to brassinosteroids in hypocotyl elongation and primary root inhibition assays, but it did retain sensitivity to auxins, cytokinins, ethylene, abscisic acid, and gibberellins. The bri1 mutant showed multiple deficiencies in developmental pathways that could not be rescued by brassinosteroid treatment, including a severely dwarfed stature; dark green, thickened leaves; male sterility; reduced apical dominance; and de-etiolation of darkgrown seedlings. Genetic analysis suggests that the Bri1 phenotype is caused by a recessive mutation in a single gene with pleiotropic effects that maps 1.6 centimorgans from the cleaved, amplified, polymorphic sequence marker DHS1 on the bottom of chromosome IV. The multiple and dramatic effects of mutation of the BRI1 locus on development suggests that the BRI1 gene may play a critical role in brassinosteroid perception or signal transduction.

This article has been cited by other articles:

				Z. Deng, X. Zhang, W. Tang, J. A. Oses-Prieto, N. Suzuki, J. M. Gendron, H. Chen, S. Guan, R. J. Chalkley, T. K. Peterman, et al. A Proteomics Study of Brassinosteroid Response in Arabidopsis Mol. Cell. Proteomics, December 1, 2007; 6(12): 2058 - 2071. [Abstract] [Full Text] [PDF]

				H. Ryu, K. Kim, H. Cho, J. Park, S. Choe, and I. Hwang Nucleocytoplasmic Shuttling of BZR1 Mediated by Phosphorylation Is Essential in Arabidopsis Brassinosteroid Signaling PLANT CELL, September 1, 2007; 19(9): 2749 - 2762. [Abstract] [Full Text] [PDF]

				M. A. Domagalska, F. M. Schomburg, R. M. Amasino, R. D. Vierstra, F. Nagy, and S. J. Davis Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering Development, August 1, 2007; 134(15): 2841 - 2850. [Abstract] [Full Text] [PDF]

				N. Geldner, D. L. Hyman, X. Wang, K. Schumacher, and J. Chory Endosomal signaling of plant steroid receptor kinase BRI1 Genes & Dev., July 1, 2007; 21(13): 1598 - 1602. [Abstract] [Full Text] [PDF]

				N. Holton, A. Cano-Delgado, K. Harrison, T. Montoya, J. Chory, and G. J. Bishop Tomato BRASSINOSTEROID INSENSITIVE1 Is Required for Systemin-Induced Root Elongation in Solanum pimpinellifolium but Is Not Essential for Wound Signaling PLANT CELL, May 1, 2007; 19(5): 1709 - 1717. [Abstract] [Full Text] [PDF]

				H. Bauby, F. Divol, E. Truernit, O. Grandjean, and J.-C. Palauqui Protophloem Differentiation in Early Arabidopsis thaliana Development Plant Cell Physiol., January 1, 2007; 48(1): 97 - 109. [Abstract] [Full Text] [PDF]

				Y. Belkhadir and J. Chory Brassinosteroid Signaling: A Paradigm for Steroid Hormone Signaling from the Cell Surface Science, December 1, 2006; 314(5804): 1410 - 1411. [Abstract] [Full Text] [PDF]

				X. Wang and J. Chory Brassinosteroids Regulate Dissociation of BKI1, a Negative Regulator of BRI1 Signaling, from the Plasma Membrane Science, August 25, 2006; 313(5790): 1118 - 1122. [Abstract] [Full Text] [PDF]

				B. Chow and P. McCourt Plant hormone receptors: perception is everything Genes & Dev., August 1, 2006; 20(15): 1998 - 2008. [Abstract] [Full Text] [PDF]

				A. Bishopp, A. P. Mahonen, and Y. Helariutta Signs of change: hormone receptors that regulate plant development. Development, May 1, 2006; 133(10): 1857 - 1869. [Abstract] [Full Text] [PDF]

				C. Albrecht, E. Russinova, V. Hecht, E. Baaijens, and S. de Vries The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 Control Male Sporogenesis PLANT CELL, December 1, 2005; 17(12): 3337 - 3349. [Abstract] [Full Text] [PDF]

				L. Li, J. Xu, Z.-H. Xu, and H.-W. Xue Brassinosteroids Stimulate Plant Tropisms through Modulation of Polar Auxin Transport in Brassica and Arabidopsis PLANT CELL, October 1, 2005; 17(10): 2738 - 2753. [Abstract] [Full Text] [PDF]

				N. A. Eckardt Brassinosteroid Perception and Signaling: Heterodimerization and Phosphorylation of Receptor-Like Kinases BRI1 and BAK1 PLANT CELL, June 1, 2005; 17(6): 1638 - 1640. [Full Text] [PDF]

				X. Wang, M. B. Goshe, E. J. Soderblom, B. S. Phinney, J. A. Kuchar, J. Li, T. Asami, S. Yoshida, S. C. Huber, and S. D. Clouse Identification and Functional Analysis of in Vivo Phosphorylation Sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 Receptor Kinase PLANT CELL, June 1, 2005; 17(6): 1685 - 1703. [Abstract] [Full Text] [PDF]

				G. T.S. Beemster, L. De Veylder, S. Vercruysse, G. West, D. Rombaut, P. Van Hummelen, A. Galichet, W. Gruissem, D. Inze, and M. Vuylsteke Genome-Wide Analysis of Gene Expression Profiles Associated with Cell Cycle Transitions in Growing Organs of Arabidopsis Plant Physiology, June 1, 2005; 138(2): 734 - 743. [Abstract] [Full Text] [PDF]

				J. Lisso, D. Steinhauser, T. Altmann, J. Kopka, and C. Mussig Identification of brassinosteroid-related genes by means of transcript co-response analyses Nucleic Acids Res., May 12, 2005; 33(8): 2685 - 2696. [Abstract] [Full Text] [PDF]

				J.-X. He, J. M. Gendron, Y. Sun, S. S. L. Gampala, N. Gendron, C. Q. Sun, and Z.-Y. Wang BZR1 Is a Transcriptional Repressor with Dual Roles in Brassinosteroid Homeostasis and Growth Responses Science, March 11, 2005; 307(5715): 1634 - 1638. [Abstract] [Full Text] [PDF]

				X.-H. Yang, Z.-H. Xu, and H.-W. Xue Arabidopsis Membrane Steroid Binding Protein 1 Is Involved in Inhibition of Cell Elongation PLANT CELL, January 1, 2005; 17(1): 116 - 131. [Abstract] [Full Text] [PDF]

				A. Cano-Delgado, Y. Yin, C. Yu, D. Vafeados, S. Mora-Garcia, J.-C. Cheng, K. H. Nam, J. Li, and J. Chory BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis Development, November 1, 2004; 131(21): 5341 - 5351. [Abstract] [Full Text] [PDF]

				K. H. Nam and J. Li The Arabidopsis Transthyretin-Like Protein Is a Potential Substrate of BRASSINOSTEROID-INSENSITIVE 1 PLANT CELL, September 1, 2004; 16(9): 2406 - 2417. [Abstract] [Full Text] [PDF]

				T. Nomura, C. E. Jager, Y. Kitasaka, K. Takeuchi, M. Fukami, K. Yoneyama, Y. Matsushita, H. Nyunoya, S. Takatsuto, S. Fujioka, et al. Brassinosteroid Deficiency Due to Truncated Steroid 5{alpha}-Reductase Causes Dwarfism in the lk Mutant of Pea Plant Physiology, August 1, 2004; 135(4): 2220 - 2229. [Abstract] [Full Text] [PDF]

				S. Mora-Garcia, G. Vert, Y. Yin, A. Cano-Delgado, H. Cheong, and J. Chory Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis Genes & Dev., February 15, 2004; 18(4): 448 - 460. [Abstract] [Full Text] [PDF]

				A. Dievart and S. E. Clark LRR-containing receptors regulating plant development and defense Development, January 15, 2004; 131(2): 251 - 261. [Abstract] [Full Text] [PDF]

				J. L. Nemhauser and J. Chory BRing it on: new insights into the mechanism of brassinosteroid action J. Exp. Bot., January 2, 2004; 55(395): 265 - 270. [Abstract] [Full Text] [PDF]

				E. M. Turk, S. Fujioka, H. Seto, Y. Shimada, S. Takatsuto, S. Yoshida, M. A. Denzel, Q. I. Torres, and M. M. Neff CYP72B1 Inactivates Brassinosteroid Hormones: An Intersection between Photomorphogenesis and Plant Steroid Signal Transduction Plant Physiology, December 1, 2003; 133(4): 1643 - 1653. [Abstract] [Full Text]

				C. Mussig, G.-H. Shin, and T. Altmann Brassinosteroids Promote Root Growth in Arabidopsis Plant Physiology, November 1, 2003; 133(3): 1261 - 1271. [Abstract] [Full Text] [PDF]

				M. Chono, I. Honda, H. Zeniya, K. Yoneyama, D. Saisho, K. Takeda, S. Takatsuto, T. Hoshino, and Y. Watanabe A Semidwarf Phenotype of Barley uzu Results from a Nucleotide Substitution in the Gene Encoding a Putative Brassinosteroid Receptor Plant Physiology, November 1, 2003; 133(3): 1209 - 1219. [Abstract] [Full Text] [PDF]

				E. D. Shpak, M. B. Lakeman, and K. U. Torii Dominant-Negative Receptor Uncovers Redundancy in the Arabidopsis ERECTA Leucine-Rich Repeat Receptor-Like Kinase Signaling Pathway That Regulates Organ Shape PLANT CELL, May 1, 2003; 15(5): 1095 - 1110. [Abstract] [Full Text]

				Y. Shimada, H. Goda, A. Nakamura, S. Takatsuto, S. Fujioka, and S. Yoshida Organ-Specific Expression of Brassinosteroid-Biosynthetic Genes and Distribution of Endogenous Brassinosteroids in Arabidopsis Plant Physiology, January 1, 2003; 131(1): 287 - 297. [Abstract] [Full Text] [PDF]

				C. S. Thummel and J. Chory Steroid signaling in plants and insects---common themes, different pathways Genes & Dev., December 15, 2002; 16(24): 3113 - 3129. [Full Text] [PDF]

				T. Montoya, T. Nomura, K. Farrar, T. Kaneta, T. Yokota, and G. J. Bishop Cloning the Tomato Curl3 Gene Highlights the Putative Dual Role of the Leucine-Rich Repeat Receptor Kinase tBRI1/SR160 in Plant Steroid Hormone and Peptide Hormone Signaling PLANT CELL, December 1, 2002; 14(12): 3163 - 3176. [Abstract] [Full Text] [PDF]

				D. M. Friedrichsen, J. Nemhauser, T. Muramitsu, J. N. Maloof, J. Alonso, J. R. Ecker, M. Furuya, and J. Chory Three Redundant Brassinosteroid Early Response Genes Encode Putative bHLH Transcription Factors Required for Normal Growth Genetics, November 1, 2002; 162(3): 1445 - 1456. [Abstract] [Full Text] [PDF]

				S. Choe, R. J. Schmitz, S. Fujioka, S. Takatsuto, M.-O. Lee, S. Yoshida, K. A. Feldmann, and F. E. Tax Arabidopsis Brassinosteroid-Insensitive dwarf12 Mutants Are Semidominant and Defective in a Glycogen Synthase Kinase 3beta -Like Kinase Plant Physiology, November 1, 2002; 130(3): 1506 - 1515. [Abstract] [Full Text] [PDF]

				M. Mori, T. Nomura, H. Ooka, M. Ishizaka, T. Yokota, K. Sugimoto, K. Okabe, H. Kajiwara, K. Satoh, K. Yamamoto, et al. Isolation and Characterization of a Rice Dwarf Mutant with a Defect in Brassinosteroid Biosynthesis Plant Physiology, November 1, 2002; 130(3): 1152 - 1161. [Abstract] [Full Text] [PDF]

				J. Zhao, P. Peng, R. J. Schmitz, A. D. Decker, F. E. Tax, and J. Li Two Putative BIN2 Substrates Are Nuclear Components of Brassinosteroid Signaling Plant Physiology, November 1, 2002; 130(3): 1221 - 1229. [Abstract] [Full Text] [PDF]

				E. A. Iliev, W. Xu, D. H. Polisensky, M.-H. Oh, R. S. Torisky, S. D. Clouse, and J. Braam Transcriptional and Posttranscriptional Regulation of Arabidopsis TCH4 Expression by Diverse Stimuli. Roles of cis Regions and Brassinosteroids Plant Physiology, October 1, 2002; 130(2): 770 - 783. [Abstract] [Full Text] [PDF]

				Y. Yin, H. Cheong, D. Friedrichsen, Y. Zhao, J. Hu, S. Mora-Garcia, and J. Chory A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development PNAS, July 23, 2002; 99(15): 10191 - 10196. [Abstract] [Full Text] [PDF]

				G. J. Bishop and C. Koncz Brassinosteroids and Plant Steroid Hormone Signaling PLANT CELL, May 1, 2002; 14(90001): S97 - 110. [Full Text] [PDF]

				A. J.M. Peeters, M. C.H. Cox, J. J. Benschop, R. A.M. Vreeburg, J. Bou, and L. A.C.J. Voesenek Submergence research using Rumex palustris as a model; looking back and going forward J. Exp. Bot., March 1, 2002; 53(368): 391 - 398. [Abstract] [Full Text] [PDF]

				J. Li and K. H. Nam Regulation of Brassinosteroid Signaling by a GSK3/SHAGGY-Like Kinase Science, February 15, 2002; 295(5558): 1299 - 1301. [Abstract] [Full Text] [PDF]

				J. Leon, J. Royo, G. Vancanneyt, C. Sanz, H. Silkowski, G. Griffiths, and J. J. Sanchez-Serrano Lipoxygenase H1 Gene Silencing Reveals a Specific Role in Supplying Fatty Acid Hydroperoxides for Aliphatic Aldehyde Production J. Biol. Chem., January 4, 2002; 277(1): 416 - 423. [Abstract] [Full Text]

				G. J. Budziszewski, S. P. Lewis, L. W. Glover, J. Reineke, G. Jones, L. S. Ziemnik, J. Lonowski, B. Nyfeler, G. Aux, Q. Zhou, et al. Arabidopsis Genes Essential for Seedling Viability: Isolation of Insertional Mutants and Molecular Cloning Genetics, December 1, 2001; 159(4): 1765 - 1778. [Abstract] [Full Text] [PDF]

				T. Bouquin, C. Meier, R. Foster, M. E. Nielsen, and J. Mundy Control of Specific Gene Expression by Gibberellin and Brassinosteroid Plant Physiology, October 1, 2001; 127(2): 450 - 458. [Abstract] [Full Text] [PDF]

				J. Li, K. H. Nam, D. Vafeados, and J. Chory BIN2, a New Brassinosteroid-Insensitive Locus in Arabidopsis Plant Physiology, September 1, 2001; 127(1): 14 - 22. [Abstract] [Full Text] [PDF]

				D. R. Corbin, R. J. Grebenok, T. E. Ohnmeiss, J. T. Greenplate, and J. P. Purcell Expression and Chloroplast Targeting of Cholesterol Oxidase in Transgenic Tobacco Plants Plant Physiology, July 1, 2001; 126(3): 1116 - 1128. [Abstract] [Full Text] [PDF]

				H. Li, J.-J. Shen, Z.-L. Zheng, Y. Lin, and Z. Yang The Rop GTPase Switch Controls Multiple Developmental Processes in Arabidopsis Plant Physiology, June 1, 2001; 126(2): 670 - 684. [Abstract] [Full Text] [PDF]

				Y. Shimada, S. Fujioka, N. Miyauchi, M. Kushiro, S. Takatsuto, T. Nomura, T. Yokota, Y. Kamiya, G. J. Bishop, and S. Yoshida Brassinosteroid-6-Oxidases from Arabidopsis and Tomato Catalyze Multiple C-6 Oxidations in Brassinosteroid Biosynthesis Plant Physiology, June 1, 2001; 126(2): 770 - 779. [Abstract] [Full Text] [PDF]

				J. Li, K. A. Lease, F. E. Tax, and J. C. Walker BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana PNAS, April 18, 2001; (2001) 91065998. [Abstract] [Full Text]

				M. Fellner, R. Zhang, R. P. Pharis, and V. K. Sawhney Reduced de-etiolation of hypocotyl growth in a tomato mutant is associated with hypersensitivity to, and high endogenous levels of, abscisic acid J. Exp. Bot., April 15, 2001; 52(357): 725 - 738. [Abstract] [Full Text] [PDF]

				G. J. Bishop and T. Yokota Plants Steroid Hormones, Brassinosteroids: Current Highlights of Molecular Aspects on their Synthesis/Metabolism, Transport, Perception and Response Plant Cell Physiol., February 1, 2001; 42(2): 114 - 120. [Abstract] [Full Text] [PDF]

				R. Yamamoto, S. Fujioka, T. Demura, S. Takatsuto, S. Yoshida, and H. Fukuda Brassinosteroid Levels Increase Drastically Prior to Morphogenesis of Tracheary Elements Plant Physiology, February 1, 2001; 125(2): 556 - 563. [Abstract] [Full Text]

				C. M. Steber and P. McCourt A Role for Brassinosteroids in Germination in Arabidopsis Plant Physiology, February 1, 2001; 125(2): 763 - 769. [Abstract] [Full Text]

				C. Lu and N. Fedoroff A Mutation in the Arabidopsis HYL1 Gene Encoding a dsRNA Binding Protein Affects Responses to Abscisic Acid, Auxin, and Cytokinin PLANT CELL, December 1, 2000; 12(12): 2351 - 2366. [Abstract] [Full Text]

				M.-H. Oh, W. K. Ray, S. C. Huber, J. M. Asara, D. A. Gage, and S. D. Clouse Recombinant Brassinosteroid Insensitive 1 Receptor-Like Kinase Autophosphorylates on Serine and Threonine Residues and Phosphorylates a Conserved Peptide Motif in Vitro Plant Physiology, October 1, 2000; 124(2): 751 - 766. [Abstract] [Full Text]

				T. Noguchi, S. Fujioka, S. Choe, S. Takatsuto, F. E. Tax, S. Yoshida, and K. A. Feldmann Biosynthetic Pathways of Brassinolide in Arabidopsis Plant Physiology, September 1, 2000; 124(1): 201 - 210. [Abstract] [Full Text]

				D. M. Friedrichsen, C. A.P. Joazeiro, J. Li, T. Hunter, and J. Chory Brassinosteroid-Insensitive-1 Is a Ubiquitously Expressed Leucine-Rich Repeat Receptor Serine/Threonine Kinase Plant Physiology, August 1, 2000; 123(4): 1247 - 1256. [Abstract] [Full Text]

				S.-K. Kim, S. C. Chang, E. J. Lee, W.-S. Chung, Y.-S. Kim, S. Hwang, and J. S. Lee Involvement of Brassinosteroids in the Gravitropic Response of Primary Root of Maize Plant Physiology, July 1, 2000; 123(3): 997 - 1004. [Abstract] [Full Text]

				J.-C. Jang, S. Fujioka, M. Tasaka, H. Seto, S. Takatsuto, A. Ishii, M. Aida, S. Yoshida, and J. Sheen A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana Genes & Dev., June 15, 2000; 14(12): 1485 - 1497. [Abstract] [Full Text]

				J.-C. Cheng, K. Lertpiriyapong, S. Wang, and Z. R. Sung The Role of the Arabidopsis ELD1 Gene in Cell Development and Photomorphogenesis in Darkness Plant Physiology, June 1, 2000; 123(2): 509 - 520. [Abstract] [Full Text]

				C. V. Koka, R. E. Cerny, R. G. Gardner, T. Noguchi, S. Fujioka, S. Takatsuto, S. Yoshida, and S. D. Clouse A Putative Role for the Tomato Genes DUMPY and CURL-3 in Brassinosteroid Biosynthesis and Response Plant Physiology, January 1, 2000; 122(1): 85 - 98. [Abstract] [Full Text] [PDF]