Abstract
A rice (Oryza sativa L.) semi-dwarf cultivar, Tan-Ginbozu (d35 Tan-Ginbozu), contributed to the increase in crop productivity in Japan in the 1950s. Previous studies suggested that the semi-dwarf stature of d35 Tan-Ginbozu is caused by a defective early step of gibberellin biosynthesis, which is catalyzed by ent-kaurene oxidase (KO). To study the molecular characteristics of d35 Tan-Ginbozu, we isolated 5 KO-like(KOL) genes from the rice genome, which encoded proteins highly homologous to Arabidopsis and pumpkin KOs. The genes (OsKOL1to5) were arranged as tandem repeats in the same direction within a 120 kb sequence. Expression analysis revealed that OsKOL2 and OsKOL4 were actively transcribed in various organs, while OsKOL1 and OsKOL5 were expressed only at low levels; OsKOL3 may be a pseudogene. Sequence analysis and complementation experiments demonstrated that OsKOL2corresponds to D35. Homozygote with null alleles of D35showed a severe dwarf phenotype; therefore, d35 Tan-Ginbozu is a weak allele of D35. Introduction of OsKOL4 into d35 Tan-Ginbozu did not rescue its dwarf phenotype, indicating that OsKOL4 is not involved in GA biosynthesis. OsKOL4 and OsKOL5 are likely to take part in phytoalexin biosynthesis, because their expression was promoted by UV irradiation and/or elicitor treatment. Comparing d35 Tan-Ginbozu with other high yielding cultivars, we discuss strategies to produce culm architectures suitable for high crop yield by decreasing GA levels.
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REFERENCES
Ashikari, M., Sasaki, A., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Swapan, D., Ishiyama, K., Saito, T., Kobayashi, M., Khush, G.S., Kitano, H. and Matsuoka, M. 2002.Loss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), led to the rice 'Green Revolution'. Breed Sci. 52: 143–150.
Evans, L.T. 1998. Feeding the ten billion. Plant and Population Growth. Cambridge University Press, Cambridge.
Feng, Q., Zhang, Y., Hao, P., Wang, S., Fu, G., Huang, Y., Li, Y., Zhu, J., Liu, Y., Hu, X. et al. 2002. Sequence and analysis of rice chromosome 4. Nature 420: 316–320.
Goff, S.A., Ricke, D., Lan, T.H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P.H. et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92–100.
Hedden, P. 2003. The genes of the green revolution. Trends in Genetics 19: 5–9.
Helliwell, C.A., Sheldon, C.C., Olive, M.R., Walker, A.R.W., Zeevaart, J.A.D., Peacock, W.J. and Dennis, E.S. 1998. Cloning of the Arabidopsis ent-kaurene oxidase gene GA3. Proc. Natl. Acad. Sci. USA 95: 9019–9024.
Helliwell, C.A., Olive, M.R., Gebbie, L., Forster, R., Peacock, W.J. and Dennis, E.S. 2000. Isolation of an ent-kaurene oxidase cDNA from Cucurbita maxima. Aust. J. Plant. Physiol. 27: 1141–1149.
Itoh, H., Ueguchi-Tanaka, M., Sentoku, N., Kitano, H., Matsuoka, M. and Kobayashi, M. 2001. Cloning and functional analysis of gibberellin 3b-hydroxylase genes that are differently expressed during the growth of rice. Proc. Natl. Acad. Sci. USA 98: 8909–8914.
Izumi, K., Kamiya, Y., Sakurai, A., Oshio, H. and Takahashi, N. 1985. Studies of sites of action of a new plant growth retardant (E)-1-(4-chloro-phenyl)-4,4-dimethyl-2-(1,2,4-triazol-1-yl)-1-penten-3-ol (S-3307) and comparative effects of its stereoisomers in a cell-free system from Cucurbita maxima. Plant. Cell. Physiol. 26: 821–827.
Kaneko, M., Itoh, H., Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Ashikari, M. and Matsuoka, M. 2003. Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J. 35: 104–115.
Kato, H., Kodama, O. and Akatsuka, T. 1995. Characterization of an inducible P450 hydroxylase involved in the rice diterpene phytoalexin biosynthetic pathway. Arch. Biochem. Biophys. 316: 707–712.
Khush, G.S. 1999. Green revolution: preparing for the 21st century. Genome 42: 646–655.
Kikuchi, S., Satoh, K., Nagata, T., Kawagashira, N., Doi, K., Kishimoto, N., Yazaki, J., Ishikawa, M., Yamada, H., Ooka, H. et al. 2003. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301: 376–379.
Kuchitsu, K., Kikuyama, M. and Shibuya, N. 1993. Nacetylchitooligosaccharides, biotic elicitor for phytoalexin production, induce transient membrane depolarization in suspension-cultured rice cells. Protoplasma 174: 79–81.
Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincon, S.E. and Newburg, L. 1987. MAPMAKER: an interactive computer package for constructing primery genetic linkage maps of experimental and natural populations. Genomics 1: 174–181.
Lei, H-Y., Zhou, B., Zhang, Y., Hong, G-F. and Han, B. 2002. Structural analysis of a gene cluster encoding DFR-like proteins from rice chromosome 4. Acta. Biochem. Biophys. Sinica 34: 685–689.
Lynch, M. and Conery, J.S. 2000. The evolutional fate and consequences of duplicate genes. Science 290: 1151–1155.
Lin, S.Y., Sasaki, T. and Yano, M. 1998. Mapping quantitative trait loci controlling seed dormacy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theo. Appl. Genet. 96: 997–1003.
Mohan, R.S., Yee, N.K., Coates, R.M., Ren, Y.Y., Stamenkovic, P., Mendez, I. and West, C.A. 1996. Biosynthesis of cyclic diterpene hydrocarbons in rice cell suspensions: conversion of 9,10-syn-labda-8 (17),13-dienyl diphosphate to 9-pimara-7,15-diene and stemar-13-ene. Arch. Biochem. Biophys. 330: 33–47.
Moore, T.C., Yamane, H., Murofushi, N. and Takahashi, N. 1988. Concentrations of ent-kaurene and squalene in vegetative rice shoots. J. Plant Growth. Regul. 7: 145–151.
Murakami, Y. 1968. A new rice seedling test for gibberellin, 'Microdrop method', and its use for testing extracts of rice and morning glory. Bot. Mag. Tokyo 81: 33–43.
Murakami, Y. 1972. Dwarfing genes in rice and their relation to gibberellin biosynthesis. In DJ Carr, (Ed.), Plant Growth Substances. Springer-Verlag, Berlin, pp. 166–174
Ogawa, S., Toyomasu, T., Yamane, H., Murofushi, N., Ikeda, R., Morimoto, Y., Nishimura, Y. and Omori, T. 1996. A step in the biosynthesis of gibberellins that is controlled by the mutation in the semi-dwarf rice cultivar Tan-Ginbozu. Plant Cell Physiol. 37: 363–368.
Peng, J., Richards, D.E., Hartley, N.M., Murphy, G.P., Devos, K.M., Flintham, J.E., Beales, J., Fish, L.J., Worland, A.J., Pelica, F., Sudhakar, D., Christou, P.J.W., Gale, M.D. and Harberd, N.P. 1999. 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400: 256–261.
Sakamoto, T., Miura, K., Itoh, H., Tatsumi, T., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Agrawal, G. K., Takeda, S., Abe, K., Miyao, A., Hirochika, H., Kitano, H., Ashikari, M. and Matsuoka, M. 2004. An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 134: 1642–1653.
Sasaki, A., Ashikari, M., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Swapan, D., Ishiyama, K., Saito, T., Kobayashi, M., Khush,G.S., Kitano,H.and Matsuoka, M.2002a. A mutant gibberellin-synthesis gene in rice. Nature 416: 701–702.
Sasaki, T., Matsumoto, T., Yamamoto, K., Sakata, K., Baba, T., Katayose, Y., Wu, J., Niimura, Y., Cheng, Z., Nagamura, Y. et al. 2002b. The genome sequence and structure of rice chromosome 1. Nature 420: 312–316.
Sentoku, N., Sato, Y. and Matsuoka, M. 2000. Overexpression of rice OSH genes induces ectopic shoots on leaf sheaths of transgenic rice plants. Develop. Biol. 220: 358–364.
Shinbashi, N., Kinoshita, T. and Takahashi, M. 1975. Gibberellin metabolism by the causal genes for 'Hosetsu-dwarf' and 'Tanginbozu-dwarf' (preliminary report)-genetic studies on rice plants, LXIII-. Mem. Fac. Agr. Hokkaido Univ. 9: 201–207.
Spielmeyer, W., Ellis, M. and Chandler, P. 2002. Semidwarf (sd-1), green revolution rice, contains a defective gibberellin 20-oxidase gene. Proc. Natl. Acad. Sci. USA 99: 9043–9048.
Suge, H. and Murakami, Y. 1968. Occurrence of a rice mutant deficient in gibberellin-like substances. Plant Cell Physiol. 9: 411–414.
Vision, T.J., Brown, D.G. and Tanksley, S.D. 2000. The origin of genomic duplication in Arabidopsis. Science 290: 2114–2117.
Ware, D. and Stein, L. 2003. Comparison of genes among cereals. Cur. Opin. Plant. Biol. 6: 121–127.
Wickham, K.A. and West, C.A. 1992. Biosynthesis of rice phytoalexins: identification of putative diterpene hydrocarbon precursors. Arch. Biochem. Biophys. 293: 320–332.
Yamada, A., Shibuya, N., Kodama, O. and Akatsuka, T. 1993. Induction of phytoalexin formation in suspensioncultured rice cells by N-acetylchitooligosaccharides. Biosci. Biotech. Biochem. 57: 405–409.
Yu, J., Hu, S., Wang, J., Wong, G.K., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X. et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79–92.
Zhang, W., McElroy, D. and Wu, R. 1991. Analysis of rice Act1 5' region activity in transgenic rice plants. Plant Cell 3: 1155–1165.
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Itoh, H., Tatsumi, T., Sakamoto, T. et al. A Rice Semi-Dwarf Gene, Tan-Ginbozu (D35), Encodes the Gibberellin Biosynthesis Enzyme, ent-Kaurene Oxidase. Plant Mol Biol 54, 533–547 (2004). https://doi.org/10.1023/B:PLAN.0000038261.21060.47
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DOI: https://doi.org/10.1023/B:PLAN.0000038261.21060.47