Abstract
Cytochrome P450s (P450s) are essential for both plant steroid hormone biosynthesis and inactivation. Synthesis of plant steroid hormones, brassinosteroids (BRs), requires P450s of the CYP85 clan. This includes members of the CYP85, CYP90 and CYP724B families of P450s. These enzymes are associated with the hydroxylation/oxidation of the C-2, C-3, C-6, C-22 and C-23 positions with their function being determined via genetic and biochemical approaches. P450s involved in BR metabolism belong to the CYP72C and CYP734A families in the CYP72 clan of P450s. The CYP734A family is associated with C-26 hydroxylation of BRs. The transcriptional regulation of these genes via feedback regulation provides a mechanism for the maintenance of optimum BR levels. Phylogenetic analysis of these P450s highlights that the biosynthesis and metabolism genes have evolved independently. Similar analysis suggests that the Baeyer–Villiger reaction catalysed by the CYP85 family of P450s may have evolved independently in several dicotyledonous species.
Similar content being viewed by others
References
Altmann T (1999) Molecular physiology of brassinosteroids revealed by the analysis of mutants. Planta 208:1–11
Asami T, Mizutani M, Fujioka S, Goda H, Min YK, Shimada Y, Nakano T, Takatsuto S, Matsuyama T, Nagata N, Sakata K, Yoshida S (2001) Selective interaction of triazole derivatives with DWF4, a P450 monooxygenase of the brassinosteroid pathway, correlates with brassinosteroid deficiency in planta. J Biol Chem 276:25687–25691
Asami T, Mizutani M, Shimada Y, Goda H, Kitahata N, Sekimata K, Han S-Y., Fujioka S, Takatsuto S, Sakata K, Yoshida S (2003) Triadimefon, a fungicidal triazole-type P450 inhibitor, induces brassinosteroid deficiency-like phenotypes in plants and binds to DWF4 protein in the brassinosteroid biosynthesis pathway. Biochem J 369:71–76
Azpiroz R, Wu Y, LoCascio JC, Feldmann KA (1998) An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10:219–230
Bancos S, Nomura T, Sato T, Molnár G, Bishop GJ, Koncz C, Yokota T, Nagy F, Szekeres M (2002) Regulation of transcript levels of the Arabidopsis cytochrome P450 genes involved in brassinosteroid biosynthesis. Plant Physiol 130:504–513
Bancos S, Szatmari AM, Castle J, Kozma-Bognar L, Shibata K, Yokota T, Bishop GJ, Nagy F, Szekeres M (2006) Diurnal regulation of the brassinosteroid-biosynthetic CPD gene in Arabidopsis. Plant Physiol 141:299–309
Bishop GJ, Harrison K, Jones JDG (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
Bishop GJ, Nomura T, Yokota T, Harrison K, Noguchi T, Fujioka S, Takatsuto S, Jones JDG, Kamiya Y (1999) The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis. Proc Natl Acad Sci USA 96:1761–1766
Bishop GJ, Yokota T (2001) Plants steroid hormones, brassinosteroids: Current highlights of molecular aspects on their synthesis/metabolism, transport, perception and response. Plant Cell Physiol 42:114–120
Cano-Delgado A, Yin YH, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351
Castle J, Szekeres M, Jenkins G, Bishop GJ (2005) Unique and overlapping expression patterns of Arabidopsis CYP85 genes involved in brassinosteroid C-6 oxidation. Plant Mol Biol 57:129–140
Choe S, Dilkes BP, Fujioka S, Takatsuto S, Sakurai A, Feldmann KA (1998) The DWF4 gene of Arabidopsis encodes a cytochrome-P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10:231–243
Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann K (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J 26:573–582
Chory J, Nagpal P, Peto C (1991) Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3:445–459
Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451
Estabrook RW (2005) Steroid hydroxylations: A paradigm for cytochrome P450 catalyzed mammalian monooxygenation reactions. Biochem Biophys Res Commun 338:290–298
Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54:137–164
Fujioka S, Takatsuto S, Yoshida S (2002) An early C-22 oxidation branch in the brassinosteroid biosynthetic pathway. Plant Physiol 130:930–939
Fujita S, Ohnishi T, Watanabe B, Yokota T, Takatsuto S, Fujioka S, Yoshida S, Sakata K, Mizutani M (2006) Arabidopsis CYP90B1 catalyses the early C-22 hydroxylation of C27, C28 and C29 sterols. Plant J 45:765–774
Gilbert LI, Warren JT (2005) A molecular genetic approach to the biosynthesis of the insect steroid molting hormone. Vitam Horm 73:31–57
Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334
Hai T, Schneider B, Adam G (1995) Metabolic conversion of 24-epi-brassinolide into pentahydroxylated brassinosteroid glucosides in tomato cell cultures. Phytochemistry 40:443–448
He J-X, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang Z-Y (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307:1634–1638
Hong Z, Ueguchi-Tanaka M, Shimizu-Sato S, Inukai Y, Fujioka S, Shimada Y, Takatsuto S, Agetsuma M, Yoshida S, Watanabe Y, Uozu S, Kitano H, Ashikari M, Matsuoka M (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
Hong Z, Ueguchi-Tanaka M, Umemura K, Uozu S, Fujioka S, Takatsuto S, Yoshida S, Ashikari M, Kitano H, 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
Kang J-G, Yun J, Kim D-H, Chung K-S, Fujioka S, Kim J-I, Dae H-W, Yoshida S, Takatsuto S, Song P-S, Park C-M (2001) Light and brassinosteroid signals are integrated via a dark-induced small G protein in etiolated seedling growth. Cell 105:625–636
Kauschmann A, Jessop A, Koncz C, Szekeres M, Willmitzer L, Altmann T (1996) Genetic eividence for an essential role of Brassinosteroids in plant development. Plant J 9:701–713
Kim G-T, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S, Tsukaya H (2005c) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 41:710–721
Kim G-T, Tsukaya H, 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
Kim HB, Kwon M, Ryu H, Fujioka S, Takatsuto S, Yoshida S, An CS, Lee I, Hwang I, Choe S (2006) The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiol 140:548–557
Kim HB, Schaller H, Goh C-H., Kwon M, Choe S, An CS, Durst F, Feldmann KA, Feyereisen R (2005a) Arabidopsis cyp51 mutant shows postembryonic seedling lethality associated with lack of membrane integrity. Plant Physiol 138:2033–2047
Kim T-W, Hwang J-Y, Kim Y-S, Joo S-H, Chang SC, Lee JS, Takatsuto S, Kim S-K (2005b) Arabidopsis CYP85A2, a cytochrome P450, mediates the Baeyer–Villiger oxidation of castasterone to brassinolide in brassinosteroid biosynthesis. Plant Cell 17:2397–2412
Koka CV, Cerny RE, Gardner RG, Noguchi T, Fujioka S, Takatsuto S, Yoshida S, Clouse S (2000) A putative role for the tomato genes DUMPY and CURL3 in brassinosteroid biosynthesis and response. Plant Physiol 122:85–98
Kwon M, Fujioka S, Jeon JH, Kim HB, Takatsuto S, Yoshida S, An CS, Choe S (2005) A double mutant for the CYP85A1 and CYP85A2 genes of Arabidopsis exhibits a brassinosteroid dwarf phenotype. J Plant Biol 48:237–244
Li J, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272:398–401
Mathur J, Molnár G, Fujioka S, Takatsuto S, Sakurai A, Yokota T, Adam G, Voigt B, Nagy F, Maas C, Schell J, Koncz C, Szekeres M (1998) Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. Plant J 14:593–602
Montoya T, Nomura T, Yokota T, Farrar K, Harrison K, Jones JGD, Kaneta T, Kamiya Y, Szekeres M, Bishop GJ (2005) Patterns of Dwarf expression and brassinosteroid accumulation in tomato reveal the importance of brassinosteroid synthesis during fruit development. Plant J 42:262–269
Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ (2002) 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 14:3163–3176
Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, Sugimoto K, Okabe K, Kajiwara H, Satoh K, Yamamoto K, Hirochika H, Kikuchi S (2002) Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol 130:1152–1161
Nakamura M, Satoh T, Tanaka SI, Mochizuki N, Yokota T, Nagatani A (2005) Activation of the cytochrome P450 gene, CYP72C1, reduces the levels of active brassinosteroids in vivo. J Exp Bot 56:833–840
Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Yoshida S, Chory J (1999) BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc Natl Acad Sci USA 96:15316–15323
Nelson DR, Schuler MA, Paquette SM, Werck-Reichhart D, Bak S (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol 135:756–772
Noguchi T, Fujioka S, Choe S, Takatsuto S, Yoshida S, Yuan H, Feldmann KA, Tax FE (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol 121:743–752
Nomura T, Bishop GJ, Kaneta T, Reid JB, Chory J, Yokota T (2003) The LKA gene is a BRASSINOSTEROID INSENSITIVE 1 homolog of pea. Plant J 36:291–300
Nomura T, Kushiro T, Yokota T, Kamiya Y, Bishop GJ, Yamaguchi S (2005) The last reaction producing brassinolide is catalyzed by cytochrome P-450s, CYP85A3 in tomato and CYP85A2 in Arabidopsis. J Biol Chem 280:17873–17879
Nomura T, Nakayama M, Reid JB, Takeuchi Y, Yokota T (1997) Blockage of brassinosteroid biosynthesis and sensitivity causes dwarfism in garden pea. Plant Physiol 113:31–37
O’Brien M, Chantha S-C, Rahier A, Matton DP (2005) Lipid signaling in plants. Cloning and expression analysis of the obtusifoliol-demethylase from Solanum chacoense Bitt., a pollination- and fertilization-induced gene with both obtusifoliol and lanosterol demethylase activity. Plant Physiol 139:734–749
Payne AH, Hales DB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25:947–970
Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24:105–109
Schuler MA, Werck-Reichhart D (2003) Functional genomics of P450s. Annu Rev Plant Biol 54:629–667
Shimada Y, Fujioka S, Miyauchi N, Kushiro M, Takatsuto S, Nomura T, Yokota T, Kamiya Y, Bishop GJ, Yoshida S (2001) Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol 126:770–779
Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol 131:287–297
Symons GM, Reid JB (2003) Hormone levels and response during de-etiolation in pea. Planta 216:422–431
Symons GM, Reid JB (2004) Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol 135:2196–2206
Symons GM, Schultz L, Kerckhoffs LH, Davies NW, Gregory D, Reid JB (2002) Uncoupling brassinosteroid levels and de-etiolation in pea. Physiol Plant 115:311–319
Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening., Plant Physiol 140:150–158
Szekeres M, Bishop GJ (2006) Integration of brassinosteroid biosynthesis and signalling. Ann Plant Rev 24:67–92 (Hedden P, Thomas SG (eds))
Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei G, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171–182
Takahashi N, Nakazawa M, Shibata K, Yokota T, Ishikawa A, Suzuki K, Kawashima M, Ichikawa T, Shimada H, Matsui M (2005) shk1-D, a dwarf Arabidopsis mutant caused by activation of the CYP72C1 gene, has altered brassinosteroid levels. Plant J 42:13–22
Tanabe S, Ashikari M, Fujioka S, Takatsuto S, Yoshida S, Yano M, Yoshimura A, Kitano H, Matsuoka M, Fujisawa Y, Kato H, Iwasaki Y (2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17:776–790
Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138:1117–1125
Tsuge T, Tsukaya H, Uchimiya H (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L) Heynh. Development 122:1589–1600
Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Denzel MA, Torres QI, Neff MM (2003) CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol 133:1643–1653
Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Wang H, Torres QI, Ward JM, Murthy G, Zhang J, Walker JC, Neff MM (2005) BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J 42:23–34
Yang M-T, Chen S-L, Lin C-Y, Chen Y-M (2005) Chilling stress suppresses chloroplast development and nuclear gene expression in leaves of mung bean seedlings. Planta 221:374–385
Yokota T, Sato T, Takeuchi Y, Nomura T, Uno K, Watanabe T, Takatsuto S (2001) Roots and shoots of tomato produce 6-deoxo-28-norcastasterone, 6-deoxo-28-nortyphasterol and 6-deoxo-28-norcastasterone, possible precursors of 28-norcastasterone. Phytochemistry 58:233–238
Acknowledgements
GB thanks the BBSRC for supporting research in his lab. TN acknowledges support of Special Postdoctoral Researchers Program from RIKEN and a grant-in-aid for scientific research from the JSPS (grant no. 17780095).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nomura, T., Bishop, G.J. Cytochrome P450s in plant steroid hormone synthesis and metabolism. Phytochem Rev 5, 421–432 (2006). https://doi.org/10.1007/s11101-006-9024-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-006-9024-2