AJPS  Vol.4 No.2 , February 2013
Genetic Background Influences Brassinosteroid-Related Mutant Phenotypes in Rice
ABSTRACT
In two cases, mutations in the same brassinosteroid-related genes caused different phenotypes in japonica varieties Nipponbare and Taichung 65. The mutant phenotypes were less severe in the Taichung 65 background than in the Nipponbare background. Three newly isolated brassinosteroid-insensitive mutants (d61-1N, d61-11, and d61-12) derived from a Nipponbare mutant library were found to be alleles of d61, which represent defects in the OsBRI1 gene. Although the Nipponbare-derived mutant d61-1N had the same nucleotide substitution as the previously characterized Taichung 65-derived mutant d61-1T, these two mutants showed different phenotypes for plant stature, internode elongation pattern, and seed shape; in each case, d61-1N (in the Nipponbare genetic background) had the more severe mutant phenotype. Similar trends were seen for phenotypes caused by mutants of d2, a brassinosteroid biosynthesis gene. Consistent with these phenotypes, the expression of brassinosteroid-responsive genes was lower in the Nipponbare-derived mutants. These results can be explained by our findings that feed-forward up-regulation of OsBRI1 did not occur in the Nipponbare-derived mutants and that an mPing transposon is inserted into the promoter region of Nipponbare OsBRI1. Based on these results, we conclude that the expression of OsBRI1, especially its feed-forward up-regulation, is misregulated in wild-type Nipponbare and in brassinosteroid-related mutants in a Nipponbare genetic background. Although Nipponbare is a model rice genotype, it can be categorized as an OsBRI1 mutant that has reduced sensitivity to brassinosteroid.

Cite this paper
T. Sakamoto, H. Kitano and S. Fujioka, "Genetic Background Influences Brassinosteroid-Related Mutant Phenotypes in Rice," American Journal of Plant Sciences, Vol. 4 No. 2, 2013, pp. 212-221. doi: 10.4236/ajps.2013.42028.
References
[1]   S. D. Clouse and J. M. Sasse, “Brassinosteroids: Essential Regulators of Plant Growth and Development,” Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 49, 1998, pp. 427-451. doi:10.1146/annurev.arplant.49.1.427

[2]   J. M. Sasse, “Physiological Action of Brassinosteroids: An Update,” Journal of Plant Growth Regulation, Vol. 22, No. 4, 2003, pp. 276-288. doi:10.1007/s00344-003-0062-3

[3]   P. Krishna, “Brassinosteroid-Mediated Stress Responses,” Journal of Plant Growth Regulation, Vol. 22, No. 4, 2003, pp. 289-297. doi:10.1007/s00344-003-0058-z

[4]   G. J. Bishop and T. Yokota, “Plant Steroid Hormones, Brassinosteroids: Current Highlights of Molecular Aspects on Their Synthesis/Metabolism, Transport, Perception and Response,” Plant and Cell Physiology, Vol. 42, No. 2, 2001, pp. 114-120. doi:10.1093/pcp/pce018

[5]   S. Fujioka and T. Yokota, “Biosynthesis and Metabolism of Brassinosteroids,” Annual Review of Plant Biology, Vol. 54, 2003, pp. 137-164. doi:10.1146/annurev.arplant.54.031902.134921

[6]   T. Sakamoto, Y. Morinaka, T. Ohnishi, H. Sunohara, S. Fujioka, M. Ueguchi-Tanaka, M. Mizutani, K. Sakata, S. Takatsuto, S. Yoshida, H. Tanaka, H. Kitano and M. Matsuoka, “Erect Leaves Caused by Brassinosteroid Deficiency Increase Biomass Production and Grain Yield in Rice,” Nature Biotechnology, Vol. 24, No. 1, 2006, pp. 105-109. doi:10.1038/nbt1173

[7]   T. Sakamoto, T. Ohnishi, S. Fujioka, B. Watanabe and M. Mizutani, “Rice CYP90D2 and CYP90D3 Catalyze C-23 Hydroxylation of Brassinosteroids in Vitro,” Plant Physiology and Biochemistry, Vol. 58, 2012, pp. 220-226. doi:10.1016/j.plaphy.2012.07.011

[8]   Z. Hong, M. Ueguchi-Tanaka, S. Shimizu-Sato, Y. Inukai, S. Fujioka, Y. Shimada, S. Takatsuto, M. Agetsuma, S. Yoshida, Y. Watanabe, S. Uozu, H. Kitano, M. Ashikari and M. Matsuoka, “Loss-of-Function of a Rice Brassinosteroid Biosynthetic Enzyme, C-6 Oxidase, Prevents the Organized Arrangement and Polar Elongation of Cells in the Leaves and Stem,” Plant Journal, Vol. 32, No. 4, 2002, pp. 495-508. doi:10.1046/j.1365-313X.2002.01438.x

[9]   M. Mori, T. Nomura, H. Ooka, M. Ishizaka, T. Yokota, K. Sugimoto, K. Okabe, H. Kajiwara, K. Satoh, K. Yamamoto, H. Hirochika and S. Kikuchi, “Isolation and Characterization of a Rice Dwarf Mutant with a Defect in Brassinosteroid Biosynthesis,” Plant Physiology, Vol. 130, No. 3, 2002, pp. 1152-1161. doi:10.1104/pp.007179

[10]   T. Sakamoto and M. Matsuoka, “Characterization of Constitutive Photomorphogenesis and Dwarfism Homologs in Rice (Oryza sativa L.),” Journal of Plant Growth Regulation, Vol. 25, No. 3, 2006, pp. 245-251. doi:10.1007/s00344-006-0041-6

[11]   A. Bajguz and A. Tretyn, “The Chemical Characteristic and Distribution of Brassinosteroids in Plants,” Phytochemistry, Vol. 62, No. 7, 2003, pp. 1027-1046. doi:10.1016/S0031-9422(02)00656-8

[12]   B. K. Kim, S. Fujioka, S. Takatsuto, M. Tsujimoto and S. Choe, “Castasterone Is a Likely End Product of Brassinosteroid Biosynthetic Pathway in Rice,” Biochemical and Biophysical Research Communications, Vol. 374, No. 4, 2008, pp. 614?-619.

[13]   T. W. Kim and Z. Y. Wang, “Brassinosteroid Signal Transduction from Receptor Kinases to Transcription Factors,” Annual Review of Plant Biology, Vol. 61, 2010, pp. 681-704. doi:10.1146/annurev.arplant.043008.092057

[14]   S. D. Clouse, “Brassinosteroid Signal Transduction: From Receptor Kinase Activation to Transcriptional Networks Regulating Plant Development,” Plant Cell, Vol. 23, No. 4, 2011, pp. 1219-1230. doi:10.1105/tpc.111.084475

[15]   C. Yamamuro, Y. Ihara, X. Wu, T. Noguchi, S. Fujioka, S. Takatsuto, M. Ashikari, H. Kitano and M. Matsuoka, “Loss of Function of a Rice Brassinosteroid Insensitive1 Homolog Prevents Internode Elongation and Bending of the Lamina Joint,” Plant Cell, Vol. 12, No. 9, 2000, pp. 1591-1606.

[16]   A. Nakamura, S. Fujioka, H. Sunohara, N. Kamiya, Z. Hong, Y. Inukai, K. Miura, S. Takatsuto, S. Yoshida, M. Ueguchi-Tanaka, Y. Hasegawa, H. Kitano and M. Matsuoka, “The Role of OsBRI1 and Its Homologous Genes, OsBRL1 and OsBRL3, in Rice,” Plant Physiology, Vol. 140, No. 2, 2006, pp. 580-590. doi:10.1104/pp.105.072330

[17]   H. Tong, Y. Jin, W. Liu, F. Li, J. Fang, Y. Yin, Q. Qian, L. Zhu and C. Chu, “Dwarf and Low-Tillering, a New Member of the GRAS Family, Plays Positive Roles in Brassinosteroid Signaling in Rice,” Plant Journal, Vol. 58, No. 5, 2009, pp. 803-816. doi:10.1111/j.1365-313X.2009.03825.x

[18]   C. Zhang, Y. Xu, S. Guo, J. Zhu, Q. Huan, H. Liu, L. Wang, G. Luo, X. Wang and K. Chong, “Dynamics of Brassinosteroid Response Modulated by Negative Regulator LIC in Rice,” PLoS Genetics, Vol. 8, 2012, e100-2686. doi:10.1371/journal.pgen.1002686

[19]   H. Hirochika, K. Sugimoto, Y. Otsuki, H. Tsugawa and M. Kanda, “Retrotransposons of Rice Involved in Mutations Induced by Tissue Culture,” Proceedings of the National Academy of Sciences of the United States of America, Vo. 93, No. 15, 1996, pp. 7783-7788. doi:10.1073/pnas.93.15.7783

[20]   Y. Hiei, S. Ohta, T. Komari and T. Kumashiro, “Efficient Transformation of RIce (Oryza sativa L.) Mediated by Agrobacterium and Sequence Analysis of Boundaries of the T-DNA,” Plant Journal, Vol. 6, No. 2, 1994, pp. 271-282. doi:10.1046/j.1365-313X.1994.6020271.x

[21]   E. Maeda, “Rate of Lamina Inclination in Excised Rice Leaves,” Physiologia Plantarum, Vol. 18, No. 3, 1965, pp. 813-827. doi:10.1111/j.1399-3054.1965.tb06940.x

[22]   K. Wada, S. Marumo, N. Ikekawa, M. Morisaki and K. Mori, “Brassinolide and Homobrassinolide Promotion of Lamina Inclination of Rice Seedlings,” Plant and Cell Physiology, Vol. 22, No. 2, 1981, pp. 323-325.

[23]   K. Takeno and R. P. Pharis, “Brassinosteroid-Induced Bending of the Leaf Lamina of Dwarf Rice Seedlings: An Auxin-Mediated Phenomenon,” Plant and Cell Physiology, Vol. 23, No. 7, 1982, pp. 1275-1281.

[24]   S. Fujioka, T. Noguchi, S. Takatsuto and S. Yoshida, “Activity of Brassinosteroids in the Dwarf Rice Lamina Inclination Bioassay,” Phytochemistry, Vol. 49, No. 7, 1998, pp. 1841-1848. doi:10.1016/S0031-9422(98)00412-9

[25]   Y. Morinaka, T. Sakamoto, Y. Inukai, M. Agetsuma, H. Kitano, M. Ashikari and M. Matsuoka, “Morphological Alteration Caused by Brassinosteroid Insensitivity Increases the Biomass and Grain Production of Rice,” Plant Physiology, Vol. 141, No. 3, 2006, pp. 924-931. doi:10.1104/pp.106.077081

[26]   S. Tanabe, M. Ashikari, S. Fujioka, S. Takatsuto, S. Yoshida, M. Yano, A. Yoshimura, H. Kitano, M. Matsuoka, Y. Fujisawa, H. Kato and Y. Iwasaki, “A Novel Cytochrome P450 Is Implicated in Brassinosteroid Biosynthesis via the Characterization of a Rice Dwarf Mutant, dwarf11, with Reduced Seed Length,” Plant Cell, Vol. 17, No. 3, 2005, pp. 776-790. doi:10.1105/tpc.104.024950

[27]   K. Takeda, “Internode Elongation and Dwarfism in Some Gramineous Plants,” Gamma Field Symposium, Vol. 16, 1977, pp. 1-18.

[28]   Z. Hong, M. Ueguchi-Tanaka, K. Umemura, S. Uozu, S. Fujioka, S. Takatsuto, S. Yoshida, M. Ashikari, Kitano and M. Matsuoka, “A Rice Brassinosteroid-Deficient Mutant, ebisu dwarf (d2), Is Caused by a Loss of Function of a New Member of Cytochrome P450,” Plant Cell, Vol. 15, No. 12, 2003, pp. 2900-2910. doi:10.1105/tpc.014712

[29]   K. Hoshikawa, “Stem,” In: K. Hoshikawa, Ed., The Growing Rice Plant, Nobunkyo, Tokyo, 1989, pp. 123-148.

[30]   T. Sakamoto, Y. Morinaka, H. Kitano and S. Fujioka, “New Alleles of Rice ebisu dwarf (d2) Mutant Show Both Brassinosteroid-Deficient and -Insensitive Phenotypes,” American Journal of Plant Sciences, Vol. 3, No. 12, pp. 1699-1707.

[31]   A. Tanaka, H. Nakagawa, C. Tomita, Z. Shi-matani, M. Ohtake, T. Nomura, C. J. Jiang, J. G. Dubouzet, S. Kikuchi, H. Sekimoto, T. Yokota, T. Asami, T. Kamakura and M. Mori, “BRASSINOSTEROID UPREGULATED1, Encoding a Helix-Loop-Helix Protein, Is a Novel Gene Involved in Brassinosteroid Signaling and Controls Bending of the Lamina Joint in Rice,” Plant Physiology, Vol. 151, No. 2, 2009, pp. 669-680. doi:10.1104/pp.109.140806

[32]   N. Jiang, Z. Bao, X. Zhang, H. Hirochika, S. R. Eddy, S. R. McCouch and S. R. Wessler, “An Active DNA Transposon Family in Rice,” Nature, Vol. 421, No. 6919, 2003, pp. 163-167. doi:10.1038/nature01214

[33]   K. Kikuchi, K. Terauchi, M. Wada and H. Y. Hirano, “The Plant MITE mPing Is Mobilized in another Culture,” Nature, Vol. 421, No. 6919, 2003, pp. 167-170. doi:10.1038/nature01218

[34]   T. Nakazaki, Y. Okumoto, A. Horibata, S. Yamahira, M. Teraishi, H. Nishida, H. Inoue and T. Tanisaka, “Mobilization of a Transposon in the Rice Genome,” Nature, Vol. 421, No. 6919, 2003, pp. 170-172. doi:10.1038/nature01219

[35]   Y. Ohmori, M. Abiko, A. Horibata and H. Y. Hirano, “A Transposon, Ping, Is Integrated into Intron 4 of the DROOPING LEAF Gene of Rice, Weakly Reducing Its Expression and Causing a Mild Drooping Leaf Phenotype,” Plant and Cell Physiology, Vol. 49, No. 8, 2008, pp. 1176-1184. doi:10.1093/pcp/pcn093

 
 
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