A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length

Plant Cell

Volumn 17, Issue 3, 2005, Pages 776-790

  Tanabe, Sumiyo ^a   Ashikari, Motoyuki ^b   Fujioka, Shozo ^c   Takatsuto, Suguru ^d   Yoshida, Shigeo ^c   Yano, Masahiro ^e   Yoshimura, Atsushi ^f   Kitano, Hidemi ^b   Matsuoka, Makoto ^b   Fujisawa, Yukiko ^a   Kato, Hisaharu ^a   Iwasaki, Yukimoto ^a  

^a FUKUI PREFECTURAL UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^d JOETSU UNIVERSITY OF EDUCATION   (Japan)

^e NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^f KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CLONING; ENZYMES; GENES; MUTAGENESIS; PLANTS (BOTANY); RNA; SEED;

BIOSYNTHESIS NETWORK; BRASSINOLIDE (BL); BRASSINOSTEROID (BR); RICE;

BIOSYNTHESIS;

BIOSYNTHESIS; CLONES; ENZYMES; GENES; MUTATION; NUCLEIC ACIDS; PLANTS;

ORYZA SATIVA;

CYTOCHROME P450; HETEROCYCLIC STEROID; PHYTOHORMONE; PLANT DNA;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CHROMOSOME MAP; GENE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PLANT SEED; RADIATION EXPOSURE; RICE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHROMOSOME MAPPING; CYTOCHROME P-450 ENZYME SYSTEM; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC COMPLEMENTATION TEST; LIGHT; MOLECULAR SEQUENCE DATA; MUTATION; ORYZA SATIVA; PHENOTYPE; PHYLOGENY; PLANT GROWTH REGULATORS; SEEDS; SEQUENCE HOMOLOGY, AMINO ACID; STEROIDS, HETEROCYCLIC;

EID: 27244450198     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.024950     Document Type: Article

References (51)

1. Ashikari, M., Wu, J., Yano, M., Sasaki, T., and Yoshimura, A. (1999). Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the α-subunit of GTP-binding protein. Proc. Natl. Acad. Sci. USA 96, 10284-10289.
2. Azpiroz, R., Wu, Y., LoCascio, J.C., and Feldmann, K.A. (1998). An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10, 219-230.
3. Baba, T., et al. (2000). Construction and characterization of rice genomic libraries: PAC library of japonica variety, Nipponbare and BAC library of indica variety. Kasalath. Bull. Natl. Inst. Agrobiol. Resour. 14, 41-49.
4. Bak, S., and Feyereisen, R. (2001). The involvement of two P450 enzymes, CYP83B1 and CYP83A1, in auxin homeostasis and glucosinolate biosynthesis. Plant Physiol. 127, 108-118.
5. Bancos, S., Nomura, T., Sato, T., Molnar, G., Bishop, G.J., Koncz, C., Yokota, T., Nagy, F., and Szekeres, M. (2002). Regulation of transcript levels of the Arabidopsis cytochrome P450 genes involved in brassinosteroid biosynthesis. Plant Physiol. 130, 504-513.
6. Bishop, G.J., Harrison, K., and Jones, J.D. (1996). The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell 8, 959-969.
7. Bishop, G.J., Nomura, T., Yokota, T., Harrison, K., Noguchi, T., Fujioka, S., Takatsuto, S., Jones, J.D., and Kamiya, Y. (1999). The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis. Proc. Natl. Acad. Sci. USA 96, 1761-1766.
8. Choe, S., Dilkes, B.P., Fujioka, S., Takatsuto, S., Sakurai, A., and Feldmann, K.A. (1998). The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10, 231-243.
9. Choe, S., Dilkes, B.P., Gregory, B.D., Ross, A.S., Yuan, H., Noguchi, T., Fujioka, S., Takatsuto, S., Tanaka, A., Yoshida, S., Tax, F.E., and Feldmann, K.A. (1999b). The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiol. 119, 897-907.
10. Choe, S., Noguchi, T., Fujioka, S., Takatsuto, S., Tissier, C.P., Gregory, B.D., Ross, A.S., Tanaka, A., Yoshida, S., Tax, F.E., and Feldmann, K.A. (1999a). The Arabidopsis dwf7/ste1 mutant is defective in the Δ 7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11, 207-221.
11. Choe, S., Tanaka, A., Noguchi, T., Fujioka, S., Takatsuto, S., Ross, A.S., Tax, F.E., Yoshida, S., and Feldmann, K.A. (2000). Lesions in the sterol Δ reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J. 21, 431-443.
12. Chory, J. (1993). Out of darkness: Mutants reveal pathways controlling light-regulated development in plants. Trends Genet. 9, 167-172.
13. Chory, J., Nagpal, P., and Peto, C.A. (1991). Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3, 445-459.
14. Clouse, S.D., and Sasse, J.M. (1998). Brassinosteroids: Essential regulators of plant growth and development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 427-451.
15. Fujioka, S., Noguchi, T., Takatsuto, S., and Yoshida, S. (1998). Activity of brassinosteroid in the dwarf rice lamina inclination bioassay. Phytochemistry 49, 1841-1848.
16. Fujioka, S., and Yokota, T. (2003). Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54, 137-164.
17. Fujisawa, Y., Kato, T., Ohki, S., Ishikawa, A., Kitano, H., Sasaki, T., Asahi, T., and Iwasaki, Y. (1999). Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. Proc. Natl. Acad. Sci. USA 96, 7575-7580.
18. Fuse, T., Sasaki, T., and Yano, M. (2001). Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol. 18, 219-222.
19. 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.
20. Harushima, Y., et al. (1998). A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148, 479-494.
21. He, J.X., Gendron, J.M., Yang, Y., Li, J., and Wang, Z.Y. (2002). The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 10185-10190.
22. Helliwell, C.A., Chandler, P.M., Poole, A., Dennis, E.S., and Peacock, W.J. (2001). The CYP88A cytochrome P450, enf-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc. Natl. Acad. Sci. USA 98, 2065-2070.
23. Hiei, Y., Ohta, S., Komari, T., and Kumashiro, T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282.
24. Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H., and Kanda, M. (1996). Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci. USA 93, 7783-7788.
25. Hong, Z., et al. (2002). 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 J. 32, 495-508.
26. Hong, Z., Ueguchi-Tanaka, M., Umemura, K., Uozu, S., Fujioka, S., Takatsuto, S., Yoshida, S., Ashikari, M., Kitano, H., and Matsuoka, M. (2003). A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15, 2900-2910.
27. Huelsken, J., and Birchmeier, W. (2001). New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11, 547-553.
28. Hull, A.K., Vij, R., and Celenza, J.L. (2000). Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc. Natl. Acad. Sci. USA 97, 2379-2384.
29. Iwata, N., Satoh, H., and Omura, T. (1984). The relationships between chromosomes identified cytologically and linkage groups. Rice Genet. Newsl. 1, 128-132.
30. Jang, J.C., Fujioka, S., Tasaka, M., Seto, H., Takatsuto, S., Ishii, A., Aida, M., Yoshida, S., and Sheen, J. (2000). A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev, 14, 1485-1497.
31. Kalb, V.F., and Loper, J.C. (1988). Proteins from eight eukaryotic cytochrome P-450 families share a segmented region of sequence similarity. Proc. Natl. Acad. Sci. USA 85, 7221-7225.
32. Kim, G.T., Tsukaya, H., and Uchimiya, H. (1998). The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev. 12, 2381-2391.
33. Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929-938.
34. Li, J., and Nam, K.H. (2002). Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295, 1299-1301.
35. Li, J., Wen, J., Lease, K.A., Poke, 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.
36. Mitsunaga, S., Tashiro, T., and Yamaguchi, J. (1994). Identification and characterization of gibberellin-insensitive mutants selected from among dwarf mutants of rice. Theor. Appl. Genet. 87, 705-712.
37. Mori, M., Nomura, T., Ooka, H., Ishizaka, M., Yokota, T., Sugimoto, K., Okabe, K., Kajiwara, H., Satoh, K., Yamamoto, K., Hirochika, H., and Kikuchi, S. (2002). Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol. 130, 1152-1161.
38. Nam, K.H., and Li, J. (2002). BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203-212.
39. Nelson, D.R., Koymans, L., Kamataki, T., Stegeman, J.J., Feyereisen, R., Waxman, D.U., Waterman, M.R., Gotoh, O., Coon, M.J., Estabrook, R.W., Gunsalus, I.C., and Nebert, D.W. (1996). P450 superfamily: Update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics 6, 1-42.
40. Peng, J., et al. (1999). 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400, 256-261.
41. 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. (2002). Green revolution: A mutant gibberellin-synthesis gene in rice. Nature 416, 701-702.
42. Shimada, Y., Fujioka, S., Miyauchi, N., Kushiro, M., Takatsuto, S., Nomura, T., Yokota, T., Kamiya, Y., Bishop, G.J., and Yoshida, S. (2001). Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol. 126, 770-779.
43. Spielmeyer, W., Ellis, M.H., and Chandler, P.M. (2002). Semidwarf (sd-1), "green revolution" rice, contains a defective gibberellin 20-oxidase gene. Proc. Natl. Acad. Sci. USA 99, 9043-9048.
44. Symons, G.M., and Reid, J.B. (2004). Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol. 135, 2196-2206.
45. Szekeres, M., Nemeth, K., Koncz-Kalman, Z., Mathur, J., Kauschmann, A., Altmann, T., Redei, G.P., Nagy, F., Schell, J., and Koncz, C. (1996). Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85, 171-182.
46. Turk, E.M., Fujioka, S., Seto, H., Shimada, Y., Takatsuto, S., Yoshida, S., Denzel, M.A., Torres, Q.I., and Neff, M.M. (2003). CYP72B1 inactivates brassinosteroid hormones: An intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol. 133, 1643-1653.
47. Ueguchi-Tanaka, M., Fujisawa, Y., Kobayashi, M., Ashikari, M., Iwasaki, Y., Kitano, H., and Matsuoka, M. (2000). Rice dwarf mutant d1, which is defective in the α subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc. Natl. Acad. Sci. USA 97, 11638-11643.
48. Wang, Z.Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., Yang, Y., Fujioka, S., Yoshida, S., Asami, T., and Chory, J. (2002). Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505-513.
49. 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 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12, 1591-1606.
50. 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.
51. Yoshimura, A., Ideta, O., and Iwata, N. (1997). Linkage map of phenotype and RFLP markers in rice. Plant Mol. Biol. 35, 49-60.