Genetic evidence for the reduction of brassinosteroid levels by a BAHD acyltransferase-like protein in Arabidopsis

Plant Physiology

Volumn 159, Issue 2, 2012, Pages 696-709

  Roh, Hyungmin ^a   Jeong, Cheol Woong ^a   Fujioka, Shozo ^b   Kim, Youn Kyung ^a   Lee, Sookjin ^a   Ahn, Ji Hoon ^c   Choi, Yang Do ^d   Lee, Jong Seob ^a  

^a Seoul National University   (South Korea)

^b RIKEN   (Japan)

^c Korea University   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84861901342     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.197202     Document Type: Article

References (71)

1. Ahn JH, Kim J, Yoo SJ, Yoo SY, Roh H, Choi JH, Choi MS, Chung KS, Han EJ, Hong SM, et al (2007) Isolation of 151 mutants that have developmental defects from T-DNA tagging. Plant Cell Physiol 48: 169-178
2. Asakawa S, Abe H, Kyokawa Y, Nakamura S, Natsume M (1994) Teasterone 3-myristate: a new type of brassinosteroid derivative in Lilium longiflorum anthers. Biosci Biotechnol Biochem 58: 219-220
3. Asakawa S, Abe H, Nishikawa N, Natsume M, Koshioka M (1996) Purification and identification of new acyl-conjugated teasterones in lily pollen. Biosci Biotechnol Biochem 60: 1416-1420
4. Azpiroz R, Wu Y, LoCascio JC, Feldmann KA (1998) An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10: 219-230
5. Bajguz A (2007) Metabolism of brassinosteroids in plants. Plant Physiol Biochem 45: 95-107
6. Bancoş 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
7. Beekwilder J, Alvarez-Huerta M, Neef E, Verstappen FW, Bouwmeester HJ, Aharoni A (2004) Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiol 135: 1865-1878
8. 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
9. 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 22alpha-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10: 231-243
10. Choe S, Dilkes BP, Gregory BD, Ross AS, Yuan H, Noguchi T, Fujioka S, Takatsuto S, Tanaka A, Yoshida S, et al (1999a) The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiol 119: 897-907
11. Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann KA (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J 26: 573-582
12. Choe S, Noguchi T, Fujioka S, Takatsuto S, Tissier CP, Gregory BD, Ross AS, Tanaka A, Yoshida S, Tax FE, et al (1999b) The Arabidopsis dwf7/ ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11: 207-221
13. Choe S, Tanaka A, Noguchi T, Fujioka S, Takatsuto S, Ross AS, Tax FE, Yoshida S, Feldmann KA (2000) Lesions in the sterol delta reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J 21: 431-443
14. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
15. Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111: 671-678
16. Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49: 427-451
17. D'Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9: 331-340
18. Dudareva N, D'Auria JC, Nam KH, Raguso RA, Pichersky E (1998) Acetyl-CoA:benzylalcohol acetyltransferase-an enzyme involved in floral scent production in Clarkia breweri. Plant J 14: 297-304
19. El-Sharkawy I, Manríquez D, Flores FB, Regad F, Bouzayen M, Latché A, Pech JC (2005) Functional characterization of a melon alcohol acyltransferase gene family involved in the biosynthesis of ester volatiles: identification of the crucial role of a threonine residue for enzyme activity. Plant Mol Biol 59: 345-362
20. Fujioka S, Li J, Choi YH, Seto H, Takatsuto S, Noguchi T, Watanabe T, Kuriyama H, Yokota T, Chory J, et al (1997) The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9: 1951-1962
21. Fujioka S, Takatsuto S, Yoshida S (2002) An early C-22 oxidation branch in the brassinosteroid biosynthetic pathway. Plant Physiol 130: 930-939
22. Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54: 137-164
23. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130: 1319-1334
24. Grove MD, Spencer GF, Rohwedder WK, Mandava N, Worley JF, Warthen JD, Steffens GL, Flippen-Anderson JL, Cook JC (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281: 216-217
25. Hai T, Schneider B, Porzel A, Adam G (1996)Metabolism of 24-epi-castasterone in cell suspension cultures of Lycopersicon esculentum. Phytochemistry 41: 197-201
26. He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307: 1634-1638
27. Iliev EA, Xu W, Polisensky DH, Oh MH, Torisky RS, Clouse SD, Braam J (2002) Transcriptional and posttranscriptional regulation of Arabidopsis TCH4 expression by diverse stimuli: roles of cis regions and brassinosteroids. Plant Physiol 130: 770-783
28. Jung JH, Lee M, Park CM (2010) A transcriptional feedback loop modulating signaling crosstalks between auxin and brassinosteroid in Arabidopsis. Mol Cells 29: 449-456
29. Kim GT, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S, Tsukaya H (2005a) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 41: 710-721
30. Kim H, Park M, Kim SJ, Hwang I (2005b) Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell 17: 888-902
31. 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
32. Kim TW, Hwang JY, Kim YS, Joo SH, Chang SC, Lee JS, Takatsuto S, Kim SK (2005c) Arabidopsis CYP85A2, a cytochrome P450, mediates the Baeyer-Villiger oxidation of castasterone to brassinolide in brassinosteroid biosynthesis. Plant Cell 17: 2397-2412
33. Kolbe A, Schnerider B, Porzel A, Adam G (1996) Metabolism of 24-epi-castasterone and 24-epi-brassinolide in cell suspension cultures of Ornithopus sativus. Phytochermistry 41: 163-167
34. Kolbe A, Schneider B, Porzel A, Schmidt J, Adam G (1995) Acyl-conjugated metabolites of brassinosteroids in cell suspension cultures of Ornithopus sativus. Phytochemistry 38: 633-636
35. Kwon M, Choe S (2005) Brassinosteroid biosynthesis and dwarf mutants. J Plant Biol 48: 1-15
36. Lee S, Lee DW, Lee Y, Mayer U, Stierhof YD, Lee S, Jürgens G, Hwang I (2009) Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 21: 3984-4001
37. 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
38. Luo J, Fuell C, Parr A, Hill L, Bailey P, Elliott K, Fairhurst SA, Martin C, Michael AJ (2009) A novel polyamine acyltransferase responsible for the accumulation of spermidine conjugates in Arabidopsis seed. Plant Cell 21: 318-333
39. Marsolais F, Boyd J, Paredes Y, Schinas AM, Garcia M, Elzein S, Varin L (2007) Molecular and biochemical characterization of two brassinosteroid sulfotransferases from Arabidopsis, AtST4a (At2g14920) and AtST1 (At2g03760). Planta 225: 1233-1244
40. Mathur J, Molnár G, Fujioka S, Takatsuto S, Sakurai A, Yokota T, Adam G, Voigt B, Nagy F, Maas C, et al (1998) Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. Plant J 14: 593-602
41. Müssig C, Fischer S, Altmann T (2002) Brassinosteroid-regulated gene expression. Plant Physiol 129: 1241-1251
42. Nakamura M, Satoh T, Tanaka S, 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
43. Nam KH, Dudareva N, Pichersky E (1999) Characterization of benzylalcohol acetyltransferases in scented and non-scented Clarkia species. Plant Cell Physiol 40: 916-923
44. Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Yoshida S, et al (1999) BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc Natl Acad Sci USA 96: 15316-15323
45. Nemhauser JL, Maloof JN, Chory J (2003) Building integrated models of plant growth and development. Plant Physiol 132: 436-439
46. Nishikawa N, Abe H, Natsume M, Shida A, Toyama S (1995) Epimerization and conjugation of 14C-labeled in cucumber seedlings. J Plant Physiol 147: 294-300
47. Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, Saeki M, Shibata D, Saito K, Ohta H (2007) ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res (Database issue) 35: D863-D869
48. Poppenberger B, Fujioka S, Soeno K, George GL, Vaistij FE, Hiranuma S, Seto H, Takatsuto S, Adam G, Yoshida S, et al (2005) The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids. Proc Natl Acad Sci USA 102: 15253-15258
49. Rouleau M, Marsolais F, Richard M, Nicolle L, Voigt B, Adam G, Varin L (1999) Inactivation of brassinosteroid biological activity by a salicylateinducible steroid sulfotransferase from Brassica napus. J Biol Chem 274: 20925-20930
50. Shalit M, Guterman I, Volpin H, Bar E, Tamari T, Menda N, Adam Z, Zamir D, Vainstein A, Weiss D, et al (2003) Volatile ester formation in roses. Identification of an acetyl-coenzyme A. Geraniol/Citronellol acetyltransferase in developing rose petals. Plant Physiol 131: 1868-1876
51. 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
52. 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
53. Soeno K, Kyokawa Y, Natsume M, Abe H (2000) Teasterone-3-O-beta-Dglucopyranoside, a new conjugated brassinosteroid metabolite from lily cell suspension cultures and its identification in lily anthers. Biosci Biotechnol Biochem 64: 702-709
54. Sohn EJ, Kim ES, Zhao M, Kim SJ, Kim H, Kim YW, Lee YJ, Hillmer S, Sohn U, Jiang L, et al (2003) Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins. Plant Cell 15: 1057-1070
55. Stündl U, Schneider B (2001) 3Beta-brassinosteroid dehydrogenase activity in Arabidopsis and tomato. Phytochemistry 58: 989-994
56. Suzuki H, Kim SK, Takahashi N, Yokota T (1993) Metabolism of castasterone and brassinolide in mung bean explant. Phytochemistry 33: 1361-1367
57. 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
58. 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
59. Thornton LE, Rupasinghe SG, Peng H, Schuler MA, Neff MM (2010) Arabidopsis CYP72C1 is an atypical cytochrome P450 that inactivates brassinosteroids. Plant Mol Biol 74: 167-181
60. 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
61. Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Wang H, Torres QI, Ward JM, Murthy G, et al (2005) BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J 42: 23-34
62. Voigt B, Porzel A, Naumann H, Hörhold-Schubert C, Adam G (1993) Hydroxylation of the native brassinosteroids 24-epicastasterone and 24-epibrassinolide by the fungus Cunninghamella echinulata. Steroids 58: 320-323
63. Walker K, Long R, Croteau R (2002) The final acylation step in taxol biosynthesis: cloning of the taxoid C13-side-chain N-benzoyltransferase from Taxus. Proc Natl Acad Sci USA 99: 9166-9171
64. Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410: 380-383
65. Watanabe T, Yokota T, Shibata K, Nomura T, Seto H, Takatsuto S (2000) Cryptolide, a new brassinolide catabolite with a 23-oxo group from Japanese cedar pollen anther and its synthesis. J Chem Res 2000: 18-19
66. Weigel D, Ahn JH, Blázquez MA, Borevitz JO, Christensen SK, Fankhauser C, Ferrándiz C, Kardailsky I, Malancharuvil EJ, Neff MM, et al (2000) Activation tagging in Arabidopsis. Plant Physiol 122: 1003-1013
67. Yamamoto R, Fujioka S, Iwamoto K, Demura T, Takatsuto S, Yoshida S, Fukuda H (2007) Co-regulation of brassinosteroid biosynthesis-related genes during xylem cell differentiation. Plant Cell Physiol 48: 74-83
68. Yang Q, Reinhard K, Schiltz E, Matern U (1997) Characterization and heterologous expression of hydroxycinnamoyl/benzoyl-CoA:anthranilate N-hydroxycinnamoyl/benzoyltransferase from elicited cell cultures of carnation, Dianthus caryophyllus L. Plant Mol Biol 35: 777-789
69. Yokota T, Matsuoka T, Koarai T, Nakayama M (1996) 2-Deoxybrassinolide, a brassinosteroid from Pisum sativum seed. Phytochemistry 42: 509-511
70. Yu XH, Gou JY, Liu CJ (2009) BAHD superfamily of acyl-CoA dependent acyltransferases in Populus and Arabidopsis: bioinformatics and gene expression. Plant Mol Biol 70: 421-442
71. Yuan T, Fujioka S, Takatsuto S, Matsumoto S, Gou X, He K, Russell SD, Li J (2007) BEN1, a gene encoding a dihydroflavonol 4-reductase (DFR)-like protein, regulates the levels of brassinosteroids in Arabidopsis thaliana. Plant J 51: 220-233