Genome-wide identification of glucosinolate synthesis genes in Brassica rapa

FEBS Journal

Volumn 276, Issue 13, 2009, Pages 3559-3574

  Zang, Yun Xiang ^a,b   Kim, Hyun Uk ^a   Kim, Jin A ^a   Lim, Myung Ho ^a   Jin, Mina ^a   Lee, Sang Choon ^a   Kwon, Soo Jin ^a   Lee, Soo In ^a   Hong, Joon Ki ^a   Park, Tae Ho ^a   Mun, Jeong Hwan ^a   Seol, Young Joo ^a   Hong, Seung Beom ^c   Park, Beom Seok ^a  

^a National Institute of Animal Science   (South Korea)

^b ZHEJIANG A F UNIVERSITY   (China)

^c San Jacinto College Department of Philosophy San Jacinto College North Campus   (United States)

Author keywords

Bioinformatics; Biosynthesis pathway; Brassica rapa; Gene identification; Glucosinolate

Indexed keywords

ALDOXIME; GLUCOSINOLATE; METHIONINE; PHENYLALANINE; TRYPTOPHAN;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CHROMOSOME INVERSION; EXON; GENE DELETION; GENE EXPRESSION; GENE IDENTIFICATION; GENE INSERTION; GENE MUTATION; GENE NUMBER; GENETIC VARIABILITY; INTRON; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RETROPOSON; SEQUENCE HOMOLOGY; TURNIP;

ANIMALS; ARABIDOPSIS; BRASSICA RAPA; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; EVOLUTION; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENOME, PLANT; GLUCOSINOLATES; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; SULFOTRANSFERASES;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA RAPA;

EID: 67650445669     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07076.x     Document Type: Article

References (82)

1. Brader G, Mikkelsen MD, Halkier BA Palva ET (2006) Altering glucosinolate profiles modulates disease resistance in plants. Plant J 46, 758 767. (Pubitemid 43780623)
2. Kim JH, Lee BW, Schroeder F Jander G (2008) Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J 54, 1015 1026. (Pubitemid 351794022)
3. Zhang Y, Kensler TW, Cho C, Posner GH Talalay P (1994) Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proc Natl Acad Sci USA 91, 3147 3150. (Pubitemid 24130192)
4. Fimognari C Hrelia P (2007) Sulforaphane as a promising molecule for fighting cancer. Mutat Res 635, 90 104. (Pubitemid 46756397)
5. Myzak MC Dashwood RH (2006) Chemoprotection by sulforaphane: keep one eye beyond keap. Cancer Lett 233, 208 218. (Pubitemid 43327375)
6. Myzak MC, Dashwood WM, Orner GA, Ho E Dashwood RH (2006) Sulforaphane inhibits histone deacetylase in vivo and suppresses tumorigenesis in Apcmin mice. FASEB J 20, 506 508. (Pubitemid 46671231)
7. Myzak MC, Karplus PA, Chung F Dashwood RH (2004) A novel mechanism of chemoprevention by sulforaphane: inhibition of histone deacetylase. Cancer Res 64, 5767 5774. (Pubitemid 39095576)
8. Parnaud G, Li P, Cassar G, Rouimi P, Tulliez J, Combaret L Gamet-Payrastre L (2004) Mechanism of sulforaphane-induced cell cycle arrest and apoptosis in human colon cancer cells. Nutr Cancer 48, 198 206. (Pubitemid 39045782)
9. Pledgie-Tracy A, Sobolewski MD Davidson NE (2007) Sulforaphane induces cell type-specific apoptosis in human breast cancer cell lines. Mol Cancer Ther 6, 1013 1021. (Pubitemid 46554571)
10. Solowiej E, Kaspizycka-Guttman T, Fiedor P Rowinski W (2003) Chemoprevention of cancerogenesis - the role of sulforaphane. Acta Pol Pharm 60, 97 100. (Pubitemid 36603840)
11. Takahashi N, Dashwood RH, Bjeldanes LF, Williams DE Bailey GS (1995) Mechanisms of indole-3-carbinol (I3C) anticarcinogenesis: inhibition of aflatoxin B1-DNA adduction and mutagenesis by I3C acid condensation products. Food Chem Toxicol 33, 851 857.
12. Bradlow HL, Sepkovic DW, Telang NT Osborne MP (1999) Multifunctional aspects of the action of indole-3-carbinol as an antitumor agent. Ann NY Acad Sci 889, 204 213. (Pubitemid 30040438)
13. Chinni SR, Li Y, Upadhyay S, Koppolu PK Sarkar FH (2001) Indole-3-carbinol (I3C) induced cell growth inhibition, G1 cell cycle arrest and apoptosis in prostate cancer cells. Oncogene 20, 2927 2936. (Pubitemid 33027760)
14. Nho CW Jeffery E (2001) The synergistic upregulation of phase II detoxification enzymes by glucosinolate breakdown products in cruciferous vegetables. Toxicol Appl Pharmacol 174, 146 152. (Pubitemid 32675517)
15. Meng Q, Qi M, Chen DZ, Goldberg ID, Rosen EM, Auborn K Fan S (2000) Suppression of breast cancer invasion and migration by indole-3-carbinol: associated with up-regulation of BRCA1 and E-cadherin/catenin complexes. J Mol Med 78, 155 165. (Pubitemid 30337497)
16. Chung FL, Conaway CC, Rao CV Reddy VS (2000) Chemoprevention of colonic aberrant crypt foci in Fischer rats by sulforaphane and phenethyl isothiocyanate. Carcinogenesis 21, 2287 2291. (Pubitemid 32049237)
17. Huang C, Ma WY, Li J, Hecht SS Dong Z (1998) Essential role of p53 in phenethyl isothiocyanate-induced apoptosis. Cancer Res 58, 4102 4106. (Pubitemid 28440564)
18. Yao S, Zhang Y Li J (2006) c-jun/AP-1 activation does not affect the antiproliferative activity of phenethyl isothiocyanate, a cruciferous vegetable-derived cancer chemopreventive agent. Mol Carcinog 45, 605 612. (Pubitemid 44205100)
19. Canistro D, Croce CD, Iori R, Barillari J, Bronzetti G, Poi G, Cini M, Caltavuturo L, Perocco P Paolini M (2004) Genetic and metabolic effects of gluconasturtiin, a glucosinolate derived from cruciferae. Mutat Res 545, 23 35. (Pubitemid 38036988)
20. Hirose M, Yamaguchi T, Kimoto N, Ogawa K, Futakuchi M, Sano M Shirai T (1998) Strong promoting activity of phenylethyl isothiocyanate and benzyl isothiocyanate on urinary bladder carcinogenesis in F344 male rats. Int J Cancer 77, 773 777. (Pubitemid 28341396)
21. Kassie F Knasmüller S (2000) Genotoxic effects of allyl isothiocyanate (AITC) and phenethyl isothiocyanate (PEITC). Chem Biol Interact 127, 163 180. (Pubitemid 30599481)
22. March TH, Jeffery EH Wallig MA (1998) The cruciferous nitrile, crambene, induces rat hepatic and pancreatic glutathione S-transferases. Toxicol Sci 42, 82 90. (Pubitemid 28211136)
23. Halkier BA Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57, 303 333. (Pubitemid 44061027)
24. Kroymann J, Textor S, Tokuhisa JG, Falk KL, Bartram S, Gershenzon J Mitchell-Olds T (2001) A gene controlling variation in Arabidopsis glucosinolate composition is part of the methionine chain elongation pathway. Plant Physiol 127, 1077 1088. (Pubitemid 33112167)
25. Textor S, de Kraker JW, Hause B, Gershenzon J Tokuhisa JG (2007) MAM3 catalyzes the formation of all aliphatic glucosinolate chain lengths in Arabidopsis. Plant Physiol 144, 60 71. (Pubitemid 46941605)
26. Hansen BG, Kerwin RE, Ober JA, Lambrix VM, Mitchell-Olds T, Gershenzon J, Halkier BA Kliebenstein DJ (2008) A novel 2-oxoacid-dependent dioxygenase involved in the formation of the goiterogenic 2-hydroxybut-3-enyl glucosinolate and generalist insect resistance in Arabidopsis. Plant Physiol 148, 2096 2108. (Pubitemid 352847462)
27. Hansen BG, Kliebenstein DJ Halkier BA (2007) Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J 50, 902 910. (Pubitemid 46855038)
28. Li J, Hansen BG, Ober JA, Kliebenstein DJ Halkier BA (2008) Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol 148, 1721 1733. (Pubitemid 352847524)
29. Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J Mitchell-Olds T (2001) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13, 681 693. (Pubitemid 32265384)
30. Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, Gershenzon J Mitchell-Olds T (2001) Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol 126, 811 825. (Pubitemid 32566630)
31. Kliebenstein DJ, D'Auria JC, Behere AS, Kim JH, Gunderson KL, Breen JN, Lee G, Gershenzon J, Last RL Jander G (2007) Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J 51, 1062 1076. (Pubitemid 47373573)
32. Keck AS Finley JW (2004) Cruciferous vegetables: cancer protective mechanisms of glucosinolate hydrolysis products and selenium. Integr Cancer Ther 3, 5 12. (Pubitemid 38233800)
33. Wu L, Ashraf MHN, Facci M, Wang R, Paterson PG, Ferrie A Juurlink BH (2004) Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proc Natl Acad Sci USA 101, 7094 7099. (Pubitemid 38596448)
34. Tang L, Zirpoli GR, Guru K, Moysich KB, Zhang Y, Ambrosone CB McCann SE (2008) Consumption of raw cruciferous vegetables is inversely associated with bladder cancer risk. Cancer Epidemiol Biomarkers Prev 17, 938 944.
35. Grubb CD Abel S (2006) Glucosinolate metabolism and its control. Trends Plant Sci 11, 89 100. (Pubitemid 43238420)
36. Celenza JL, Quiel JA, Smolen GA, Merrikh H, Silvestro AR, Normanly J Bender J (2005) The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol 137, 253 262. (Pubitemid 43034307)
37. Levy M, Wang Q. Kaspi R, Parrella MP Abel S (2005) Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J 43, 79 96. (Pubitemid 40962737)
38. Skirycz A, Reichelt M, Burow M, Birkemeyer C, Rolcik J, Kopka J, Zanor MI, Gershenzon J, Strnad M, Szopa J et al. (2006) DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J 47, 10 24. (Pubitemid 43883010)
39. Gigolashvili T, Berger B, Mock HP, Müller C, Weisshaar B Flügge UI (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50, 886 901. (Pubitemid 46855037)
40. Gigolashvili T, Engqvist M, Yatusevich R, Müller C Flügge UI (2008) HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol 177, 627 642.
41. Gigolashvili T, Yatusevich R, Berger B, Müller C Flügge UI (2007) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 51, 247 261. (Pubitemid 47030119)
42. Sønderby IE, Hansen BG, Bjarnholt N, Ticconi C, Halkier BA Kliebenstein DJ (2007) A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2, e1322.
43. Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A, Araki R, Sakurai N, Suzuki H, Aoki K et al. (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci USA 104, 6478 6483. (Pubitemid 47186119)
44. Li G Quiros CF (2003) In planta side-chain glucosinolate modification in Arabidopsis by introduction of dioxygenase Brassica homolog BoGSL-ALK. Theor Appl Genet 106, 1116 1121. (Pubitemid 36599822)
45. Gao M, Li G, Yang B, McCombie WR Quiros CF (2004) Comparative analysis of a Brassica BAC clone containing several major aliphatic glucosinolate genes with its corresponding Arabidopsis sequence. Genome 47, 666 679. (Pubitemid 39342534)
46. Gao M, Li G, Potter D, McCombie WR Quiros CF (2006) Comparative analysis of methylthioalkylmalate synthase (MAM) gene family and flanking DNA sequences in Brassica oleracea and Arabidopsis thaliana. Plant Cell Rep 25, 592 598. (Pubitemid 43787388)
47. Kang JY, Ibrahim KE, Juvik JA, Kim DH Kang WJ (2006) Genetic and environmental variation of glucosinolate content in Chinese cabbage. HortSci 41, 1382 1385. (Pubitemid 44483773)
48. Engelen-Eigles G, Holden G, Cohen JD Gardner G (2006) The effect of temperature, photoperiod, and light quality on gluconasturtiin concentration in watercress (Nasturtium officinale R. Br.). J Agric Food Chem 54, 328 334. (Pubitemid 43301247)
49. 3. Planta 227, 427 437.
50. Zang YX, Lim MH, Park BS, Hong SB Kim DH (2008) Metabolic engineering of the indole glucosinolates in Chinese cabbage plants expressing Arabidopsis CYP79B2, CYP79B3, and CYP83B1. Mol Cells 25, 231 241. (Pubitemid 351819000)
51. Zang YX, Kim JH, Park YD, Kim DH Hong SB (2008) Metabolic engineering of the aliphatic glucosinolates in Chinese cabbage plants expressing Arabidopsis MAM1, CYP79F1, and CYP83A1. BMB rep 41, 472 478.
52. Mun JH, Kwon SJ, Yang TJ, Kim HS, Choi BS, Baek S, Kim JS, Jin M, Kim JA, Lim MH et al. (2008) The first generation of a BAC-based physical map of Brassica rapa. BMC Genomics 9, 280.
53. Kim JS, Chung TY, King GJ, Jin M, Yang TJ, Jin YM, Kim HI Park BS (2006) A sequence-tagged linkage map of Brassica rapa. Genetics 174, 29 39. (Pubitemid 44427651)
54. Lee JT (2003) Complicity of gene and pseudogene. Nature 423, 26 28. (Pubitemid 36569571)
55. Force A, Lynch M, Pickett FB, Amores A, Yan YL Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531 1545. (Pubitemid 29177561)
56. Blanc G Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679 1691. (Pubitemid 38908768)
57. Piotrowski M, Schemenewitz A, Lopukhina A, Müller A, Janowitz T, Weiler EW Oecking C (2004) Desulfoglucosinolate sulfotransferases from Arabidopsisthaliana catalyzing the final step in biosynthesis of the glucosinolate core structure. J Biol Chem 279, 50717 50725. (Pubitemid 40017809)
58. Schuster J, Knill T, Reichelt H, Gershenzon J Binder S (2006) Branched-chain aminotransferase4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. Plant Cell 18, 1 16.
59. Knill T, Schuster J, Reichelt M, Gershenzon J Binder S (2008) Arabidopsis thaliana branched-chain aminotransferase 3 functions in both amino acid and glucosinolate biosynthesis. Plant Physiol 146, 1028 1039. (Pubitemid 352844120)
60. Li G Quiros CF (2002) Genetic analysis, expression and molecular characterization of BoGSL-ELONG, a major gene involved in the aliphatic glucosinolate pathway of Brassica species. Genetics 162, 1937 1943. (Pubitemid 36114675)
61. De Kraker JW, Luck K, Textor S, Tokuhisa J Gershenzon J (2007) Two Arabidopsis genes (IPMS1 and IPMS2) encode isopropylmalate synthase, the branchpoint step in the biosynthesis of leucine. Plant Physiol 143, 970 986. (Pubitemid 46940956)
62. Lou P, Zhao J, He H, Hanhart C, Pino Del Carpio D, Verkerk R, Custers J, Koornneef M Bonnema G (2008) Quantitative trait loci for glucosinolate accumulation in Brassica rapa leaves. New Phytol 179, 1017 1032.
63. Rangkadilok N, Nicolas ME, Bennett RN, Premier RR, Eagling DR Taylor PWJ (2002) Determination of sinigrin and glucoraphanin in Brassica species using a simple extraction method combined with ion-pair HPLC analysis. Sci Hortic 96, 27 41. (Pubitemid 35399907)
64. Wentzell AM, Rowe HC, Hansen BG, Ticconi C, Halkier BA Kliebenstein DJ (2007) Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways. PLoS Genet 3, 1687 1701. (Pubitemid 47510261)
65. Bowers JE, Chapman BA, Rong JK Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433 438. (Pubitemid 36411396)
66. Lysak MA, Koch M, Pecinka A Schubert I (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res 15, 516 525. (Pubitemid 41065010)
67. Yang YW, Lai KN, Tai PY Li WH (1999) Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J Mol Evol 48, 597 604.
68. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796 815.
69. Hong CP, Kwon SJ, Kim JS, Yang TJ, Park BS Lim YP (2008) Progress in understanding and sequencing the genome of Brassica rapa. Int J Plant Genomics 2008, doi :.
70. Town CD, Cheung F, Maiti R, Crabtree J, Haas BJ, Wortman JR, Hine EE, Althoff R, Arbogast TS, Tallon LJ et al. (2006) Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18, 1348 1359. (Pubitemid 43956101)
71. Xiao H, Jiang N, Schaffner E, Stockinger EJ van der Knaap E (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319, 1527 1530.
72. Park J, Koo DH, Hong CP, Lee SJ, Jeon JW, Lee SH, Yun PY, Park BS, Kim HR, Bang JW et al. (2005) Physical mapping and microsynteny of Brassica rapa ssp. pekinensis genome corresponding to a 222 kbp gene-rich region of Arabidopsis chromosome 4 and partially duplicated on chromosome 5. Mol Genet Genomics 274, 579 588. (Pubitemid 41748287)
73. Kim JA, Yang TJ, Kim JS, Park JY, Kwon SJ, Lim MH, Jin M, Lee SC, Lee SI, Choi BS et al. (2007) Isolation of circadian-associated genes in Brassica rapa by comparative genomics with Arabidopsis thaliana. Mol Cells 23, 145 153. (Pubitemid 46711675)
74. Yang TJ, Yu Y, Frisch DA, Lee S, Kim HR, Kwon SJ, Park BS Wing RA (2004) Construction of various copy number plasmid vectors and their utility for genome sequencing. Genomics Inform 2, 174 179.
75. Yang TJ, Kim JS, Lim KB, Kwon SJ, Kim JA, Jin M, Park JY, Lim MH, Kim HI, Kim SH et al. (2005) The Korea Brassica Genome Project: a glimpse of the Brassica genome based on comparative genome analysiswith Arabidopsis. Comp Funct Genomics 6, 138 146. (Pubitemid 40691803)
76. Gordon D, Abajian C Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8, 195 202. (Pubitemid 28177231)
77. Murray MG Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8, 4321 4325.
78. Cho YG, Eun MY, McCouch SR Chae YA (1994) The semidwarf gene, sd-1, of rice (Oryza sativa L.) II. Molecular mapping and marker-assisted selection. Theor Appl Genet 89, 54 59. (Pubitemid 2155323)
79. Zhao Y, Hull AK, Gupta N, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16, 3100 3112. (Pubitemid 35424196)
80. Gao M, Li G, McCombie WR Quiros CF (2005) Comparative analysis of a transposon-rich Brassica oleracea BAC clone with its corresponding sequence in A. thaliana. Theor Appl Genet 111, 949 955. (Pubitemid 41473392)
81. Bak S, Nielsen HL Halkier BA (1998) The presence of CYP79 homologues in glucosinolate-producing plants show evolutionary conservation of the enzymes in the conversion of amino acid to aldoxime in the biosynthesis of cyanogenic glucosides and glucosinolates. Plant Mol Biol 38, 725 734. (Pubitemid 29053611)
82. Naur P, Hansen CH, Bak S, Hansen BG, Jensen NB, Nielsen HL Halkier BA (2003) CYP79B1 from Sinapis alba converts tryptophan to indole-3-acetaldoxime. Arch Biochem Biophys 409, 235 241. (Pubitemid 36042921)